Regional-Scale Migrations and Habitat Use of Juvenile Lemon Sharks (Negaprion brevirostris) in the US South Atlantic

Abstract

Resolving the geographic extent and timing of coastal shark migrations, as well as their environmental cues, is essential for refining shark management strategies in anticipation of increasing anthropogenic stressors to coastal ecosystems. We employed a regional-scale passive acoustic telemetry array encompassing 300 km of the east Florida coast to assess what factors influence site fidelity of juvenile lemon sharks (Negaprion brevirostris) to an exposed coastal nursery at Cape Canaveral, and to document the timing and rate of their seasonal migrations. Movements of 54 juvenile lemon sharks were monitored for three years with individuals tracked for up to 751 days. While most sharks demonstrated site fidelity to the Cape Canaveral region December through February under typical winter water temperatures, historically extreme declines in ocean temperature were accompanied by rapid and often temporary, southward displacements of up to 190 km along the Florida east coast. From late February through April each year, most sharks initiated a northward migration at speeds of up to 64 km day(-1) with several individuals then detected in compatible estuarine telemetry arrays in Georgia and South Carolina up to 472 km from release locations. Nineteen sharks returned for a second or even third consecutive winter, thus demonstrating strong seasonal philopatry to the Cape Canaveral region. The long distance movements and habitat associations of immature lemon sharks along the US southeast coast contrast sharply with the natal site fidelity observed in this species at other sites in the western Atlantic Ocean. These findings validate the existing multi-state management strategies now in place. Results also affirm the value of collaborative passive arrays for resolving seasonal movements and habitat preferences of migratory coastal shark species not easily studied with other tagging techniques.

Full text

Regional-Scale Migrations and Habitat Use of Juvenile
Lemon Sharks (
Negaprion brevirostris
) in the US South
Atlantic
Eric A. Reyier
1
*, Bryan R. Franks
2
, Demian D. Chapman
3
, Douglas M. Scheidt
1
, Eric D. Stolen
1
,
Samuel H. Gruber
4
1Kennedy Space Center Ecological Program and InoMedic Health Applications, Kennedy Space Center, Florida, United States of America, 2Department of Biology, Florida
Southern College, Lakeland, Florida, United States of America, 3Institute for Ocean Conservation Science, Stony Brook University, Stony Brook, New York, United States of
America, 4Bimini Biological Field Station, Bimini, Bahamas
Abstract
Resolving the geographic extent and timing of coastal shark migrations, as well as their environmental cues, is essential for
refining shark management strategies in anticipation of increasing anthropogenic stressors to coastal ecosystems. We
employed a regional-scale passive acoustic telemetry array encompassing 300 km of the east Florida coast to assess what
factors influence site fidelity of juvenile lemon sharks (Negaprion brevirostris) to an exposed coastal nursery at Cape
Canaveral, and to document the timing and rate of their seasonal migrations. Movements of 54 juvenile lemon sharks were
monitored for three years with individuals tracked for up to 751 days. While most sharks demonstrated site fidelity to the
Cape Canaveral region December through February under typical winter water temperatures, historically extreme declines
in ocean temperature were accompanied by rapid and often temporary, southward displacements of up to 190 km along
the Florida east coast. From late February through April each year, most sharks initiated a northward migration at speeds of
up to 64 km day
21
with several individuals then detected in compatible estuarine telemetry arrays in Georgia and South
Carolina up to 472 km from release locations. Nineteen sharks returned for a second or even third consecutive winter, thus
demonstrating strong seasonal philopatry to the Cape Canaveral region. The long distance movements and habitat
associations of immature lemon sharks along the US southeast coast contrast sharply with the natal site fidelity observed in
this species at other sites in the western Atlantic Ocean. These findings validate the existing multi-state management
strategies now in place. Results also affirm the value of collaborative passive arrays for resolving seasonal movements and
habitat preferences of migratory coastal shark species not easily studied with other tagging techniques.
Citation: Reyier EA, Franks BR, Chapman DD, Scheidt DM, Stolen ED, et al. (2014) Regional-Scale Migrations and Habitat Use of Juvenile Lemon Sharks (Negaprion
brevirostris) in the US South Atlantic. PLoS ONE 9(2): e88470. doi:10.1371/journal.pone.0088470
Editor: Stefano Mariani, School of Environment & Life Sciences, University of Salford, United Kingdom
Received August 4, 2013; Accepted January 7, 2014; Published February 26, 2014
Copyright: ß2014 Reyier et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits
unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Funding: Funding provided by the Henry Foundation, Busch-Gardens & Sea World Conservation Fund, Swiss Shark Foundation, Bimini Biological Field Station,
and Kennedy Space Center Medical and Environmental Support Contract. The funders had no role in study design, data collection and analysis, decision to
publish, or preparation of the manuscript.
Competing Interests: The authors have declared that no competing interests exist.
* E-mail: eric.a.reyier@nasa.gov
Introduction
It is now widely recognized that as a group, sharks are unusually
susceptible to overfishing, relative to most other marine fishes, due
to their slow growth, late age of maturation, and low fecundity
[1,2]. However, management of shark stocks is further complicat-
ed by a growing realization that many species undertake seasonal
migrations spanning hundreds or thousands of kilometers in which
they transit through jurisdictions with incongruous fishing
regulations and enforcement strategies [3,4]. Prudent manage-
ment in a given area can be largely negated by unsustainable
harvest or habitat degradation in other portions of a species range.
Better understanding the geographic scale, directionality, and
timing of shark migrations will help guide shark conservation
efforts in coming decades as oceans are further stressed by habitat
loss and ever-growing human dependence on marine resources.
Specifically, migration data can be used to resolve stock
boundaries, refine fishing seasons and catch quotas, limit shark
bycatch, identify high value habitats (such as Habitat Areas of
Particular Concern in US waters), and establish time-area closures
or marine reserves [5].
The migrations of coastal shark species are often closely coupled
with seasonal variations in water temperature [6–8]. These
migrations appear to be adaptations to stay within a preferred
temperature range, exploit seasonally productive foraging
grounds, utilize optimal mating and parturition sites, or a
combination thereof. Along the US Atlantic and Gulf coasts,
fishery landings and field surveys demonstrate that most coastal
sharks become more abundant in northern and inshore portions of
their range as waters warm in spring [9–15]. Females use
nearshore waters and estuaries as pupping grounds where
neonates remain through summer, presumably taking advantage
of high prey availability and reduced predation [16]. By fall,
individuals again shift southward and/or offshore. Yet even in this
region where shark behavior has been a priority research focus for
several decades, migrations have not been resolved in detail for
PLOS ONE | www.plosone.org 1 February 2014 | Volume 9 | Issue 2 | e88470

most species due to the difficulties of following individual animals
as they travel long distances through open water.
Passive acoustic telemetry is steadily gaining favor as an
approach for resolving the detailed movements of fishes, including
sharks, in estuarine and coastal settings [17]. Passive telemetry
utilizes an array of submerged acoustic receivers deployed to
autonomously record the presence of fish carrying acoustic
transmitters. Individual animals can therefore be tracked for
intervals much longer than is possible with manual telemetry
where movements are recorded with a mobile (usually boat-based)
receiver. One limitation, however, is that detections are only
obtained when animals pass within a few hundred meters of a
receiver. Consequently, a large percentage of passive telemetry
studies of sharks to date [18–24], have occurred at insular
locations or targeted reef-associated species where site fidelity is
expected to be high. Studies of migratory shark species in
continental settings [25–28] are often more challenging and
generally yield data on individual animals for days to months, and
encompass small sections of coastline. Theoretically, however,
passive arrays are readily up-scalable so as to be suitable for
resolving multi-year, regional-scale migrations and habitat associ-
ations in the coastal realm. Such efforts are arguably of greater
management value since they better identify natural and
anthropogenic risks facing long-lived marine species including
sharks.
The life history of the lemon shark (Negaprion brevirostris) has
received considerable scrutiny compared with most coastal sharks.
Not only is it widely distributed throughout the western Atlantic
from North Carolina to Brazil, the Gulf of Mexico, Caribbean
Sea, and tropical eastern Atlantic and eastern Pacific, it is an apex
predator in several habitats including turbid estuaries, seagrass
beds, mangroves, and coral reefs [29,30]. Moreover, the lemon
shark exhibits life history traits that leave it prone to overfishing.
They grow slowly, only reaching sexual maturity when 225–
240 cm total length and 11–13 years of age [31]. Fecundity is also
low with females producing only 4–18 offspring every other year
[32]. Like many large sharks, the species has been heavily fished
throughout its range, is currently listed by the IUCN as a near-
threatened species, and is the subject of growing management
concern.
Studies of the lemon shark using mark-recapture, acoustic
telemetry, and genetic techniques in the Bahamas [33–37], south
Florida [38], Caribbean [39], and Brazil [24,40,41] demonstrate
that juveniles maintain fidelity to their natal nurseries for several
years, have home ranges that expand gradually with age, and show
little tendency for long distance dispersal until they approach
adulthood. However, recent findings from the US southeast coast
suggest a very different strategy with young lemon sharks forming
high density aggregations each winter in the surf zone at Cape
Canaveral, Florida, with evidence of a northward spring migration
as far as North Carolina [42]. Adult lemon sharks in the region
exhibit a similar migratory behavior but with winter aggregations
occurring near Jupiter, Florida [43], 170 km south of Cape
Canaveral. We argue here that better understanding details of
these aggregations and migration patterns is necessary to guide
long-term management of the species in the US South Atlantic
region. Therefore, the specific objectives of this study were to: (1)
use a collaborative regional-scale passive acoustic array to resolve
the degree of site fidelity of juvenile lemon sharks to Cape
Canaveral, and (2) document the timing, rate, destinations, and
temperatures associated with their seasonal migrations.
Materials and Methods
Ethics Statement
Lemon shark collection and handling was performed in
accordance with a State of Florida Special Activity License
(permit SAL-09-512-S) and the study was specifically approved by
the Kennedy Space Center Institutional Animal Care & Use
Committee (permit GRD-06-049).
Study Area
Tagging of juvenile lemon sharks was conducted at Cape
Canaveral, east-central Florida (28.5uN, Fig. 1) from the beaches
of Cape Canaveral Air Force Station and NASA’s Kennedy Space
Center. The shoreline here is among the most pristine of the
Florida Atlantic coast with no residential or commercial develop-
ment. Habitat disturbance is limited to space launch infrastructure
set back from the beach several hundred meters. Due to security
concerns associated with launch activities, public beach access has
been prohibited along 45 km of this coast since the mid-1950s
although vessel-based activities (including fishing) are permitted.
Nearshore waters are characterized by the expansive Southeast
and Chester Shoals (minimum depth 1–3 m), with adjacent waters
reaching 15 m. Bottom sediments are a mosaic of sand, shell, and
mud with little hard-bottom substrate near the beach [44]. The
shoreline exhibits longshore troughs that are partially sheltered
from the surf zone by parallel sandbars. Juvenile lemon sharks up
to 2 m long commonly aggregate within these troughs [42]. The
Indian River Lagoon system lies directly inland of the study site,
however the nearest ocean inlets are Ponce de Leon Inlet (60 km
north) and Sebastian Inlet (62 km south) as well as a small lock
system in nearby Port Canaveral. Salinity remains roughly 35 psu
year-round and tides have an amplitude of ,1 m. The Canaveral
region is a recognized climatic transition zone between warm-
temperate and sub-tropical biogeographic realms [45]. Winter
water temperatures remain above 15uC most years, however
periodic cold fronts can induce brief but rapid declines in coastal
water temperature.
Shark Tagging
A total of 54 juvenile lemon sharks were collected from two
recurring aggregation sites at Cape Canaveral (Fig. 1) over three
successive fall-winter periods from 2008 to 2010. The number of
sharks using each site occasionally exceeds several hundred
individuals. All animals were collected from shore using a 3.7 m
radius monofilament cast net. After capture, sharks were
transferred to a 125-liter tank where they were placed ventral
side up. The inverted position induced tonic immobility, after
which a 25 mm incision was made parallel to the ventral midline
and anterior to the cloaca. A coded acoustic transmitter was
inserted into the peritoneal cavity and the incision was then closed
with 2–4 absorbable sutures (Look
TM
Polysyn) and cyanoacrylate
adhesive (Vetbond
TM
, 3 M Corporation). In the first year, all
sharks were fitted with Vemco V9-2H tags (5 g in air, 180 sec.
nominal delay, ,270 day battery life). In subsequent years, larger
Vemco V16-6H tags (34 g in air, 90 sec. nominal delay, 6.4 year
battery life) were used. Sharks were also marked with external dart
tags offering a reward in case of angler recapture and then released
on site. Total time from capture to release was usually 10–15
minutes.
Florida Atlantic Coast Telemetry (FACT) Array
Movements of tagged sharks were monitored via the Florida
Atlantic Coast Telemetry (FACT) Array, a regional-scale passive
acoustic array maintained by several marine research organizations.
Coastal Migrations of Juvenile Lemon Sharks
PLOS ONE | www.plosone.org 2 February 2014 | Volume 9 | Issue 2 | e88470

During this study, the FACT Array consisted of 160–180 acoustic
receivers (Vemco VR2 and VR2W) deployed over 300 km of the
Florida east coast from West Palm Beach (26.5uN) to Ponce de
Leon Inlet (29.1uN; Fig. 1). FACT monitored multiple habitats
including beaches and nearshore reefs/wrecks in the open Atlantic
Ocean as well as estuarine waters of the adjacent Indian River
Lagoon. Special attention was taken to anchor receivers at
migratory chokepoints including all ocean inlets as well as natural
constrictions, causeway channels, and river mouths. In addition to
FACT, several other compatible passive acoustic arrays were
deployed in the US South Atlantic. Most notably, an expansive
array was established in estuarine and riverine waters of Georgia,
South Carolina, and North Carolina by January 2011, during the
third year of this study. Arrays were also located at various locations
in the Florida Keys, Bahamas, and ChesapeakeBay for the duration
of this study.
At Cape Canaveral, the number of FACT receivers (referred to
herein as the Canaveral Array) was expanded each winter (Fig. 1).
In December 2008, five ‘‘nearshore’’ receivers were deployed
250 m off the beach at a large lemon shark aggregation site south
of Cape Canaveral. In December 2009, an additional ‘‘offshore’’
row of five receivers was installed 1250 m from the beach at this
same site. Finally, in December 2010, four additional receivers
were added just north of Cape Canaveral near a second
Figure 1. Passive acoustic tracking of lemon sharks in the US South Atlantic region. A) Overall study region including locations of all
lemon shark acoustic detections (green circles) and historic angler recaptures (red circles) from sharks released at Cape Canaveral. B) Map of the full
FACT Array including all passive acoustic receivers (yellow dots). C) Close-up of the Canaveral Array including locations of two important lemon shark
aggregation sites. Nearshore receivers are numbered 1–3 which correspond to the year of the study they were deployed.
doi:10.1371/journal.pone.0088470.g001
Coastal Migrations of Juvenile Lemon Sharks
PLOS ONE | www.plosone.org 3 February 2014 | Volume 9 | Issue 2 | e88470

aggregation site, bringing the total local receiver count to 14.
Mean depth of nearshore and offshore stations were 3.7 and
6.7 m, respectively. All receivers were bracketed to large sand
screws and downloaded using SCUBA at six-month intervals.
Daily water temperature (uC) and wave height (m) within the
Canaveral Array was obtained from NOAA buoy #41113 moored
5 km east of Port Canaveral. Water temperature was also
measured using temperature recorders (HOBO
TM
loggers, Onset
Corporation) attached to receivers at Ponce de Leon Inlet, St.
Lucie Inlet, and Jupiter Inlet. When sharks were detected at
nearshore locations lacking loggers, surface water temperature was
estimated using NOAA AVHRR satellite imagery (available at
http://marine.rutgers.edu/mrs/sat_data). Air temperature data
from 1901–2011, used to provide historic context as to the relative
severity of winter temperatures experienced at Cape Canaveral
during the study, was obtained from the nearby Titusville National
Climatic Data Center Station #088942. The relationship between
air and water temperature at Cape Canaveral was explored using
Spearman’s rank correlation for all 984 days of the study when
both values were available.
Acoustic Array Performance
Assessing the performance of Canaveral Array receivers over a
broad spectrum of ocean conditions was important given that
lemon sharks frequent the surf zone where wave action may
hinder transmitter detection. The large study area made it
impractical to quantify detection distances throughout the entire
array. We instead deployed a range-test transmitter with a 3-min
fixed interval at a single location for 162 continuous days to gauge
detection rates in relation to changing habitat conditions. This
transmitter, which had a signal strength (160 dB) identical to that
used in most sharks, was deployed on a small rod midway between
a nearshore and offshore station (depth 4.2 and 8.5 m, respec-
tively). The transmitter was thus 750 m from the shore and 500 m
away from each receiver. We tested daily detection probability of
this transmitter as a function of water depth (shallow vs. deep
receiver), daily wave height, and daily water temperature, using a
limited set of nested generalized least squares models [46] within
the nlme package [47] of R. To account for potential serial
autocorrelation between successive days, we investigated models
incorporating simple autoregressive correlation structures ARMA
and AR1. Because variance in daily detection rate appeared to
differ between depths, we also considered models which allowed
for this difference in the variance structure. Once we had chosen
the best correlation and variance structure, we used model
selection based on adjusted Akaike Information Criteria (AIC
c
)
[48] to compare the full model with both interaction terms to all
simpler models (i.e., one or more terms removed).
Shark Habitat Use and Movement Analyses
Analyses of shark movements were constrained to data collected
from December 2008 through December 2011 (37 months). To
avoid inclusion of false detections resulting from code collisions
and background noise, detections at a receiver were deemed valid
only if two or more occurred within a 30-min period for a given
shark unless detections for that individual were also recorded at a
receiver ,5 km away on the same date. A scatterplot was created
to graphically depict individual lemon shark position along six pre-
defined regions of the SE US coastline including: (1) coastal waters
at Cape Canaveral (14 FACT stations), (2) southeast Florida from
Sebastian Inlet to West Palm Beach (,50 FACT stations), (3)
Ponce de Leon Inlet (4 FACT stations), (4) estuarine waters of the
Indian River Lagoon (,110 FACT stations), as well as in passive
arrays in (5) Georgia, and (6) South Carolina.
Traditional measures of animal home range size (e.g., kernel
density estimates) derived from passive receivers in the open ocean
are likely to be misleading. We instead sought to identify
individual-based and environmental variables that helped predict
lemon shark presence at Cape Canaveral by developing a series of
72 a priori candidate logistic regression-type generalized linear
models [49].The support for each ‘‘residency model’’ was
measured by its AIC
c
value [48]. Our binomial response variable
was the daily presence/absence of an individual shark anywhere
within the Canaveral Array (not detections at specific receivers).
Individual-based explanatory variables considered were shark sex,
log-transformed size at capture, size class (large vs. small), and days
at liberty. We also considered days at liberty as a categorical
variable with four levels to explore the scale of this effect on shark
detection probability. Environmental variables considered includ-
ed water temperature (uC), the magnitude of water temperature
change over the previous 3, 7, 14, and 30-day intervals (termed
D3temp, D7temp, D14temp, D30temp), day length (hours), wave
height (m), and month of year. Water temperature and day length
were highly correlated and thus never included in the same model.
Individual sharks were considered a random effect to account for
any individual heterogeneity. Study Year was included as a
random effect since the expanding array footprint each winter
resulted in growing detection probability through time. Month
crossed with year was considered a random effect to account for
temporal patterns not explained by any fixed effects. Sharks
present at Cape Canaveral for less than one week (n = 5) provided
limited information and were not included.
To account for potential serial autocorrelation in daily detection
probability, we included state dependence and time series
approaches [50]. Specifically, we created six state dependence
variables which coded for whether or not an individual shark was
detected at Cape Canaveral over the previous 1–6 days. We then
considered six state dependence models which included the first
order through sixth order autocorrelation terms added to the full
model (e.g., 1 day lag +2 day lag). We used AIC
c
to decide which
state dependence model had the best support. We also considered
time series models which incorporated the serial autocorrelation
structure directly into the generalized linear mixed effects models,
using function glmmPQL from the MASS package in R version
2.14.1 [51]. Because these models were fit using quasi-likelihood
methods, we could not use this formulation directly in model
selection; instead they were used to evaluate the use of state
dependence variables to address the serial autocorrelation. Once
we decided on the optimal random effects and state dependence
structure, we fit all 72 candidate residency models with this
structure using the lme4 package [52] in R version 2.14.1 [51].
In addition to residency, we examined depth preferences of
lemon sharks in the Canaveral Array by comparing the
distribution of detections on the nearshore receiver row vs.
offshore receiver row using a x
2
test. Further, to explore whether
shark detections varied across the day as a result of onshore-
offshore movements, time of each detection was rounded to the
nearest hour and the resulting distribution was also explored using
ax
2
test with the null hypothesis being equal detections
throughout a diel cycle. Only data collected after November
2009, after which equal numbers of receivers were deployed in
each row, were included.
To provide a range for lemon shark migration speeds along the
coastline, rate of movement was calculated for all occasions when
sharks transitioned between our six pre-defined coastal regions
(e.g., Cape Canaveral, Ponce Inlet, SE Florida). These movements
exceeded 50 km in all instances. Rates were noted as km day
21
,
and in body lengths sec
21
for events which occurred within six
Coastal Migrations of Juvenile Lemon Sharks
PLOS ONE | www.plosone.org 4 February 2014 | Volume 9 | Issue 2 | e88470

months of shark tagging. Distance was measured as the straight-
line distance through water between receivers. We considered
movements from Cape Canaveral to either Ponce de Leon Inlet
(north) or the Sebastian Inlet-West Palm Beach region (south) as
providing truest estimates of migration rates. These migrations
follow a relatively linear coastline and all tidal inlets were
monitored with acoustic receivers, allowing us to account for
any excursions into the Indian River Lagoon. Differences in
swimming speed between direction (north vs. south) and sex were
compared using Student’s t-tests.
Results
A total of 54 juvenile lemon sharks (27 males, 27 females) were
tagged, most during one of three successive fall-winter seasons:
December 2008 (n = 9), December 2009-January 2010 (n = 23),
and November 2010-March 2011 (n = 20) although transmitters
returned by anglers were implanted in new sharks during June
2010 (n = 1) and April 2011 (n = 1; Table 1). Captured sharks
ranged in size from 610 to 1430 mm fork length (FL) with a mean
of 840 mm FL. Shark size was similar across years (ANOVA,
F
2,51
= 0.84, P= 0.44) and between sexes (Wilcoxon Rank Sum
Test, W = 376.5, P= 0.84).
Acoustic Array Performance
The performance trial of the Canaveral Array ran for 162 days
with an overall daily detection rate of a range test transmitter
deployed near the surf zone being 64.2% from a distance of 500
meters. Performance varied markedly through time with daily
detection rates ranging from 0.4–95.3%. The best supported
model had main effects for both wave height and temperature (P
,0.001; see Table S1 for model details). As wave height increased,
tag detection rates decreased, and as water temperature increased,
tag detection rates increased. Water depth was not a significant
factor in this setting with the nearshore (4.2 m deep) and offshore
(8.5 m deep) receivers performing similarly with daily detection
rates of 64.5% and 63.9%, respectively.
Shark Residency and Habitat Use at Cape Canaveral
Juvenile lemon sharks were followed for 0.5–751 days with a
mean (61 SD) of 217 (6226) days (Table 1; see Table S2 for
details on individual sharks). A total of 41,869 position detections
were recorded from December 2008 through December 2011 and
all 54 sharks were detected in the Canaveral Array at some point.
With the exception of early 2010 (see migration details below),
tagged sharks generally demonstrated site fidelity to the Cape
Canaveral region from late November through late February with
few detections elsewhere along the southeastern US coast (Fig. 2).
While no shark was detected at Cape Canaveral more than 2600
times, many sharks were recorded here on a near-daily basis for
several weeks duration while others were detected more sporad-
ically. The installation of receivers at a second (more northerly)
aggregation site in late 2010 demonstrated that individual sharks
regularly moved between aggregations and thus commonly spent
time beyond the bounds of the initial Canaveral Array footprint.
The best-supported residency model (AIC
c
weight = 0.87;
Table 2) determined that day length, categorical days at liberty,
and the magnitude of water temperature change over the previous
three days (i.e., D3temp) helped predict daily detection probability
of lemon sharks at Cape Canaveral. In this model, day length had
the greatest (negative) effect size with individuals most likely to be
present on the shortest days of the year (Table 3; Fig.3). D3temp
also had a negative effect meaning that cooling trends resulted in
higher predicted probability of shark detection, while warming
trends resulted in lower predicted probability. The effect size for
days at liberty was also negative meaning that sharks were more
often detected on dates nearer their release date. Neither sex nor
size helped predict lemon shark presence at Canaveral. Further,
an effect of wave height on detection probability, shown during
range testing to reduce receiver performance, was not supported,
confirming that sharks were detected at least sporadically when
present in the Canaveral Array, even during periods of high seas.
The state dependence variables showed a strong positive
correlation between the probability of detection for the 1 day
lag, and weaker effects for the 2–4 day lags (Fig. 3). Measures of
autocorrelation for Days 1–4 (0.23, 0.05, 0.05, 0.03) agreed well
with those estimated by the time series model (0.32, 0.1, 0.03,
0.01). Both methods produced similar parameter estimates,
increasing confidence in state dependence modeling for evaluating
the effects of covariates on shark detections.
Lemon sharks were strongly associated with the shoreline when
at Cape Canaveral. Nearly 82% of all detections were recorded by
the nearshore receiver row, more than expected by chance if
sharks used both depths equally (x
2
= 9820, df = 1, P,0.001; Fig.
4). Only eight of 42 animals were more commonly detected at
offshore receivers, all of which spent little time at Cape Canaveral
relative to other sharks. Further, detections were not evenly
distributed across the diel period with peak detections occurring at
night between 1900–0600 (x
2
= 5289, df = 23, P,0.001).
Direction, Timing, and Rate of Coastal Migrations
Of the 54 lemon sharks tagged, 41 were detected away from
Cape Canaveral. These individuals were recorded on 62
additional FACT stations from Palm Beach Inlet (26.8uN) to
Ponce de Leon Inlet (29.1uN) at various times during the study
(Figs. 1,2). Sharks also entered other passive arrays in Ossabaw
Sound (n = 3) and Savannah River (n = 1), Georgia (32.0uN), and
Charleston Harbor (n = 2), South Carolina (32.8uN). The
minimum linear distance between the northernmost and south-
ernmost detection was 663 km but over 770 km when following
the coast. On average, sharks were detected on 9.1 receiver
stations with individual animals visiting as many as 27 stations.
Locational information was also provided via angler recaptures at
Jupiter Inlet (170 km south of release site) and Ponce de Leon
Inlet, Florida (88 km north of release site), and Little St. Simons
Island, Georgia (323 km north of release site).
Nearshore water temperature at Cape Canaveral ranged from
11–30uC and averaged 23.3uC across the study (Fig. 2). Lemon
sharks were detected throughout this range (12–30uC) but .70%
of detections occurred at temperatures between 15–20uC (Fig.
5).Winter water temperature, averaged from December through
March, differed across years (One-Way ANOVA, F = 17.85, P
,0.001) as a result of severe declines in January-March 2010 and
again in December 2010. This atypical variability was accompa-
nied by notable differences in shark migration patterns across the
three winters of this study. While extensive records of water
temperature are unavailable, local water and air temperatures
were strongly correlated (Spearman’s rank correlation, r
s
= 0.92,
df = 982, P,0.001) suggesting that air temperature serves as a
good proxy for the relative severity of winters at Cape Canaveral.
The winter of 2008–2009 was moderate with air temperature
averaging 17.2uC, (near the long term mean of 17.0 uC) and water
temperature ranging from 16–23uC. The nine lemon sharks
released in December 2008 were detected locally for 3–106 days
with the last two sharks recorded on 5 March (Fig. 2). Five of these
sharks were later detected at Ponce de Leon Inlet between 27
February and 22 March 2009 confirming a northward spring
migration for these individuals (Table 4). Sharks were not detected
Coastal Migrations of Juvenile Lemon Sharks
PLOS ONE | www.plosone.org 5 February 2014 | Volume 9 | Issue 2 | e88470

elsewhere until sharks #8 and 9 returned to Cape Canaveral on
24 November and 9 December 2009, respectively.
The 23 lemon sharks released in the second winter of the study
were also initially detected only in the Canaveral Array (Fig. 2). By
early January 2010, however, several reinforcing cold fronts swept
across peninsular Florida resulting in one of the most severe cold
weather events on record at Cape Canaveral. Daily air temper-
ature from 2–13 January averaged from 2–10uC, resulting in
significant cold-induced mortalities of coastal fishes with tropical
affinities (Reyier, personal observation). Moreover, temperatures
remained below average for several weeks; winter air temperature
averaged only 14.7uC, the sixth coldest on record since 1901.
Water temperature in the Canaveral Array reached a minimum of
11uC on 11 January and generally remained below 16uC through
mid-March.
This rapid drop in ocean temperature was accompanied by the
exodus of all 23 tagged sharks from the Canaveral Array with the
last individual (#19) detected on 10 January at a water
temperature of 12.0uC. Fifteen sharks made confirmed southward
migrations along the coast and were recorded at multiple FACT
stations from Sebastian Inlet to West Palm Beach, 62–191 km
south of Cape Canaveral. Water temperature in this region was
typically 3–6uC warmer than Cape Canaveral due to the
moderating influence of the Florida Current which diverges from
the Florida east coast near Jupiter. Migrating sharks were always
detected singly, a behavior observed consistently across the study.
Sharks generally followed the coastline with 13 individuals
detected at ocean inlets although one shark was detected 10 km
offshore in water 22 m deep. Shark #25 reached West Palm
Beach in three days, a rate of 59 km day
21
and several others
moved at .40 km day
21
. Five animals (#22–25, 31) passed by
receivers at the south end of FACT at this time and never
returned. Other sharks were simply never detected again after
leaving the Canaveral Array in early January. Notably, shark #12
actually moved north to Ponce de Leon Inlet in late January (water
temperature of 13.6uC) before returning to Cape Canaveral in
early February. Eight of 23 tagged sharks returned to the
Canaveral Array from 29 January to 8 April. Five of these
individuals (#10, 11, 13, 20, 29) were then recorded swimming
north past Ponce de Leon Inlet from 3 – 26 April (later in the
spring than observed in 2009) with shark #10 subsequently
harvested nearby. Like the previous year, the location of these four
remaining animals from late spring through fall was undetermined
but all four returned to Cape Canaveral between 14 November
and 6 December 2010. A single shark (#33) tagged in spring
remained within the Canaveral Array throughout the summer
2010 and summer 2011 as well, confirming that at least some
juvenile lemon sharks at Cape Canaveral do not undertake
northward spring migrations.
December 2010 was also unusually cold; local air temperature
averaged 10.8uC, the second coldest December on record since
1901. This event also resulted in mortality of tropical fish species
but water temperature was less severe than the previous winter,
falling to a low of 14.1uC in late December before returning to
more seasonable conditions by early January. Twelve lemon
sharks (five released the previous year and seven new releases) were
present in the Canaveral Array in early December 2010. While
several animals disappeared as water temperature declined, only
two (#35, 39) were detected elsewhere in FACT, both near St.
Lucie Inlet, 140 km south, and all sharks returned to the
Canaveral Array by early January. Further, the 14 animals
released later in the winter were never detected south of Cape
Canaveral. As in previous years, sharks left the Canaveral Array in
spring with 20 individuals recorded at Ponce de Leon Inlet from
17 March to 17 May 2011 (Table 4).
Newly established passive arrays in coastal Georgia and South
Carolina provided the first details regarding the destinations and
habitat use of north-migrating lemon sharks from spring through
fall. Shark #41 was recorded at the mouth of the Savannah River
on 31 March. Sharks #45 and 50 were detected within Charleston
Harbor on 4 April and 4 May, respectively. Shark #38 was
captured and released at Little St. Simon Island, Georgia, on 10
May, and most notably, shark #43 was detected up to 10 km
inside Ossabaw Sound, Georgia, on 33 separate dates from May -
October 2011, providing a near-complete record of this shark’s
location since its release. Despite this extensive northward
migration of lemon sharks in spring, 18 of the tagged individuals
present at Cape Canaveral during fall-winter of 2010–2011
returned to Cape Canaveral by December 2011 including three
of the five sharks (#38, 43, 45) detected in Georgia and South
Carolina.
In total, we recorded 72 instances by 40 lemon sharks where
individuals travelled .50 km between receivers. The longest
movements (420 km) were observed in two sharks swimming
between Ponce de Leon Inlet and Charleston Harbor. Rate of
movement ranged from 0.3–63.5 km day
21
(mean 18.6 km
Table 1. Summary information for all 54 lemon sharks tagged at Cape Canaveral.
Year of Release
Winter 2008–2009 Winter 2009–2010 Winter 2010–2011 Total
Sharks Released 9 23 22 54
Sex Ratio (F:M) 5:4 11:12 11:11 27:27
Size (mm fork length; mean 6SD) 8676143 7766162 8966211 8406186
Days at Liberty (mean 6SD) 1486141 2366300 2246156 2176226
Position Detections (mean 6SD) 5966715 102261838 5916721 77561316
Receiver Stations Visited 4.061.1 11.366.2 9.064.3 9.165.5
Max. Observed Displacement (km)
North (mean 6SD) 47643 29639 1316156 746114
South (mean 6SD) 261 107680 24643 56674
Days at liberty equals the number of days between release and last detection. Maximum displacement means the farthest known detection north and south of release
point.
doi:10.1371/journal.pone.0088470.t001
Coastal Migrations of Juvenile Lemon Sharks
PLOS ONE | www.plosone.org 6 February 2014 | Volume 9 | Issue 2 | e88470

Figure 2. Lemon shark migrations. A) Acoustic detections of all 54 lemon sharks through time, and B) associated nearshore water temperature at
Cape Canaveral.
doi:10.1371/journal.pone.0088470.g002
Coastal Migrations of Juvenile Lemon Sharks
PLOS ONE | www.plosone.org 7 February 2014 | Volume 9 | Issue 2 | e88470

day
21
). In cases when migrations occurred within six months of
release (i.e., when shark size was known), movement rate measured
as body lengths sec
21
ranged from 0.02–1.1 (mean 0.27, n = 59).
And when considering only migrations along the linear Florida
east coast, rates were similar, averaging 18.9 km day
21
(n = 66)
and 0.27 bl sec
21
(n = 53), respectively. Southerly and northerly
migrations occurred at similar speeds (t-test, t = –1.384, df = 43.6,
P= 0.17), were similar across sexes (t-test, t = –0.349, df = 47.1,
P= 0.72) and were not related to size at capture (Spearman’s rank
correlation, r
s
= 0.02, P= 0.88).
Regional Habitat Use
Tagged lemon sharks were detected within every major habitat
monitored by the FACT Array. While all 54 sharks (73% of all
detections) were recorded in nearshore Atlantic waters, 40 sharks
(19% of detections) were also recorded at tidal inlets including
Ponce de Leon (n = 30), Sebastian (n = 2), Ft. Pierce (n = 9), St.
Lucie (n = 7), and Jupiter Inlets (n = 6) as well as nearby Port
Canaveral (n = 2). Nine animals (7% of detections) penetrated
.5 km into estuarine waters of the Indian River Lagoon and one
shark (1% of detections) was recorded 7 km up the Loxahatchee
River near Jupiter Inlet although salinity at this site was not
available. Shark #21 spent $166 days in the estuary and moved
106 km north from Sebastian Inlet before returning south and
offshore, spending more time and moving farther up-estuary than
any other tagged individual. With the exception of Ponce de Leon
Inlet, which lies along the annual migration route, use of inlet and
estuarine habitats within the FACT Array occurred almost
exclusively during early 2010 as sharks moved south from Cape
Canaveral in association with rapidly falling water temperature.
Discussion
In this study, we utilized a collaborative passive acoustic array to
document regional-scale migrations and habitat associations of
juvenile lemon sharks in the US South Atlantic for the first time.
Tagged sharks utilized at least 660 km of coastline from southeast
Florida to South Carolina with individuals tracked for up to 751
days. Our findings clearly demonstrated that: (1) immature lemon
sharks found in nearshore aggregations at Cape Canaveral
exhibited site fidelity to this region from December through
February under seasonally typical water temperatures; (2)
temperature declines below 15uC were accompanied by a rapid
but often temporary southward displacement along the Florida
east coast; and (3) in contrast to other populations studied to date,
most juvenile lemon sharks overwintering in east-central Florida
undertook an annual northward migration starting in late winter,
and spent summer in nearshore and estuarine waters of north
Florida, Georgia, and the Carolinas before returning south to east-
central Florida in fall.
Cape Canaveral as a Lemon Shark Nursery
The notion that many coastal shark species have discrete
nurseries has been widely accepted for decades with many
adopting the definition of Bass [53] who states that primary
nurseries are locations where parturition takes place and
secondary nurseries are where young reside when growing to
maturity. Huepel et al. [54] argue convincingly that this concept is
too often applied to areas where immature sharks occur in low
density or spend little time. They instead propose three testable
criteria for evaluating whether a location is indeed a shark nursery:
(1) young sharks of a given species are more abundant than in
other areas, (2) individuals use the putative nursery for extended
periods (i.e., exhibit site fidelity), and (3) the area is utilized by a
species repeatedly across years.
Our growing understanding of lemon shark life history in the
US South Atlantic suggests that nearshore waters at Cape
Canaveral merit the definition of a winter nursery for the species
even under these stricter standards, and may constitute the single
most valuable winter nursery for lemon sharks in US waters north
of the Florida Keys-Florida Bay region. While abundance was not
quantified here, tagged sharks were sampled from aggregations of
several hundred individuals, and winter densities as high as 22
sharks per shoreline km have been observed locally in recent years
[42]. To our knowledge, this aggregating behavior has not been
noted for juveniles elsewhere along the US Atlantic coast, and
immature lemon sharks are a minor component of shark surveys
elsewhere in Florida [29,55], Georgia [56], South Carolina
[57,58], and North Carolina [59]. Our findings directly address
more challenging questions regarding site fidelity and seasonal
philopatry (i.e., homing) to the Canaveral region. The FACT
Array provided strong evidence that most juvenile lemon sharks
arrived at Cape Canaveral beginning in late November, remained
through February (often longer), and utilized coastal waters south
of Cape Canaveral only when water temperature receded below
15uC. And while aggregations dissipated each spring, they
reformed the ensuing winter, as they have annually since first
encountered in 2003 [42]. Most notably, 19 of 54 tagged
individuals returned for a second or even third successive winter.
Given that mortality of young lemon sharks has been estimated at
38–65% annually [60], and that transmitters deployed the first
winter had battery life ,1 year, this rate of return appears high.
The reason(s) why lemon sharks aggregate at Cape Canaveral is
not fully understood but our data suggest that water temperature
largely underlies this phenomenon. Cape Canaveral is a climatic
transition zone where winter water temperature grades rapidly
from north to south and does not drop below 15 uC most years
[45]. This condition is partially a function of latitude, however
satellite ocean temperature imagery also suggests that the nearby
shoal complex partially deflects the predominant south-flowing
nearshore current eastward, allowing warmer north-flowing
offshore currents to intrude near the coast. On some winter days,
water temperature on either side of the shoals may differ by up to
Table 2. Ten best supported models from the 72 a priori
models relating environmental and individual covariates to
daily detection probability (DDP) of lemon sharks at Cape
Canaveral.
Model k LogL DAIC
c1
W
i
DDP ,DAL(cat) +Dtemp3d +daylength 12 –2046.5 0.0 0.87
DDP ,size +DAL(cat) +daylength 12 –2049.7 6.4 0.03
DDP ,DAL(cat) +Dtemp7d +daylength 12 –2049.8 6.6 0.03
DDP ,DAL(cat) +daylength +size +sex 13 –2048.8 6.6 0.03
DDP ,DAL(cat) +daylength 11 –2052.4 9.8 0.01
DDP ,Size(cat) +DAL(cat) +daylength 12 –2051.5 9.9 0.01
DDP ,sex +DAL(cat) +daylength 12 –2051.6 10.2 0.01
DDP ,DAL(cat) +Dtemp30d +daylength 12 –2051.7 10.5 0.00
DDP ,DAL(cat) +daylength +sex +
size(cat)
13 –2050.8 10.5 0.00
DDP ,DAL(cat) +Dtemp14d +daylength 12 –2052.1 11.1 0.00
All models include state dependence variables (e.g., 1 day lag) to account for
any effects of serial autocorrelation, and a random effect for shark and the
month by Year.
1
minimum AIC
c
= 4117.04.
doi:10.1371/journal.pone.0088470.t002
Coastal Migrations of Juvenile Lemon Sharks
PLOS ONE | www.plosone.org 8 February 2014 | Volume 9 | Issue 2 | e88470

2–3uC. In most years, therefore, the Canaveral region may simply
be the highest latitude where lemon sharks can safely overwinter
without serious repercussions to survival and growth. Since tagged
sharks returned to Canaveral as early as November when water
temperature in northeast Florida was still typically .20uC,
aggregations may be an instinctive or learned behavior, not a
direct response to ambient temperatures encountered during
southward fall migrations. The sand shoals here may also serve as
a predator refuge or productive foraging grounds. In fact,
following the conclusion of this study, the Canaveral Array was
further expanded with receivers deployed further offshore. To
date, a total of 13 juvenile lemon sharks have been detected up to
12 km from the beach (E. Reyier, unpubl. data). Finally, it is
conceivable that these juvenile aggregations were historically more
widespread in east Florida during winter but now persist only at
Cape Canaveral due to limits on public shore access and fishing
enacted for space launch security in the 1950s.
Seasonal Migrations in the US South Atlantic
The historically cold water temperature during January 2010
resulted in widespread mortality of tropical fish species throughout
peninsular Florida [61], but was fortuitous in the sense that it
allowed us to observe a broader suite of lemon shark behavior than
might be expected in a typical three year period. Like other
marine fishes, lemon sharks exposed to temperature approaching
their lower lethal limit would be subject to disruption of
neuroendocrine, metabolic, osmoregulatory, and immune func-
Table 3. Parameter estimates for the best supported state
dependence lemon shark residency model. Parameter
estimates are also provided for time series modeling for which
to compare to state-dependence approach.
State Dependence Time Series
Parameter Estimate
Std.
Error
z
value Pr(
.
IzI) Estimate
Std.
Error
Intercept –3.00 0.23 –12.87 ,2E-16 –2.25 0.22
DAL (cat 31–90) –0.46 0.16 –2.88 4.00E-03 –0.13 0.13
DAL (cat 91–180) –1.37 0.22 –6.19 6.20E-10 –1.53 0.21
DAL (cat 181+) –1.35 0.19 –7.04 1.90E-12 –1.51 0.14
Dtemp3d –0.16 0.05 –3.37 7.50E-04 –0.15 0.04
daylength –0.78 0.12 –6.34 2.20E-10 –0.69 0.07
1 day lag 1.77 0.10 17.56 ,2E-16
2 day lag 0.35 0.12 3.04 2.30E-03
3 day lag 0.41 0.12 3.46 5.50E-04
4 day lag 0.24 0.12 2.05 0.04
Random Effects
shark (SD) 0.94
year:month (SD) 0.61
doi:10.1371/journal.pone.0088470.t003
Figure 3. Nomogram depicting effect sizes for the best supported lemon shark residency model. To use the nomogram, locate the
desired level of each variable and follow the position vertically up to the Points Scale. Repeat this for all variables and add up the points, then find
that value on the Total Points Scale. Finally follow that position directly down to the Fitted Probability Scale which gives the predicted probabilityof
daily detection.
doi:10.1371/journal.pone.0088470.g003
Coastal Migrations of Juvenile Lemon Sharks
PLOS ONE | www.plosone.org 9 February 2014 | Volume 9 | Issue 2 | e88470

tions, potentially culminating in death [62]. The sudden exodus of
all tagged lemon sharks from Cape Canaveral once water reached
12uC in early 2010, and a rapid southern migration of at least 15
individuals to coastal waters moderated by the warm Florida
Current, was clearly in direct response to this unusual meteoro-
logical event. The near-complete exodus of sharks from Cape
Canaveral from February through April in all three years of the
study and the subsequent detections of 30 individuals at Ponce de
Leon Inlet (northeast Florida), Georgia, and South Carolina,
demonstrate that lemon sharks as small as 660 mm FL commonly
undertake extensive northward migrations each spring. In contrast
to southern migrations observed in early 2010, these annual
migrations may not be cued directly by water temperature. Day
length, not temperature, appeared as single most important factor
when predicting lemon shark presence at Cape Canaveral over the
long term, and many north-migrating sharks passed Ponce de
Leon Inlet when water temperature was only 16–18uC. We
suggest that growing day length in spring provides the primary
stimulus to initiate annual coastal migrations, as has also been
been suggested for sandbar sharks (Carcharhinus plumbeus)in
Chesapeake Bay [11].
The extensive migrations we observed contrast with results of
virtually every other study of lemon shark behavior and dispersal
in the Bahamas [33,35], Caribbean [39], Brazil [24], and even
south Florida [38]. Most notably, Chapman et al. [34] used
genetic techniques to conclude that dispersal of lemon sharks in
Bimini, Bahamas (only 320 km from Cape Canaveral), was very
slow; the majority of individuals up to six years old at Bimini were
locally born. Most previous studies have occurred at insular sites or
lower latitudes where seasonal migrations may be less advanta-
Figure 4. Distribution of lemon shark detections by receiver row and by hour of day. Nearshore receivers were located 250 m from the
beach while offshore receivers were 1250 m from the beach.
doi:10.1371/journal.pone.0088470.g004
Figure 5. Distribution of available water temperature at Cape Canaveral and associated percentage of lemon shark detections.
Water temperature was derived from daily means recorded December 2008 through December 2011.
doi:10.1371/journal.pone.0088470.g005
Coastal Migrations of Juvenile Lemon Sharks
PLOS ONE | www.plosone.org 10 February 2014 | Volume 9 | Issue 2 | e88470

geous because annual temperature variability is less extreme, or
because dispersal is not attempted - or not often successful - due to
high juvenile mortality in the open ocean. Regular lemon shark
migrations along the US southeast coast are presumably an
adaption which allows seasonal use of productive estuaries from
spring through early fall as temperatures allow. These migrations
also result in lower densities which may be necessary since the
condition of lemon sharks in aggregations deteriorates as winter
progresses [42], suggesting that Canaveral waters cannot sustain
such high shark numbers year-round.
The stark regional differences in lemon shark behavior and
habitat associations underscore the wisdom of tailoring manage-
ment strategies to both a species basic biology, which may vary
little over broad geographic scales, and its behavior, which varies
from site to site. Along the US east coast, lemon sharks are
currently managed as a single stock in the large coastal shark
management group [63], subject to recreational and commercial
size and catch quotas. Further, In 2010, due to mounting evidence
that lemon shark aggregating behavior made them especially
vulnerable to overfishing, the State of Florida imposed an outright,
although potentially temporary, harvest ban in state waters [43].
Given the extensive migrations we observed in individual sharks,
coupled with the spatially predictable nature of their aggregations,
this dual approach seems warranted. That said, permanent
protection of Florida’s lemon shark aggregations in both state
and federal waters (possibly through extremely stringent quotas or
time-area closures) may be the single most important step for
ensuring long-term conservation of the species in the US south
Atlantic region.
Remaining Questions
Adult lemon sharks that overwinter off Jupiter, Florida, exhibit a
similar north-south migratory pattern along the coast. Almost 60
tagged adults passed through the Canaveral Array in late spring
and several remained in the region well into summer. Female
lemon sharks give birth in spring but the apparent lack of neonates
at Cape Canaveral or adjacent estuary [42] suggests that
parturition occurs primarily north of east-central Florida; to date
these pupping areas have not been located. And while ongoing
genetic sampling has demonstrated that adults in Jupiter
aggregations are the parents of some Canaveral juveniles (D.
Chapman, unpubl. data), it remains unclear to what extent, and at
what age, the immature sharks recruit into adult aggregations
down the Florida coast. That said, this study validates the use of
collaborative passive arrays for the purposes of resolving regional-
scale migrations for managed coastal fishes not easily tracked in
detail with satellite-based techniques. As the technology becomes
more widely embraced, answers to these questions will be within
reach for lemon sharks and other coastal shark species.
Supporting Information
Table S1 Canaveral Array Performance. The best supported
generalized least squares model for the receiver performance trial
had main effects for wave height and temperature. Test distance
between transmitter and receivers was 500 m.
(DOCX)
Table S2 Detailed information for all 54 lemon sharks tagged at
Cape Canaveral. Days at Liberty equals the number of days
between date of release and date of last detection within the
acoustic array. Maximum displacement means the farthest known
detection (in km) north and south of release point. Asterisk
indicates angler capture. Stations visited includes all FACT and
non-FACT locations.
(DOCX)
Acknowledgments
The FACT Array is jointly managed by the Bimini Biological Field Station,
Florida Fish & Wildlife Conservation Commission, Florida Program for
Shark Research at the University of Florida, Florida International
University, Kennedy Space Center Ecological Program, Naval Undersea
Warfare Center, and Stony Brook University. We offer special thanks to
Carla Garreau, Russ Lowers, Karen Holloway-Adkins, Steve Kessel,
Debra Abercrombie, and Bill Parks for assistance in shark tagging and field
support. We further thank Carlton Hall (Inomedic Health Applications),
Lynne Phillips (NASA), Mike Legare (Merritt Island National Wildlife
Refuge), and Don George and Angy Chambers (Cape Canaveral Air Force
Station) for logistical support. Georgia Dept. of Natural Resources and
South Carolina Dept. of Natural Resources provided valuable data for
lemon sharks detected by acoustic receivers north of Florida. Sea surface
temperature data was used with permission of the Rutgers Coastal Ocean
Observation Laboratory.
Author Contributions
Conceived and designed the experiments: EAR BRF DDC DMS EDS
SHG. Performed the experiments: EAR BRF DDC DMS SHG. Analyzed
the data: EDS EAR. Contributed reagents/materials/analysis tools: EAR
BRF DDC. Wrote the paper: EAR EDS.
Table 4. Date and water temperature (uC) associated with lemon sharks passing by Ponce de Leon Inlet during annual migrations.
Season No. Sharks Sex (F:M) Date Range (Median) Temperature Range (Median)
Winter-Spring 2009 5 3:2 27 Feb. –22 Mar. (14 Mar.) 17.5–22.0 (19.5)
Fall 2009 0
Winter-Spring 2010 5 1:4 3 Apr. –26 Apr. (13 Apr.) 17.3–21.6 (20.0)
Fall 2010 3 0:3 9 Nov. –16 Nov. (11 Nov.) 21.0–22.2 (22.1)
Winter-Spring 2011 20 12:8 17 Mar. –7 May (23 Mar.) 16.4–22.3 (16.9)
Fall 2011 2* 1:1 1 Oct. (both sharks) 28.6
Instances where sharks made forays to/past Ponce Inlet but quickly returned to Canaveral (n =2) are excluded. *Burial of two receivers in fall 2011 limited the ability to
detect south-migrating lemon sharks passing by this area.
doi:10.1371/journal.pone.0088470.t004
Coastal Migrations of Juvenile Lemon Sharks
PLOS ONE | www.plosone.org 11 February 2014 | Volume 9 | Issue 2 | e88470

References
1. Musick JA, Burgess G, Cailliet G, Camhi M, Fordham S (2000) Management of
sharks and their relatives (Elasmobranchii). Fisheries 25: 9–13.
2. Hoenig JM, Gruber SH (1990) Life-history patterns in the elasmobranchs:
implications or fisheries management. In: Pratt HL, Gruber SH, Taniuchi T,
editors. Elasmobranchs as living resources: advances in the biology, ecology,
systematics, and the status of fisheries: NOAA/National Marine Fisheries
Service.
3. Speed CW, Field IC, Meekan MG, Bradshaw CJA (2010) Complexities of
coastal shark movements and their implications for management. Marine
Ecology Progress Series 408: 275–293.
4. Kohler NE, Casey JG, Turner PA (1998) NMFS Cooperative SharkTagging
Program, 1962–93: An Atlas of SharkTag and Recapture Data. Marine
Fisheries Review 60: 1–87.
5. Speed CW, Field IC, Meekan MG, Bradshaw CJA (2010) Complexities of
coastal shark movements and their implications for management. Marine
Ecology-Progress Series 408: 275–U305.
6. Castro JI (2011) The sharks of North America. New York: Oxford University
Press.
7. Springer S (1967) Social organization of shark populations. In: Gilbert PW, R.W
M, Rall DP, editors. Sharks, skates and rays. Baltimore, Maryland: John
Hopkins Press. pp. 149–174.
8. Schwartz FJ (2003) Sharks, skates, and rays of the Carolinas. Chapel Hill, NC:
University of North Carolina Press.
9. Castro JI (1996) Biology of the blacktip shark, Carcharhinus limbatus, off the
southeastern United States. Bulletin of Marine Science 59: 508–522.
10. Curtis TH, Adams DH, Burgess GH (2011) Seasonal Distribution and Habitat
Associations of Bull Sharks in the Indian River Lagoon, Florida: A 30-Year
Synthesis. Transactions of the American Fisheries Society 140: 1213–1226.
11. Grubbs RD, Musick JA, Conrath CL, Romine JG (2007) Long-Term
Movements, Migration, and Temporal Delineation of a Summer Nursery for
Juvenile Sandbar Sharks in the Chesapeake Bay Region. In: McCandless CT,
Kohler NE, Pratt HL, editors. Shark nursery grounds of the Gulf of Mexico and
the east coast of the United States. Bethesda, Maryland: American Fisheries
Society Symposium 50. pp. 87–107.
12. Heupel MR (2007) Exiting Terra Ceia Bay: An examination of cues stimulating
migration from a summery nursery area. In: McCandless CT, Kohler NE, Pratt
HL, editors. Shark Nursery Grounds of the Gulf of Mexico and the East Coast
Waters of the United States. Bethesda, Maryland: American Fisheries Society
Symposium 50. pp. 265–280.
13. Merson RR, Pratt HL (2001) Distribution, movements and growth of young
sandbar sharks, Carcharhinus plumbeus, in the nursery grounds of Delaware Bay.
Environmental Biology of Fishes 61: 13–24.
14. Stehlik LL (2007) Essential fish habitat source document: spiny dogfish, Squalus
acanthias, life history and habitat characteristics. Woods Hole, MA: NOAA.
15. Castro JI (1993) The biol ogy of the finetooth shark, Carcharhinus isodon.
Environmental Biology of Fishes 36: 219–232.
16. Castro JI (1993) The shark nursery of Bulls Bay, South Carolina, with a review of
the shark nurseries of the southeastern coast of the United States. Environmental
Biology of Fishes 38: 37–48.
17. Heupel MR, Semmens JM, Hobday AJ (2006) Automated acoustic tracking of
aquatic animals: scales, design and deployment of listening station arrays.
Marine and Freshwater Research 57: 1–13.
18. Papastamatiou YP, Friedlander AM, Caselle JE, Lowe CG (2010) Long-term
movement patterns and trophic ecology of blacktip reef sharks (Carcharhinus
melanopterus) at Palmyra Atoll. Journal of Experimental Marine Biology and
Ecology 386: 94–102.
19. Bond ME, Babcock EA, Pikitch EK, Abercrombie DL, Lamb NF, et al. (2012)
Reef Sharks Exhibit Site-Fidelity and Higher Relative Abundance in Marine
Reserves on the Mesoamerican Barrier Reef. PLoS One 7.
20. Chapman DD, Pikitch EK, Babcock F, Shivji MS (2005) Marine reserve design
and evaluation using automated acoustic telemetry: A case-study involving coral
reef-associated sharks in the mesoamerican Caribbean. Marine Technology
Society Journal 39: 42–55.
21. Speed CW, Meekan MG, Field IC, McMahon CR, Stevens JD, et al. (2011)
Spatial and temporal movement patterns of a multi-species coastal reef shark
aggregation. Marine Ecology Progress Series 429: 261–275.
22. Field IC, Meekan MG, Speed CW, White W, Bradshaw CJA (2011) Quantifying
movement patterns for shark conservation at remote coral atolls in the Indian
Ocean. Coral Reefs 30: 61–71.
23. Heupel MR, Simpfendorfer CA, Fitzpatrick R (2010) Large-scale movement
and reef fidelity of grey reef sharks. PLoS One 5: e9650.
24. Wetherbee BM, Gruber SH, Rosa RS (2007) Movement patterns of juvenile
lemon sharks Negaprion brevirostris within Atol das Rocas, Brazil: a nursery
characterized by tidal extremes. Marine Ecology-Progress Series 343: 283–293.
25. Heupel MR, Simpfendorfer CA (2002) Estimation of mortality of juvenile
blacktip sharks, Carcharhinus limbatus, within a nursery area using telemetry data.
Canadian Journal of Fisheries and Aquatic Sciences 59: 624–632.
26. Heupel MR, Simpfendorfer CA, Collins AB, Tyminski JP (2006) Residency and
movement patterns of bonnethead sharks, Sphyrna tiburo, in a large Florida
estuary. Environmental Biology of Fishes 76: 47–67.
27. Yeiser BG, Heupel MR, Simpfendorfer CA (2008) Occurrence, home range and
movement patterns of juvenile bull (Carcharhinus leucas) and lemon (Negaprion
brevirostris) sharks within a Florida estuary. Marine and Freshwater Research 59:
489–501.
28. Heupel MR, Yeiser BG, Collins AB, Ortega L, Simpfendorfer CA (2010) Long-
term presence and movement patterns of juvenile bull sharks, Carcharhinus leucas,
in an estuarine river system. Marine and Freshwater Research 61: 1–10.
29. Snelson FF, Williams SE (1981) Notes on the Occurrence, Distribution, and
Biology of Elasmobranch Fishes in the Indian River Lagoon System, Florida.
Estuaries 4: 110–120.
30. Morrissey JF, Gruber SH (1993) Habita t selection by juvenile lemon sharks,
Negaprion brevirostris. Environmental Biology of Fishes 38: 311–319.
31. Brown CA, Gruber SH (1988) Age assessment of the lemon shark, Negaprion
brevirostris, using tetracycline validated vertebral centra. Copeia: 747–753.
32. Feldheim KA, Gruber SH, Ashley MV (2002) The breeding biology of lemon
sharks at a tropical nursery lagoon. Proceedings of the Royal Society of London
Series B-Biological Sciences 269: 1655–1661.
33. Morrissey JF, Gruber SH (1993) Home range of juvenile lemon sharks, Negaprion
brevirostris. Copeia: 425–434.
34. Chapman DD, Babcock EA, Gruber SH, Dibattista JD, Franks BR, et al. (2009)
Long-term natal site-fidelity by immature lemon sharks (Negaprion brevirostris)ata
subtropical island. Mol Ecol 18: 3500–3507.
35. Murchie KJ, Schwager E, Cooke SJ, Danylchuk AJ, Danylchuk SE, et al. (2010)
Spatial ecology of juvenile lemon sharks (Negaprion brevirostris) in tidal creeks and
coastal waters of Eleuthera, The Bahamas. Environmental Biology of Fishes 89:
95–104.
36. Franks BR (2007) The spatial ecology and resourc e selection of juvenile lemon
sharks (Negaprion breviro stris) in their primary nu rsery areas. Philadelp hia,
Pennsylvania: Drexel University.
37. Guttridge TL, Gru ber SH, Franks BR, Kessel ST, Gledhill KS, et al. (2012)
Deep danger: intra-specific predation risk influences habitat use and aggregation
formation of juvenile lemon sharks Negaprion brevirostris. Marine Ecology-Progress
Series 445: 279–291.
38. Wiley TR, Simpfendorfer CA (2007) The ecology of elasmobranchs occurring in
the Everglades National Park, Florida: implications for conservation and
management. Bulletin of Marine Science 80: 171–189.
39. DeAngelis BM, McCandless CT, Kohler NE, Recksiek CW, Skomal GB (2008)
First characterization of shark nursery habitat in the United States Virgin
Islands: evidence of habitat partitioning by two shark species. Marine Ecology
Progress Series 358: 257–271.
40. Freitas RHA, Rosa RS, Grub er SH, Wetherbee BM (2006) Early growth and
juvenile population structure of lemon sharks Negaprion brevirostris in the Atol das
Rocas Biological Reserve, off north-east Brazil. J Fish Biol 68: 1319–1332.
41. Garla RC, Garcia JJ, Veras LB, Lopes NP (2009) Fernando de Noronha as an
insular nursery area for lemon sharks, Negaprion brevirostris, and nurse sharks,
Ginglymostoma cirratum, in the equatorial western Atlant ic Ocean. Marine
Biodiversity Records 2: e109.
42. Reyier EA, Adams DH, Lowers RH (2008) First Evidence Of A High Density
Nursery Ground For The Lemon Shark, Negaprion brevirostris, Near Cape
Canaveral, Florida. Florida Scientist 71: 134–148.
43. Kessel ST (2010) An investigation into the behaviour and population dynamics
of the lemon shark (Negaprion brevirostris) [Thesis (Ph D ) - Cardiff University,
2010]. 312 leaves. p.
44. Perkins T, Norris H, Wilder D, Kaiser S, Camp D, et al. (1997) Distribution of
Hard-Bottom Habitats on the Continental Shelf off the Northern and Central
East Coast of Florida Final Report. Southeast Area Monitoring and Assessment
Program Bottom Mapping Workgroup and the National Marine and Fisheries
Service.
45. Gilmore RG (1995) Environmental and Biogeographic Factors Influencing
Ichthyofaunal Diversity: Indian River Lagoon. Bulletin of Marine Science 57:
153–170.
46. Zuur AF, Ieno EN, Walker NJ, Saveliev AA, Smith GM (2009) Mixed Effects
Models and Extensions in Ecology with R. New York: Springer. 574 p.
47. Pinheiro J, Bates D, DebRoy S, Sarkar D, Team RC (2012) nlme: Linear and
Nonlinear Mixed Effects Models.
48. Burnham KP, Anderson DR (2002) Model selection and multimodel inference :
a practical information-theoretic approach. New York: Springer. xxvi, 488 p. p.
49. Hosmer DW, Lemeshow T (2000) Appl ied logistic regression. New York: John
Wiley and Sons.
50. Hamel S, Yoccoz NG, Gaillard JM (2012) Statistical evaluation of parameters
estimating autocorrelation and individual heterogeneity in longitudinal studies.
Methods in Ecology and Evolution 3: 731–742.
51. Team RDC (2012) R: A language and environment for statistical computing. R
Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0,
URL http://www.R-project.org/.
52. Bates D, Maechler M, Bolker B (2011) lme4: Linear mixed-effects models using
S4 classes. R package version 0.999375-42.
53. Bass AJ (1978) Problems in studies of sharks in the Southwest Indian Ocean In:
Hodgson ES, Mathewson RF, United States. Office of Naval Research, Naval
Research Laboratory (U.S.). Technical Information Division., editors. Sensory
biology of sharks, skates, and rays. Arlington, Va.: Office of Naval Research,
Coastal Migrations of Juvenile Lemon Sharks
PLOS ONE | www.plosone.org 12 February 2014 | Volume 9 | Issue 2 | e88470

Dept. of the Navy : for sale by the Supt. of Docs., U.S. Govt. Print. Off. pp. 545–
594.
54. Heupel MR, Carlson JK, Simpfendorfer CA (2007) Shark nursery areas:
concepts, definition, characterization and assumptions. Marine Ecology-Progress
Series 337: 287–297.
55. Dodrill JW (1977) A Hook and Line Survey of the Sharks Found Within Five
Hundred Meters of Shore Along Melbourne Beach, Brevard County, Florida.
Florida Institute of Technology.
56. Gurshin CWD (2007) Shark nursery grounds in Sapelo Island National
Estuarine Research Reserve, Georgia. In: McCandless CTK, N.E.; Pratt,
H.L, Jr., editor. Shark nursery grounds of the Gulf of Mexico and the east coast
waters of the United States. Bethesda, Maryland: American Fisheries Society.
pp. 141–151.
57. Abel DC, Young RF, Garwoo d JA, Travaline MJ, Yednock BK (2007) Survey of
the shark fauna in two South Carolina estuaries and the impact of salinity
structure. In: McCandless CT, Kohler NE, Pratt HL, editors . Shark Nursery
Grounds of the Gulf of Mexico and the East Coast of the United States.
Bethesda, Maryland: American Fisheries Society Symposium 50. pp. 109–124.
58. Ulrich GF, Jones CP, Driggers WB, Drymon JM, Oakley D, et al. (2007) Habitat
utilization, relative abundance, and seasonality of sharks in the estuarine and
nearshore waters of South Carolina. In: McCandless CT, Kohler NE, Pratt HL,
Jr., editors. Shark nursery grounds of the Gulf of Mexico and the east coast
waters of the United States. Bethesda, Maryland: American Fisheries Society.
pp. 125–139.
59. Thorpe T, Jensen CF, Moser ML (2004) Relative Abundance and Reproductive
Characteristics of Sharks in Southeastern North Carolina Coastal Waters.
Bulletin of Marine Science 74: 3–20.
60. Gruber SH, de Marignac JRC, Hoenig JM (2001) Survival of juvenile lemon
sharks at Bimini, Bahamas, estimated by mark-depletion experiments.
Transactions of the American Fisheries Society 130: 376–384.
61. Matich P, Heithaus MR (2012) Effects of an extreme temperature event on the
behavior and age structure of an estuarine top predator, Carcharhinus leucas.
Marine Ecology Progress Series 447: 165–178.
62. Donaldson MR, Cooke SJ, Patterson DA, Macdonald JS (2008) Cold shock and
fish. J Fish Biol 73: 1491–1530.
63. ASMFC (2008) Interstate Fishery Management Plan for Atlantic Coastal Sharks.
Fishery Management Report No. 46 of the Atlantic States Marine Fisheries
Commission. 172 p.
Coastal Migrations of Juvenile Lemon Sharks
PLOS ONE | www.plosone.org 13 February 2014 | Volume 9 | Issue 2 | e88470