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297
Stress response and postrelease mortality of
blacktip sharks (Carcharhinus limbatus)captured
in shore-based and charter-boat-based
recreational fisheries
D. Nick Weber (contact author)1,2
Bryan S. Frazier1
Nicholas M. Whitney3
James Gelsleichter4
Gorka Sancho2
Email address for contact author: d.nick.weber@gmail.com
1 Marine Resources Research Institute
South Carolina Department of Natural Resources
217 Fort Johnson Road
Charleston, South Carolina 29412
Present address of contact author:
153 Tidal Hall
Texas A&M University—Corpus Christi
6300 Ocean Drive
Corpus Christi, Texas 78412
2 Grice Marine Laboratory
Department of Biology
College of Charleston
205 Fort Johnson Road
Charleston, South Carolina 29412
3 Anderson Cabot Center for Ocean Life
New England Aquarium
1 Central Wharf
Boston, Massachusetts 02110
4 Department of Biology
University of North Florida
1 UNF Drive
Jacksonville, Florida 32224
Abstract—In the coastal waters of the
southeastern United States, the black-
tip shark (Carcharhinus limbatus) is
targeted by recreational anglers and
is currently one of the most often
captured large coastal shark species.
We estimated postrelease mortality
(PRM) rates for blacktip sharks cap-
tured on rod and reel by shore- based
and charter- boat- based fishermen by
using acoustic transmitters (number
of sharks=81). Additionally, 24 black-
tip sharks were tagged with pop- off
satellite archival tags (PSATs) to vali-
date the survivorship obtained through
analysis of data from the acoustic trans-
mitters. The stress response associated
with both recreational capture meth-
ods was quantified by using numer-
ous blood chemistry characteristics.
Overall, 18.5% of blacktip sharks died
postrelease (17.1% and 20.0% of those
captured from shore and from charter
boats, respectively). The results of sur-
vivorship analysis based on data from
transmitters are consistent with results
inferred from data from PSATs, sup-
porting our use of acoustic transmitters
to assess PRM in blacktip sharks. Fight
time had a significant effect on blood
pH, lactate, hematocrit, potassium, and
glucose for sharks caught from shore
but only on lactate for sharks caught
from charter boats. In general, the blood
chemistry characteristics assessed were
poor predictors of PRM. Fifty percent of
foul- hooked sharks (i.e., sharks hooked
anywhere but the jaw) died postrelease,
indicating the importance of the effect
of hook placement on PRM.
Manuscript submitted 20 February 2020.
Manuscript accepted 25 September 2020.
Fish. Bull. 118:297–314 (2020).
Online publication date: 9 October 2020.
doi: 10.7755/FB.118.3.8
The views and opinions expressed or
implied in this article are those of the
author (or authors) and do not necessarily
reflect the position of the National
Marine Fisheries Service, NOAA.
In the late 1900s, shark populations
in the western North Atlantic Ocean
declined drastically in size (Musick
et al., 1993), because of overexploita-
tion and sharks being captured as
bycatch in commercial fisheries (Bonfil,
1994; Rose, 1996). In an effort to ensure
the sustainability of shark fisheries, a
variety of national and international
management measures, including man-
dated release of imperiled species, were
introduced (Ellis et al., 2017). These
management measures have since been
augmented by an increasing emphasis
on the catch and release of sharks by
recreational anglers (Bartholomew and
Bohnsack, 2005; Skomal, 2007), and
the release of captured sharks by both
commercial and recreational anglers
has become a common practice (Press
et al., 2016; Ellis et al., 2017). Although
catch and release is broadly advocated
to minimize effects on fish stocks,
postrelease mortality (PRM) may still
occur as a result of the physiological
stress or physical injury of capture
(Bartholomew and Bohnsack, 2005;
Cooke and Schramm, 2007). There-
fore, there is an increasing interest
in understanding the conditions that
bring about PRM, as well as in how to
minimize PRM rates (Cooke and Cowx,
2004; Gallagher et al., 2014).
Postrelease mortality rates vary
widely among shark species (Ellis
et al., 2017) and depend on factors such
as gear type, duration of capture, respi-
ratory mode (Dapp et al., 2016), and
aerobic scope (Priede, 1985; Korsmeyer
et al., 1996; Talwar et al., 2017). Tradi-
tionally, PRM rates have been assessed
by using pop- off satellite archival tags
NOAA
National Marine
Fisheries Service Fishery Bulletin First U.S. Commissioner
of Fisheries and founder
of Fishery Bulletin
established in 1881
298 Fishery Bulletin 118(3)
(PSATs) (e.g., Heberer et al., 2010; French et al., 2015), but
the cost of such tags often precludes the use of large sam-
ple sizes (Donaldson et al., 2008), making accurate assess-
ments of PRM for a species difficult. To circumvent this
issue, the use of acoustic telemetry to assess PRM has been
investigated in recent years (Kneebone et al., 2013; Kilfoil
et al., 2017). Results of previous research indicate that
acoustic transmitters can be used to assess PRM in the
presence of acoustic receiver arrays (Kneebone et al., 2013;
Kilfoil et al., 2017). Because the number of acoustic receiv-
ers deployed along the eastern coast of the United States
continues to grow (Kneebone et al., 2013), the applicability
and effectiveness of this method will likely increase. The
smaller size of acoustic transmitters, compared with the
size of the electronic tags traditionally used to assess PRM
(e.g., PSATs), could reduce any potential effects of the tag
on a shark’s behavior postrelease. Additionally, the lower
cost of acoustic transmitters could allow the assessment
of larger sample sizes across a wider range of conditions,
providing more robust estimates of PRM.
Efforts have been made to link PRM with perturbations
in blood chemistry caused by the stress of capture (Whitney
et al., 2017). The stress experienced by captured sharks has
traditionally been quantified by an assessment of the acid-
base status of blood (e.g., Mandelman and Skomal, 2009),
based on the notion that stress causes a decrease in blood
pH, known as acidemia, due to both metabolic and respira-
tory acidoses (Skomal, 2007). Additionally, stress- related
cellular fluid shifts, which can result in haemoconcen-
tration and disruptions to ionic and osmotic homeostasis
(Wood, 1991; Skomal and Mandelman, 2012), have been
quantified through changes in plasma electrolyte concen-
trations (e.g., Marshall et al., 2012; French et al., 2015).
Because interspecific differences in responses to capture
stress may be linked to the metabolism and physiology of
the species in question (Skomal and Mandelman, 2012),
analyzing a suite of blood chemistry characteristics may
allow for a better understanding of the implications of
capture on subsequent mortality events (Skomal, 2007;
French et al., 2015). Moreover, when blood chemistry mea-
surements are coupled with estimates of PRM, insights
into the causes of physiological stress and mortality, as
well as into potential mitigation measures, can be gained
(Skomal, 2007; Mandelman and Skomal, 2009).
The blacktip shark (Carcharhinus limbatus) is a rel-
atively large coastal species with a circumglobal distri-
bution in temperate coastal waters (Compagno, 1984;
Castro, 2011). In the western North Atlantic Ocean,
blacktip sharks migrate seasonally, inhabiting the near-
shore waters of Georgia, South Carolina, and North
Carolina during the summer months and moving south-
ward to southeastern Florida during the winter months
(Castro, 1996; Kajiura and Tellman, 2016). The coastal
distribution of blacktip sharks, combined with the sea-
sonal predictability of their center of abundance (Kajiura
and Tellman, 2016), makes them easily accessible for both
commercial and recreational fisheries. Consequently, the
blacktip shark is currently one of the most often landed
large coastal shark species (NMFS, 2019). Compared
with other large coastal sharks, blacktip sharks have an
intermediate life history, defined by the fact that they
have a relatively low age at maturity (4–7 years; Killam
and Parsons, 1989), reproduce biennially (Castro, 1996),
and have an average of 4−6 pups per reproductive cycle
(Bigelow and Schroeder, 1948). Collectively, proximity to
the coast, intermediate life history characteristics, and
exposure to high commercial and recreational fishing
pressure make the blacktip shark particularly sensitive
to overfishing.
Few studies have investigated the effects of capture
on the blacktip shark, but blood chemistry characteris-
tics measured in blacktip sharks caught on drumlines
and longlines indicate that the magnitude of the stress
response in this species is greater than that in other
carcharhinid species (Mandelman and Skomal, 2009;
Marshall et al., 2012; Gallagher et al., 2014). Data on acid-
base blood chemistry obtained from blacktip sharks caught
on longlines indicate that this species may have a strictly
respiratory response to capture because the observed aci-
dosis was driven by increases in pCO2 (Mandelman and
Skomal, 2009). Consequently, it has been suggested that
blacktip sharks could lack the mechanisms (e.g., splenic
red blood cell ejection and red blood cell swelling through
Na+—H+ exchangers; Nikinmaa, 1992; Brill et al., 2008)
responsible for maintaining or increasing oxygen deliv-
ery during strenuous activity (Mandelman and Skomal,
2009). Although the results of this research indicate that
blacktip sharks may be particularly sensitive to the stress
associated with capture, Whitney et al. (2017) found a
relatively low rate of PRM in the recreational fishery for
blacktip sharks in the Gulf of Mexico. Additional data are
needed on both the physical and physiological effects of
recreational rod- and- reel capture on the blacktip shark,
and how these effects influence PRM.
Recreational fishing is increasing in popularity world-
wide (Arlinghaus and Cooke, 2009; Press et al., 2016). In
particular, a specialized method of fishing that targets
large coastal sharks from beaches, known as shore- based
or land- based shark angling, has been receiving increas-
ing attention in terms of management and conservation in
recent years (Ajemian et al., 2016; Shiffman et al., 2017).
The Florida Fish and Wildlife Conservation Commission
recently formally defined shore- based shark fishing and
instituted a mandatory shore- based shark fishing permit
in response to perceived issues with handling methods
and mortality of captured sharks (Shiffman et al., 2017).
Because shore- based anglers typically bring captured
sharks onto the beach for hook removal and photographs,
sharks caught from the shore may be subject to increased
handling stress and increased exposure to air, reducing
the shark’s ability to breathe (Casselman1). However,
shore- based anglers often fish at night and on deserted
beaches, and there are limited data available on their
1 Casselman, S. J. 2005. Catch- and- release angling: a review with
guidelines for proper fish handling practices, 26 p. Fish Wildl.
Branch, Ontario Minist. Nat. Resour., Peterborough, Canada.
[Available from website.]
Weber et al.: Stress response and postrelease mortality of Carcharhinus limbatus captured in recreational fisheries 299
fishing and handling techniques or on the effects on the
survival of released sharks.
Given the attention that recreational shore- based shark
fishing has been receiving (Ajemian et al., 2016; Shiffman
et al., 2017), and an increased emphasis on catch- and- release
angling (Bartholomew and Bohnsack, 2005), the determi-
nation of gear- and species- specific PRM rates is critical to
the effective management of shark species. Through collab-
oration with recreational anglers, in this study we assessed
PRM rates of blacktip sharks captured and released in both
the shore- based and charter- boat- based recreational fisher-
ies and quantified the physiological stress response associ-
ated with both recreational capture methods.
Materials and methods
Research was completed under the South Carolina
Code of Law Section 50- 5- 202 that authorizes the South
Carolina Department of Natural Resources to conduct
research in state waters. Research was conducted in
accordance with the College of Charleston Institutional
Animal Care and Use Committee (IACUC) through pro-
tocol no. IACUC- 2017- 007.
Sampling location and design
Blacktip sharks were caught with rod and reel by rec-
reational anglers from the shore (i.e., beach) and from
charter fishing boats. All fishing from charter boats was
conducted by the clients who hired the charter boat;
therefore, a wide range of angler experience was sampled.
Anglers used their personal fishing equipment, which var-
ied in size and strength, and no input was provided by the
authors on the fishing equipment (e.g., rod- and- reel type
and size or hook type and size) or capture techniques used.
Sampling was conducted from May through October 2017
and from February through October 2018, in the coastal
waters of South Carolina and Florida, at locations chosen
by participating anglers (Fig. 1, A and B). During each
angling trip, reel type (i.e., conventional level wind versus
spinning), hook type (circle versus J), and sea- surface tem-
perature were recorded.
Once an angler hooked a shark, the fight time, defined
as the time from the initial strike until the time the shark
was landed and secured by anglers, was recorded to the
nearest second. Once secured, the shark went through the
sampling procedure in the state that the angler handled
it (e.g., sharks caught from charter boats were sampled
either on board the boat or in the water, depending on
whether or not the charter captain decided to bring the
shark on board for photographs or hook removal). All
sharks caught by shore- based anglers were brought out
of the water and onto the beach. Sharks were then sam-
pled while the recreational anglers completed their rou-
tine (which often included hook removal, measurement,
2 Jurisdiction of Department of Natural Resources, S.C. Code
§ 50- 5- 20 (2000). [Available from website.]
and photographs), to minimize any increase in handling
time due to the sampling procedure. Blood was drawn
through caudal venipuncture immediately after the shark
was secured, a tag was or tags were applied, fork length
was measured (in centimeters), and sex was determined.
Phlebotomies were performed through caudal venipunc-
ture to ensure that blood sampling was quick, efficient,
and minimally invasive (Lawrence et al., 2020).
Once the sampling procedure was complete, anglers
were responsible for releasing the shark. The handling
time, defined as the time from when the shark was initially
secured to the release of the shark, was recorded to the
nearest second. Upon release, the condition of the shark
was assigned to 1 of 5 categories, ranging from condition
1 (excellent) to condition 5 (moribund), on the basis of the
shark’s behavior at release (Table 1). If the anglers decided
to revive the shark (i.e., hold the shark in the water until
they deemed it strong enough for release), the revival time
was recorded. Hook status was recorded as removed or
retained, and hook location was recorded. The authors pro-
vided no input to the anglers regarding hook removal, and
some anglers chose to leave hooks that could not be easily
removed.
Blood chemistry
Blood samples (3 mL) were drawn by using 18- gauge,
sterilized needles and heparin- rinsed syringes, and sam-
ples were immediately injected into 10- mL vacutainers
that contained sodium heparin. To avoid compromising
accuracy of blood gas analysis after phlebotomy (Whitney
et al., 2017), a subsample of whole blood (90 μL) was
immediately (within 30 s) analyzed for pH and lactate
by using an i- STAT3 portable blood analyzer (Zoetis Inc.,
Parsippany- Troy Hills, NJ) with a CG4+ cartridge (Zoetis
Inc.). This analyzer has been used in prior field studies
on elasmobranch species (e.g., Mandelman and Skomal,
2009; Brooks et al., 2012; Gallagher et al., 2014), and
the relative accuracy of measurements of pH and lactate
in ectothermic sharks has been validated (Gallagher
et al., 2010; Harter et al., 2015). Measurements of blood
pH were temperature corrected to sea- surface tempera-
tures at the locations of capture by using the following
equation:
pHTC = pHM – 0.011(T – 37),
where pHTC = temperature- corrected pH values;
pHM = measured pH values; and
T = sea- surface temperatures
(Mandelman and Skomal, 2009; Gallagher et al., 2010;
Brooks et al., 2012; Kneebone et al., 2013; Gallagher
et al., 2014; Whitney et al., 2017). All pH values subse-
quently reported herein were temperature corrected in
this manner.
3 Mention of trade names or commercial companies is for identi-
fication purposes only and does not imply endorsement by the
National Marine Fisheries Service, NOAA.
300 Fishery Bulletin 118(3)
A separate subsample of whole blood (0.2 mL) was simul-
taneously placed on ice (within 30 s) for hematocrit analy-
sis, which was completed within 4 h of capture (Manire
et al., 2001). At the time of hematocrit analysis, whole blood
samples (3 samples per shark) were transferred into micro-
capillary tubes and centrifuged (centrifuge, Vernitron Med-
ical Products Inc., South Hackensack, NJ) for 5 min at
10,000 rpm (10,062 × gravity). Hematocrit was determined
as the percentage of total blood volume composed of red
blood cells, calculated by using an EZ Reader Microhemato-
crit Card (LW Scientific Inc., Lawrenceville, GA).
The remaining whole blood was centrifuged (E8 Porta-
fuge, LW Scientific Inc.) for 5 min at 3500 rpm (1534 ×
gravity), to separate the plasma and the red blood cells.
Three subsamples of plasma (each 0.5 mL) were frozen
immediately in liquid nitrogen and, subsequently, stored
at –80°C. At the time of plasma electrolyte analysis,
plasma samples were thawed and diluted with deion-
ized water (dH2O) at a plasma- to- dH2O ratio of 2:3, and
approximately 55 μL of the diluted samples was injected
into a Critical Care Xpress benchtop analyzer (CCX, Nova
Biomedical, Waltham, MA) to quantify levels of Na+,
Cl−, K+, Ca2+, Mg2+, and glucose. All concentrations were
within the detection limits of the instrument used to mea-
sure them.
Postrelease mortality
Blacktip sharks were tagged with V16- 4H acoustic trans-
mitters (Vemco, Bedford, Canada) that measured 18.2 by
Figure1
Maps showing the sites where blacktip sharks (Carcharhinus limbatus) were caught and tagged
off the coasts of (A) South Carolina and (B) Florida from May through October 2017 and from Feb-
ruary through October 2018 and (C) locations of acoustic receivers present along the southeastern
coast of the United States. Open circles indicate sites where sharks were caught from charter
boats, and solid circles indicate sites where sharks were caught from shore. The numerals next to
circles indicate the number of blacktip sharks tagged at each sampling site.
Weber et al.: Stress response and postrelease mortality of Carcharhinus limbatus captured in recreational fisheries 301
88 mm, had a 30- s nominal delay in transmission rate,
and were deployed in an external case. The tagging was
accomplished by threading monofilament through a hole
drilled into the radial musculature at the base of the first
dorsal fin and crimping the monofilament together behind
the dorsal fin. This technique of using an external attach-
ment allowed handling times to be short and, therefore,
minimized any bias introduced by the tagging procedure
(Kilfoil et al., 2017). Survivorship was assessed by pas-
sively monitoring sharks following release and examin-
ing movements of sharks among fixed acoustic receivers
deployed along the southeastern coast of the United States
as part of the Atlantic Cooperative Telemetry (ACT) and
FACT Networks (Fig. 1C).
To identify and remove false detections potentially cre-
ated by collisions of acoustic transmitters (Heupel et al.,
2006), the full detection database was filtered by using the
glatos package (vers. 0.4.2; Holbrook et al., 2020), which
flags false detections on the basis of the “short- interval”
criteria described by Pincock4, in the statistical program
R (vers. 3.5.1; R Core Team, 2018). Specifically, detections
isolated on a single receiver for more than 30 times the
nominal delay of the transmitter (i.e., 15 min) were con-
sidered to be false and were removed. Because most mor-
talities associated with a capture event occur within 12 h
of release (Marshall et al., 2015; Talwar et al., 2017; Whit-
ney et al., 2017), sharks that were detected multiple times
by an acoustic receiver more than 10 d postrelease were
considered to have survived the capture event. Moreover,
because tags that are ingested during predation events
are typically regurgitated within approximately 8 d of
ingestion (Kerstetter et al., 2004), we assumed survival
only for individuals detected more than 10 d postrelease
to account for possible capture- related predation events
4 Pincock, D. G. 2012. False detections: what they are and how
to remove them from detection data. AMIRIX Document
DOC- 004691, vers. 03, 10 p. [Available from website.]
(i.e., acoustic detections recorded <10 d postrelease could
represent movements of the transmitter consumer rather
than the target individual).
To validate the data obtained from the acoustic
transmitters and used for survivorship analysis, a sub-
set of sharks were also tagged with PSATs (PSATLife,
Lotek Wireless Inc., Newmarket, Canada). The PSATs
(40 × 125 mm) are designed for monitoring postrelease
survival and were programmed to record pressure, exter-
nal temperature, and light intensity every 10 s over a
28- d deployment. If the PSAT was not recovered, sum-
mary data were obtained from PSATs through the use of
satellite- derived pressure- temperature profiles (means
for 5- min periods). Recovery of PSATs allowed more
detailed analysis of the entire archived data set, which
included pressure, external temperature, and light inten-
sity measured every 10 s. The PSATs were programmed
to release prematurely if pressure values remained con-
stant (±50,000 Pa) over a 3- d period, a consistency in
pressure values that would be observed in data from a
tag on a dead shark on the ocean floor (Heberer et al.,
2010). The PSATs were attached in the same way as
the acoustic transmitters, by threading monofilament
through a hole drilled into the radial musculature at the
base of the first dorsal fin. Survival of sharks tagged with
PSATs was inferred by assessing the pressure, external
temperature, and light intensity profiles, following pro-
tocols previously used to infer mortality from PSAT data
records (Heberer et al., 2010).
Data analysis
Postrelease mortality rates were calculated as the percent-
age of the total number of tagged individuals that either
died after release (as indicated by PSAT data) or were
assumed to have died as a result of capture (because they
were not detected by an acoustic receiver more than 10 d
after release). For individuals whose PSAT was shed <10 d
Table1
Number of tagged blacktip sharks (Carcharhinus limbatus) assigned to categories of release con-
dition on the basis of behavior at the time of release. Blacktip sharks were caught from shore
(number of samples [n]=41) and from charter boats (n=40), tagged, and then released in coastal
waters of South Carolina and Florida between May and October 2017 and between February and
October 2018.
Condition
category Issues observed and resulting diagnosis
Capture method
Shore Charter
1 Excellent: rapidly swam with no signs of distress 10 28
2 Good: stressed, swam away but appeared slow or disoriented 14 10
3 Fair: swam laboriously or had signs of physical trauma 10 0
4 Poor: attempted to swim and had potentially lethal physical
trauma (e.g., excessive bleeding or deep hooking)
7 2
5 Moribund: made no effort to swim 0 0
302 Fishery Bulletin 118(3)
postrelease, acoustic telemetry data were used to ver-
ify survivorship. We used the Clopper–Pearson interval
to calculate 95% confidence intervals (CIs) for mortality
rates. Linear regressions were used to determine if fight
time (i.e., time on the line) had an effect on blood chem-
istry characteristics. Analyses of covariance (ANCOVA)
were used to determine if blood chemistry characteristics
differed between the 2 recreational capture methods, cap-
ture from shore and capture from charter boats, to account
for extraneous variability due to differences in fight time
between capture methods.
To predict PRM by using the measured blood chemistry
characteristics, generalized linear models (GLMs) with a
binomial probability distribution and a logit link function
were fitted to the data for all sharks combined (number
of sharks [n]=81) and then separately to data for sharks
caught from shore (n=41) and to data for sharks caught
from charter boats (n=40) (Schlenker et al., 2016; Talwar
et al., 2017). Before constructing the GLMs, principal
components analyses were performed to examine poten-
tial correlations between explanatory variables and to
reduce the number of explanatory variables included in
the GLMs (Suppl. Fig. 1). The full models for all sharks
combined and for sharks caught from shore described the
relationships between PRM as a binary response variable
and 4 potential explanatory variables, including pH, K+,
Na+, and glucose. The full model for sharks caught from
charter boats included pH, K+, glucose, and hematocrit as
variables. Nonsignificant factors were removed in back-
ward stepwise fashion, starting with the least significant
factor and evaluating the increases in deviance and in the
Akaike information criterion (AIC) (Akaike, 1973) with
each removal (Talwar et al., 2017). The model with the
fewest number of explanatory variables and lowest AIC
was considered the best- fit model.
To predict PRM with the observed capture charac-
teristics, GLMs were used to describe the relationship
between PRM as a binary response variable and water
temperature, fight time, handling time, hook location
(foul- hooked, i.e., hooked anywhere but the jaw, versus
not foul- hooked), release condition, and capture method
(from shore versus from charter boat). Because the
majority of sharks caught from shore were caught with
spinning reels (76%) and the majority of sharks caught
from charter boats were caught with conventional level-
wind reels (85%), reel type was omitted from the GLM.
As previously described, GLMs were fitted to the data
for all sharks combined (n=81) and then separately to
data for sharks caught from shore (n=41) and to data
for sharks caught from charter boats (n=40). The best- fit
model was again selected in a backward stepwise fashion
and had the fewest number of explanatory variables and
lowest AIC.
Fisher’s exact tests were used to test the null hypothe-
sis that the distribution of survivors and mortalities was
equal across both hook locations and release conditions.
All analyses were conducted by using R, and all graphs
were created in RStudio (vers. 1.1.456; RStudio, Boston,
MA). The level of significance for all tests was 0.05.
Results
Capture characteristics
A total of 81 blacktip sharks were caught and tagged with
acoustic transmitters (from shore: n=41; from charter
boats: n=40). A subset of those individuals (shore: n=12;
charter boats: n=12) were also tagged with PSATs. There
were no significant differences in fork length, fight time,
handling time, or water temperature between recreational
capture methods (Table 2). Additionally, there was no dif-
ference in fight time between reel types. All participating
recreational anglers chose to use circle hooks, and hook
locations were as follows: jaw, including corner, bottom,
and top jaw (n=75); basihyal (n=3); gut (n=1); throat (n=1);
and tail (n=1). Any shark not hooked somewhere in the
jaw was considered to be foul- hooked in all subsequent
analyses. Anglers chose to remove the hook in all but 3
instances (corner jaw: n=1; basihyal: n=1; gut: n=1).
Observed postrelease mortality
Fifteen blacktip sharks (shore: n=7; charter boats: n=8)
died within 10 d of being released by recreational anglers,
resulting in postrelease mortality rates of 17.1% (95% CI:
7.2–32.1) for sharks caught from shore and 20.0% (95%
CI: 9.1–35.6) for sharks caught from charter boats. No
immediate mortalities were observed, with all individu-
als swimming away at the time of release. Only 4 of the
81 tagged sharks were revived by anglers before being
released, and revival times ranged from 1 to 4 min. Six of
the 15 sharks considered to have died after release were
assigned release conditions of 3 (fair: n=2) or 4 (poor: n=4),
either because of signs of physical injury or trauma (e.g.,
excessive bleeding from the hook location) or because of a
complete lack of movement during the handling procedure
and difficulty swimming postrelease. Additionally, of the
sharks considered to have died, one was hooked in the tail
and one was hooked in the jaw but with its tail wrapped in
the fishing line. Both individuals were reeled in backward,
with fight times (6 min 35 s and 8 min 57 s, respectively)
exceeding the average fight time observed throughout the
study (4 min 55 s [standard deviation (SD) 2 min 27 s]).
The 7 remaining sharks that died had no signs of injury or
trauma and were assigned release conditions of 1 (excel-
lent: n=6) or 2 (good: n=1).
Five of the 15 sharks that died were tagged with both
PSATs and acoustic transmitters (shore: n=3; charter
boats: n=2; Table 3); whereas, the mortalities of the other
10 sharks were confirmed with acoustic data only. Data
obtained from the PSATs attached to these sharks indi-
cate that 2 PSATs were ingested within 6 h of being
deployed. Shark 9 was actively swimming when its PSAT
was ingested 6 h postrelease (Fig. 2A). This PSAT recorded
fluctuating pressure (0–97,200 Pa) and light intensity
(93–384) for the 6 h prior to ingestion, variations that are
consistent with vertical movements in the water column
during daytime hours. Subsequent to its ingestion, the tag
provided data that indicate darkness for 3 d followed by a
Weber et al.: Stress response and postrelease mortality of Carcharhinus limbatus captured in recreational fisheries 303
Table2
Capture characteristics, blood chemistry characteristics, and postrelease mortality rates for blacktip sharks (Carcharhinus
limbatus) caught with rod and reel by recreational anglers from shore and from charter boats in the coastal waters of South
Carolina and Florida between May and October 2017 and between February and October 2018. Mean values are provided with
standard deviations in parentheses. Once caught, sharks were tagged and measured, and blood samples were taken from them.
Upon release, the condition of sharks was assessed (see Table 1). pHTC=temperature- corrected blood pH.
Capture
method
Capture characteristics
Postrelease
mortality (%)No. tagged
Fight
time (min)
Handling
time (min)
Water
temp. (°C)
Proportion
female (%)
Fork length
(cm)
Release
condition
Charter 40 4.75 (2.02) 3.55 (1.22) 26.9 (2.5) 71 124.2 (19.2) 1.4 (0.7) 20.0
Shore 41 5.09 (2.82) 3.33 (1.16) 27.7 (2.6) 77 124.5 (24.4) 2.4 (1.0) 17.1
Capture
method
Acid- base status
Hematocrit
(%)
Plasma electrolytes and metabolites
pHTC
Lactate
(mmol/L)
Na+
(mmol/L)
Cl−
(mmol/L)
K+
(mmol/L)
Ca2+
(mmol/L)
Mg2+
(mmol/L)
Glucose
(mg/dL)
Charter 7.34 (0.08) 2.01 (0.87) 25.2 (2.1) 273.1 (9.2) 267.3 (7.3) 5.7 (0.7) 2.8 (0.1) 1.1 (0.2) 56.3 (5.9)
Shore 7.33 (0.10) 1.74 (1.07) 24.1 (3.0) 273.4 (7.4) 266.5 (6.0) 5.3 (0.7) 2.7 (0.2) 1.1 (0.3) 58.3 (4.9)
Table3
Characteristics of the capture of blacktip sharks (Carcharhinus limbatus) tagged with both pop- off satel-
lite archival tags and acoustic transmitters in the coastal waters of South Carolina and Florida between
May and October 2017 and between February and October 2018. Upon release, the condition of sharks was
assessed (see Table 1). Asterisks (*) indicate sharks that, through the use of data from tags, were deter-
mined to have died after release.
Shark
ID no.
Capture
method Reel type
Fight
time (min)
Handling
time (min)
Hook
location
Bleeding
(yes or no)
Release
condition
7 Shore Spinning 6.83 2.58 Jaw N 3
9*Shore Conventional 4.38 3.75 Jaw Y 3
14 Charter Conventional 7.78 4.83 Jaw N 2
17 Charter Conventional 4.50 4.10 Jaw N 1
22 Charter Spinning 5.12 2.80 Jaw N 1
27 Shore Spinning 8.90 6.68 Jaw N 4
28 Shore Conventional 9.53 3.78 Jaw N 3
30*Shore Spinning 7.00 3.07 Jaw N 1
31 Shore Spinning 5.82 2.72 Jaw N 2
34 Shore Spinning 14.07 2.83 Jaw N 4
40 Charter Conventional 3.13 2.80 Jaw N 1
43*Charter Conventional 4.02 3.17 Throat Y 4
44 Charter Conventional 6.38 3.48 Jaw N 2
52 Shore Spinning 5.62 2.78 Jaw N 2
55 Shore Spinning 7.92 4.82 Jaw N 2
58*Shore Spinning 6.58 4.30 Tail N 4
59 Shore Spinning 3.40 4.05 Jaw N 2
61 Charter Conventional 3.92 4.70 Jaw N 2
63 Shore Conventional 8.45 3.78 Gut N 4
64 Charter Conventional 6.63 3.95 Jaw N 1
67 Charter Conventional 6.38 2.73 Jaw N 1
68 Charter Conventional 3.37 2.92 Jaw N 2
75 Charter Conventional 5.37 5.68 Jaw N 1
77*Charter Conventional 8.95 4.88 Jaw N 2
304 Fishery Bulletin 118(3)
return to a cyclical pattern of day and night (Fig. 2A). Brief
increases in light intensity during the ingestion period
may indicate partial regurgitation of the PSAT. Shark 43,
on the other hand, sank to the bottom immediately after
release, where it remained for 5 h before the tag was
ingested (Fig. 2B). The data from this PSAT indicate little
variation in pressure during the 5- h period prior to inges-
tion (198,400–215,900 Pa) and a complete lack of light
intensity (98–109), values consistent with the lack of
movement of a dead shark lying on the seafloor. Subse-
quent to its ingestion, the PSAT attached to shark 43 pro-
vided data that indicate darkness for 4.5 d followed by a
return to a cyclical pattern of day and night, similar to
what was observed for shark 9 (Fig. 2B). Because both pre-
dation events occurred within 6 h of capture, they were
attributed to capture and included in the estimates of
mortality.
Of the 24 PSATs deployed, all but 2 PSATs sent data to
the Argos satellite system, and 12 PSATs were physically
recovered—including 1 of the 2 PSATs that did not trans-
mit data. Excluding the PSATs deployed on the 5 sharks
that died, 12 PSATs detached prematurely and 6 PSATs
were retained for the entire 28- d deployment. Tag reten-
tion periods ranged from 17 min to 28 d (mean: 11.8 d [SD
10.6]). The PSAT pressure profiles indicate that none of
the premature detachments resulted from tags remaining
at a constant depth; when a PSAT stays at the same depth,
the burning of the release pin is triggered. Therefore, the
2 most plausible explanations for the premature detach-
ments are that the anchors were pulled out of the dorsal
musculature (e.g., as a result of tag consumption by a pred-
ator) or that the tethers broke. Two of the 12 PSATs that
were physically recovered, both of which detached prema-
turely, had numerous bite marks on them, indicating that
the tags were bitten off. Survival for individuals whose
PSATs were shed prematurely (i.e., <10 d after release)
was confirmed by using acoustic telemetry (Table 4).
The data obtained from the acoustic transmitters asso-
ciated with the 5 double- tagged sharks that died indicate
the same survivorship outcomes as the data from the
PSATs (Fig. 3). None of the acoustic transmitters that were
attached to sharks determined to be dead by using data
from PSATs were detected on an acoustic receiver more
than 5 d postrelease (Table 4). Both of the acoustic trans-
mitters associated with the PSATs that were ingested
were detected on acoustic receivers during the period
that the PSAT was inside of the stomach of the predator
or scavenger (the PSAT- ingestion period was determined
by a lack of light intensity, relative stability of tempera-
ture, and continuation of vertical movements indicated by
changes in pressure). However, the acoustic transmitters
were not detected following regurgitation of the PSATs
(within 5 d of ingestion), and the last acoustic detections
for both tags were recorded within 9 km (5 nautical miles)
Figure2
Pressure, external temperature, and light intensity profiles from pop-off satellite archival tags (PSATs) attached to 2 blacktip
sharks (Carcharhinus limbatus) during (A) July 2017 (shark 9) and (B) May 2018 (shark 43) in the coastal waters of South
Carolina and Florida, both showing a period of ingestion by another shark. Green, red, and blue lines indicate pressure, external
temperature, and light intensity, respectively. Shark 9 was actively swimming at the time of ingestion, 6 h after release. Shark
43 sank to the ocean floor immediately following release, and it remained there for 5 h prior to ingestion. Both PSATs were
regurgitated within 5 d of ingestion. The first black arrow in each panel denotes the time of assumed predation, and the second
black arrow denotes the time of assumed regurgitation.
Weber et al.: Stress response and postrelease mortality of Carcharhinus limbatus captured in recreational fisheries 305
of the location where the PSATs surfaced—indicating that
both the PSATs and acoustic transmitters were ingested
and regurgitated at the same time.
Along the southeastern coast of the United States,
286,683 acoustic detections were recorded by acoustic
receivers (Suppl. Fig. 2), and each acoustic transmitter
was detected an average of 3542 times (SD 4285). Fil-
tering, based on a 15- min isolation interval, identified
323 false detections (0.11%), which were subsequently
removed from the data set. The greatest movement
detected by using acoustic telemetry was from waters
off the Hudson Shelf in New York to waters near Miami,
Florida (straight- line distance of 1734 km). Fifteen of
the 19 double- tagged sharks that survived were detected
by acoustic receivers while their PSATs were still
attached, and all 19 sharks were detected after their
PSATs detached. Additionally, for the individual whose
PSAT did not transmit data and was not recovered,
9368 acoustic detections were recorded by 104 different
acoustic receivers over 637 d, ranging from Back Sound,
North Carolina, to Fort Pierce, Florida, and verifying sur-
vival of this shark.
Physiological effects of capture
Fight time had a significant effect on blood pH, hemato-
crit, lactate, potassium, and glucose. Blood pH decreased
significantly (P=0.02, coefficient of multiple determination
[R2]=0.11; Fig. 4A), and lactate (P=0.00, R2=0.40; Fig. 4B),
hematocrit (P=0.01, R2=0.16; Fig. 4C), potassium (P=0.02,
R2=0.10; Fig. 4D), and glucose (P=0.02, R2=0.11; Fig. 4E)
increased significantly with increasing fight times in
sharks caught from shore. Lactate (P=0.00, R2=0.45;
Fig. 4B) increased significantly with increasing fight times
for sharks caught from charter boats. However, the afore-
mentioned relationships between fight time and blood pH,
Table4
Summary of results from survivorship analysis based on data from pop- off satel-
lite archival tags (PSATs) and acoustic transmitters deployed on blacktip sharks
(Carcharhinus limbatus) in the coastal waters of South Carolina and Florida
between May and October 2017 and between February and October 2018. Asterisks
(*) indicate sharks that were determined to have died after release. The dagger (†)
indicates an individual whose PSAT never transmitted data to the Argos satellite
system and was never recovered; consequently, data were not available (NA) for this
individual.
Shark
ID no.
Duration
of PSAT
deployment
(d)
Acoustic transmitter characteristics
No. of detections
while PSAT
attached (no. of
unique receivers)
No. of detections
after PSAT
detached (no. of
unique receivers)
No. of days
between dates
of tagging and
last detection
7 8.29 0 (0) 1163 (21) 301
9*3.42 150 (5) 0 (0) 3
14 10.92 44 (4) 3296 (52) 413
17 4.63 5 (1) 1271 (12) 206
22 4.21 21 (5) 3022 (28) 213
27 1.17 21 (1) 309 (15) 219
28†NA NA 9368 (104) 637
30*0.01 0 (0) 0 (0) 0
31 8.25 0 (0) 10,167 (72) 428
34 7.25 0 (0) 289 (12) 103
40 16.13 858 (3) 462 (11) 64
43*4.46 41 (3) 0 (0) 2
44 5.63 48 (3) 2400 (29) 183
52 27.46 483 (4) 4475 (50) 333
55 27.33 1 (1) 7932 (23) 270
58*0.04 0 (0) 0 (0) 0
59 5.88 71 (3) 307 (5) 23
61 12.92 1911 (6) 10,889 (53) 321
63 27.33 30 (4) 28 (3) 123
64 27.42 61 (4) 1930 (26) 185
67 9.68 125 (5) 721 (14) 135
68 27.04 1300 (2) 11,748 (63) 305
75 27.29 174 (7) 1609 (17) 68
77*0.02 91 (2) 40 (3) 3
306 Fishery Bulletin 118(3)
hematocrit, potassium, and glucose were relatively weak
(as indicated by relatively low R2 values). There was no
change in sodium, chloride, calcium, or magnesium associ-
ated with fight time for either capture method (P>0.05).
The effect of fight time on any of the blood chemistry char-
acteristics did not differ between capture methods
(ANCOVA: P>0.05; Fig. 4, A–E).
Predicted postrelease mortality
The GLM analysis determined that a model including both
pH and glucose provided the best fit to binary PRM data
for all sharks combined (n=81; AIC for full model=74.96,
AIC for reduced model=71.24) and to data for sharks
caught from shore (n=41; full- model AIC=39.65, reduced-
model AIC=36.47), and a model including only potassium
provided the best fit to data for sharks caught from char-
ter boats (n=40; full- model AIC=43.13, reduced- model
AIC=38.40). None of the blood chemistry characteristics
were a significant predictor of mortality in any of the 3
best- fit models (P>0.05).
With respect to predicting PRM by using the observed
capture characteristics, a GLM model including only
release condition provided the best fit to binary PRM
data for all sharks combined (n=81; full- model AIC=72.52,
reduced- model AIC=63.24) and to data for sharks caught
Figure3
Detections of acoustic transmitters attached to 24 blacktip sharks (Carcharhinus limbatus) that were also tagged with pop-
off satellite archival tags (PSATs) from June 2017 through December 2019 off the coast of the southeastern United States,
by month and location. Each line of circles begins at the date tagged and shows the movement patterns of sharks over time.
Asterisks next to shark ID numbers indicate the 5 sharks determined to have died after release by using PSAT data. The ID
numbers for sharks caught from shore appear in bold, and the ID numbers for sharks caught from charter boats are not in bold.
from charter boats (n=40; full- model AIC=39.63, reduced-
model AIC=33.39). A model including water tempera-
ture (P=0.06), fight time (P=0.01), and release condition
(P=0.02) provided the best fit to data for sharks caught
from shore (n=41; full- model AIC=41.33, reduced- model
AIC=34.34).
Hook location did not have a significant effect on the
distribution of survivors and mortalities (Fisher’s exact
test: P=0.07), likely a result of small sample sizes for
hook locations other than the jaw. Of the individuals
hooked in the jaw (including corner, bottom, or top jaw),
16.0% died; whereas, 33.3% of individuals hooked in the
basihyal died and 100% of individuals hooked either in
the throat or tail died. The assigned release condition did
not have a significant effect on the distribution of sur-
vivors and mortalities (Fisher’s exact test, P=0.13). Of
the individuals assigned a release condition of excellent,
18.4% died; whereas, 8.3%, 20.0%, and 44.4% of individ-
uals assigned a condition of good, fair, and poor died,
respectively (Fig. 5).
Discussion
The results of this study provide insights into both the phys-
ical and physiological effects of recreational rod- and- reel
Weber et al.: Stress response and postrelease mortality of Carcharhinus limbatus captured in recreational fisheries 307
capture on the blacktip shark, and how these effects influ-
ence PRM rates. Furthermore, this study produced data on
the physiological stress and mortality experienced by indi-
viduals of this shark species when caught from shore, in a
recreational fishery receiving increasing management and
conservation attention. Postrelease mortality rates were
17.1% for sharks caught from shore and 20.0% for sharks
caught from charter boats, and the results of survivorship
analysis based on data from acoustic transmitters were
consistent with results inferred from data from PSATs, val-
idating our use of acoustic transmitters to assess PRM. Sig-
nificant physiological changes were documented in the
blood chemistry of sharks, and changes were influenced by
fight time.
Figure4
Linear regressions fitted to data of blood chemistry characteristics versus fight time for blacktip sharks (Carcharhi-
nus limbatus) caught by recreational anglers in the coastal waters of South Carolina and Florida between May and
October 2017 and between February and October 2018. Blood chemistry characteristics are (A) temperature-cor-
rected blood pH (pHTC), (B) lactate, (C) hematocrit, (D) potassium, and (E) glucose. Fight time refers to the time
from the initial strike until the time the shark was secured by anglers. Gray circles represent sharks caught from
shore, and black circles represent sharks caught from charter boats. Open circles indicate sharks determined to
have died after release. Solid lines indicate regression model predictions, and dashed lines indicate 95% confidence
intervals.
308 Fishery Bulletin 118(3)
Postrelease mortality
The PRM rates observed in this study are higher than
PRM rates reported for many other shark species caught
on rod and reel, such as the rates of 10% for shortfin
makos (Isurus oxyrinchus) (French et al., 2015), 12.5% for
juvenile lemon sharks (Negaprion brevirostris) (Danyl-
chuk et al., 2014), and 10% for Atlantic sharpnose sharks
(Rhizoprionodon terraenovae) (Gurshin and Szedlmayer,
2004). In addition, the observed PRM rates are approx-
imately twice as high as the rate of 9.7% reported by
Whitney et al. (2017) for blacktip sharks caught in the
charter- boat- based recreational fishery in Florida. This
difference in PRM rates may be partially attributable to
the higher incidence of physical injury or trauma (n=6),
foul- hooking (n=6), and live predation (n=1) observed in
our study but not by Whitney et al. (2017).
All sharks captured in our study were caught by rec-
reational anglers using their personal fishing equipment;
therefore, a wide range of angler experience and of gear
types and strengths were sampled. No at- vessel or at-
shore mortalities were observed, and all 5 of the mortality
events inferred from PSATs occurred within 6 h of release.
This result indicates that mortalities associated with rod-
and- reel capture of blacktip sharks do not occur at landing
but can occur up to 6 h postrelease and is consistent with
results from previous research on blacktip sharks indicat-
ing that behavioral recovery from rod- and- reel capture
takes an average of 10.5 h (Whitney et al., 2016).
This result is also consistent with those of other
studies that indicate that most capture- related
mortalities of sharks occur 1–4 h after release
(Heberer et al., 2010; Marshall et al., 2015; Whit-
ney et al., 2017).
Acoustic receiver coverage along the east-
ern coast of the United States is not consistent,
and many acoustic receivers tend to be closer to
shore, given the inherent issues with anchoring
receivers in open water. Therefore, it is possible
that surviving blacktip sharks, not tagged with a
PSAT, avoided acoustic detection (e.g., by staying
farther offshore) and as a result were considered
to be dead in our study. Additionally, it is pos-
sible that consumption of acoustic tags, without
predation on blacktip sharks themselves, could
explain the lack of acoustic detections for individ-
uals that were tagged only with acoustic trans-
mitters and were considered to have died during
our study. Because 10 of the 15 mortalities were
confirmed from acoustic data alone, the mortal-
ity rates presented herein may be overestimated.
However, given the preference of blacktip sharks
for nearshore waters and observed high detec-
tion rates of blacktip sharks tagged with acoustic
transmitters in this study (Table 4) and in other
ongoing studies (Bowers5), the probability of a
tagged blacktip shark escaping detection during
migration is likely low.
Predation postrelease
Postrelease mortality rates of blacktip sharks may be
influenced by the presence of larger shark species, such
as the tiger shark (Galeocerdo cuvier), great hammerhead
(Sphyrna mokarran), and bull shark (C. leucas), that are
commonly found off the southeastern coast of the United
States (Ulrich et al., 2007; Castro, 2011). In our study,
data profiles from PSATs deployed on 2 blacktip sharks
(sharks 9 and 43) indicate that the tags were ingested
within 6 h of release. Shark 9 was actively swimming at
the time of PSAT ingestion, but it may have been behav-
ing erratically given that the PSAT was ingested (6 h
after release) within the behavioral recovery window for
blacktip sharks caught on rod and reel (mean: 10.5 h;
Whitney et al., 2016). Shark 43 sank to the ocean floor
immediately after release, where it remained for 5 h until
the PSAT was scavenged. It was impossible to determine
with certainty if only the PSATs were consumed or if the
PSATs and the blacktip sharks were consumed. However,
the acoustic data obtained from the tags deployed on both
of these individuals (sharks 9 and 43) indicate that the
acoustic transmitters were ingested and regurgitated at
the same time as the PSATs. Therefore, it is unlikely that
5 Bowers, B. 2019. Personal commun. Charles E. Schmidt Coll.
Sci., Fla. Atl. Univ., 777 Glades Rd., Boca Raton, FL 33431.
Figure5
Proportions of blacktip sharks (Carcharhinus limbatus) determined
to have survived and died after release on the basis of data from
tags, by release condition. Blacktip sharks were caught and tagged
off the coasts of South Carolina and Florida between May and Octo-
ber 2017 and between February and October 2018. Release con-
ditions are based on behavior at the time of release (see Table 1).
n=number of sharks.
Weber et al.: Stress response and postrelease mortality of Carcharhinus limbatus captured in recreational fisheries 309
both the PSATs and acoustic transmitters were ingested
without predation upon the blacktip shark itself.
Although these events could be the first instances of
live predation on a blacktip shark recorded by a PSAT,
Lear and Whitney (2016) documented postrelease scav-
enging of a blacktip shark by a larger shark. In addition,
live predation events on other species are prevalent in the
literature; for example, such events have been reported
for the white marlin (Kajikia albida) and opah (Lampris
guttatus) (Kerstetter et al., 2004), the albacore (Thunnus
alalunga) (Cosgrove et al., 2015), and the tope (Galeorhi-
nus galeus) (Rogers et al., 2017; Tolentino et al., 2017).
Many shark species have been described to evert their
stomachs in response to physical stimuli, such as the
ingestion of hard, inedible objects (e.g., the shortfin mako;
Brunnschweiler et al., 2011), and the timing between the
ingestion and regurgitation events in our study (3.0 and
4.5 d) is similar to that reported in other studies (Kerstet-
ter et al., 2004; Brunnschweiler, 2009; Lear and Whitney,
2016; Rogers et al., 2017). It is possible that the pres-
ence of an external PSAT could increase predation risk,
because of an increase in visibility to predators (Manabe
et al., 2011; Béguer- Pon et al., 2012). However, because
both predation events observed in our study occurred in
highly turbid waters with low visibility (<0.5 m) off South
Carolina, the large sharks that prey on blacktip sharks
in such areas likely do not rely heavily on vision to target
prey (Gardiner et al., 2014). Given that blacktip sharks
are known to form large aggregations (Castro, 2011), it
is possible that individuals of conspecifics could have
dislodged other PSATs without consuming the blacktip
sharks, possibly explaining the premature PSAT detach-
ments observed in our study (Rogers et al., 2017).
Validation of acoustic telemetry for assessment of survival
Some individuals were tagged with both PSATs and
acoustic transmitters in our study, and the results indi-
cate that acoustic transmitters can be used effectively to
assess PRM in migratory, coastal shark species released
in regions with a high prevalence of acoustic receivers. In
our study, data obtained from acoustic transmitters indi-
cate the same survivorship outcome as data obtained from
the PSATs for all double- tagged individuals. In particular,
none of the 5 sharks for which mortalities were confirmed
with data from the PSATs were detected on an acoustic
receiver more than 10 d postrelease, although all 18 of the
individuals that were confirmed to have survived with
data from the PSATs, including those with PSATs that
were shed prematurely, were detected from 23 to 637 d
postrelease (mean: 238.4 d [SD 150.3]) (Table 4).
The electronic tags designed for assessing PRM (e.g.,
PSATs) can be cost prohibitive (Musyl et al., 2011; Whitney
et al., 2016; Rogers et al., 2017), forcing many researchers
to use relatively small sample sizes or to deploy tags only
on individuals that they believe have a chance at survival
(i.e., they do not want to “waste” a tag on an individual
that they believe will die), potentially biasing PRM esti-
mates (Rogers et al., 2017). Additionally, the vast majority
of PSATs (~80%) are shed before their programmed pop- up
date (Arnold and Dewar, 2001; Gunn and Block, 2001), and
others often fail to transmit data to the satellite system
altogether (Musyl et al., 2011). In our study, 67% of PSATs
deployed on surviving sharks were shed prematurely, and
2 PSATs failed to send data to the satellite system (fail-
ure rate of 8.3%). Therefore, in addition to the cost of such
electronic tags precluding the use of large sample sizes,
researchers also face relatively high tag failure rates.
The lower cost of acoustic transmitters could allow for
the inclusion of much larger sample sizes and, there-
fore, more robust assessments of PRM. Additionally, the
smaller size of acoustic transmitters, compared with the
sizes of other electronic tags (e.g., PSATs), could reduce
any potential effects of the tag on a shark’s behavior post-
release and, as a result, are likely more appropriate for the
assessment of PRM in smaller fish species. Although the
effectiveness of using acoustic transmitters to assess PRM
depends on the prevalence of acoustic receivers, the num-
ber of acoustic receivers deployed along the eastern coast
of the United States is increasing (Kneebone et al., 2013),
and the rising number of receivers will likely increase the
applicability of this method.
Physiological effects of capture
The stress experienced by captured sharks has tradi-
tionally been quantified through an assessment of the
acid- base status of blood. In this study, pH decreased
with increasing fight time for sharks caught from shore,
and lactate increased for sharks caught by using both
capture methods, indicating that blacktip sharks expe-
rienced proton (H+) loading in blood and tissues due to
the dissociation of lactic acid generated by anaerobic gly-
colysis (Skomal and Mandelman, 2012; Kneebone et al.,
2013). These findings indicate that rod- and- reel capture
of blacktip sharks results in blood acidosis that is at
least partially metabolic in origin, and they are consis-
tent with the results reported by Whitney et al. (2017).
Mandelman and Skomal (2009) found that increases in
pCO2 explained all of the variation in pH in blacktip
sharks captured with longlines, indicating that acidemia
in blacktip sharks caught with longlines is driven strictly
by respiratory acidosis. Because measurements of pCO2
made by the i- STAT system have not been validated, we
do not report pCO2 values from our study; therefore, the
potential contribution of CO2 to the observed acidosis
cannot be determined. Regardless, differences in lactate
profiles between studies indicate that the origin of the
acidosis could be associated with the type of gear used
and support the growing awareness that fishery- specific
assessments of the stress experienced by captured sharks
are necessary (Skomal, 2007; Heberer et al., 2010).
In general, exhaustive exercise leads to elevated concen-
trations of both glucose (Sherwin et al., 1980; Sheridan and
Muir, 1988) and potassium (Medbø and Sejersted, 1990).
Catecholamines are responsible for stimulating glucose
release from the liver during exercise (i.e., glycogenolysis;
Sherwin et al., 1980; Sheridan and Muir, 1988) to meet
310 Fishery Bulletin 118(3)
the energy demands of muscles, and it has been suggested
that the mobilization of glucose may be integral to survival
(Marshall et al., 2012). Increases in plasma potassium can
result from several factors, including a release of potas-
sium from muscle cells due to increased electrical activity
(Fenn, 1938; Sejersted and Sjøgaard, 2000) and a decrease
in plasma water due to increased intracellular lactate lev-
els that cause a net fluid shift from extracellular to intra-
cellular compartments (van Dijk and Wood, 1988; Wood,
1991). In our study, both glucose and potassium rose with
increasing fight times for sharks caught from shore but
not for sharks caught from charter boats. Given that fight
times did not differ between capture methods, elevated
glucose and potassium levels in sharks caught from shore
may reflect a higher degree of struggling on the line. More-
over, rhabdomyolysis, a syndrome characterized by muscle
necrosis and the release of intracellular electrolytes, often
due to muscle trauma associated with intense exercise,
can also lead to elevated potassium concentrations (Keltz
et al., 2013). The origin of the high glucose and potassium
concentrations in sharks caught from shore could simply
be a normal response to exercise, but conditions such as
rhabdomyolysis cannot be excluded.
The effect of fight time on numerous blood chemistry
characteristics for sharks caught from shore (pH, lactate,
hematocrit, potassium, and glucose), but not for sharks
caught from charter boats (only lactate), could be a result of
the tackle (i.e., fishing gear) used by the participating recre-
ational anglers. In particular, the majority of sharks caught
from shore were caught with spinning reels (76%), and the
majority of sharks caught from charter boats were caught
with conventional level- wind reels (85%). Because conven-
tional reels typically have a higher drag capacity than spin-
ning reels, making it more difficult for hooked fish to “run,”
conventional reels may restrict the movement of captured
sharks and, as a result, lessen the degree of muscular exer-
tion and metabolic stress. Additionally, many shore- based
fishermen put out far more fishing line initially (e.g., a cou-
ple hundred yards, in order to reach deeper water) than
anglers who fish from charter boats, and the additional
line may give the shark more room to run, both vertically
and horizontally, in the water column. Although traditional
sportfishing ethics has encouraged the use of light tackle
to give the fish a “fighting chance,” research results indi-
cate that slowly and carefully angling a fish can potentially
exacerbate the stress response (Malchoff and MacNeill6).
The results of our study support the notion that use of
heavy fishing tackle minimizes the fight time and there-
fore likely reduces the physiological stress experienced by
captured sharks. Future research employing the use of
serial blood sampling (e.g., sampling before and after han-
dling by anglers) could improve our understanding of the
effects of capture on shark species and of how those effects
are influenced by both gear type and handling technique.
6 Malchoff, M. H., and D. B. MacNeill. 1995. Guidelines to increase
survival of released sport fish. Released fish survival. Sport fish
fact sheet, 6 p. Cornell Coop. Ext., Sea Grant, Cornell Univ.,
Ithaca, NY. [Available from website.]
Overall, blacktip sharks caught on rod and reel (this
study; Whitney et al., 2017) have relatively less drastic
physiological disruptions than individuals caught on long-
lines (Mandelman and Skomal, 2009; Marshall et al., 2012)
and drumlines (Gallagher et al., 2014; Jerome et al., 2018).
Mean blood lactate values for blacktip sharks caught
on longlines (14.82 mmol/L, Mandelman and Skomal,
2009; 36.8 mmol/L, Marshall et al., 2012) and drumlines
(8 mmol/L, Gallagher et al., 2014; 6.3 mmol/L, Jerome
et al., 2018) are much higher than the mean lactate value
reported in our study (2.48 mmol/L). The concentrations of
plasma electrolytes in blacktip sharks caught on longlines
(potassium: 10.2 mmol/L; sodium: 298 mmol/L; Marshall
et al., 2012) are also higher than the values reported in our
study (potassium: 5.5 mmol/L; sodium: 273.3 mmol/L). Col-
lectively, the more drastic physiological changes observed
in blacktip sharks captured on longlines or drumlines are
likely due to the duration of the struggle on the line (e.g.,
up to 3 h, Mandelman and Skomal, 2009; 2–12 h, Marshall
et al., 2012; mean of 46.5 min, Jerome et al., 2018).
Prediction of postrelease mortality
Estimates of mortality for released fish are critical com-
ponents for estimation of total mortality and are therefore
of critical importance to fisheries managers. Because the
direct estimation of PRM across species and gear types is
likely unrealistic, previous studies have aimed to predict
PRM through the use of blood chemistry characteristics
(Moyes et al., 2006; Heberer et al., 2010; Schlenker et al.,
2016; Talwar et al., 2017) and various capture character-
istics (Manire et al., 2001; Hueter et al., 2006; Musyl and
Gilman, 2018). In our study, none of the blood chemistry
characteristics could be used to predict mortality with any
degree of significance. Because all blood samples were
screened for pH, lactate, hematocrit, sodium, chloride,
potassium, calcium, magnesium, and glucose, the lack of
ability to use any of the blood characteristics to predict
mortality indicates that many of the observed mortalities
were not a result of the potentially exhaustive exercise
associated with struggling on a fishing line.
In general, the assigned release condition was the best
predictor of PRM, indicating that many of the sharks that
died had observable signs of injury or trauma. Noticeable
injuries were often related to the location of the hook and
typically involved significant bleeding. However, 18.4% of
individuals assigned a release condition of excellent died
postrelease, indicating that many succumbing individuals
have no sign of physical injury or trauma and that assign-
ment of release condition can be somewhat subjective.
In our study, 6 of the 81 tagged blacktip sharks were
considered to be foul- hooked, with hook locations of the
basihyal, throat, gut, and tail. Three of the 6 foul- hooked
sharks died within 10 d of release, for a PRM rate of 50%
for foul- hooked sharks. Hook location has been shown to
influence survival in many species (Muoneke and Chil-
dress, 1994), and mortality is often associated with dam-
age to gills or visceral tissue caused by deeply embedded
hooks (Heberer et al., 2010). All recreational anglers in
Weber et al.: Stress response and postrelease mortality of Carcharhinus limbatus captured in recreational fisheries 311
our study chose to use circle hooks—again, no input was
provided by the authors on the type or size of hook that
should be used. Therefore, it is possible that instances
of foul- hooking would have been higher if J hooks were
used (Prince et al., 2002; Promjinda et al.7; Pacheco et al.,
2011), although Whitney et al. (2017) found no difference
in the incidence of foul- hooking or PRM between the use of
J hooks and the use of circle hooks.
The hook location not only can influence PRM through
physical trauma (e.g., damage to gills or visceral tissue)
but also can impair locomotion and a shark’s ability to ven-
tilate properly (Heberer et al., 2010). The blacktip shark
is a ram- ventilating species that must move forward to
subject its gills to ventilation because the orientation and
morphology of elasmobranch gill slits preclude water flow
over gills when individuals are pulled backward (Heberer
et al., 2010; Wegner et al., 2010). Therefore, sharks hooked
in the tail (i.e., caudal fin) or tail- wrapped in the fishing
line and reeled in backward experience reduced water
flow over the gills and can ventilate only during brief peri-
ods of forward swimming. Indeed, in our study, the only
shark hooked in the tail died postrelease. Additionally,
the shark that was hooked in the jaw but tail- wrapped
in the line and dragged backward also died postrelease.
The survival implications for sharks hooked in the tail are
well- documented; for example, in another study, 78% of
common thresher sharks (Alopias vulpinus) hooked in the
tail died postrelease (Sepulveda et al., 2015).
Overall, PRM rates in our study are similar for black-
tip sharks captured in recreational fisheries from shore
(17.1%) and from charter boats (20.0%) and are higher than
PRM rates that have been reported for many other shark
species caught on rod and reel. The agreement between the
results we obtained from analyzing data from the acous-
tic transmitters and from the PSATs verify that acous-
tic transmitters can be used to effectively assess PRM in
migratory, coastal shark species released in regions with a
high prevalence of acoustic receivers (e.g., the eastern coast
of the United States). Significant physiological disruptions
in the blood chemistry of sharks were identified, and fight
time had a significant effect on pH, lactate, hematocrit,
potassium, and glucose. Fifty percent of foul- hooked sharks
died postrelease, with important implications for the use of
gear and methods that reduce foul- hooking.
Acknowledgments
We thank all participating recreational fishermen and
all acoustic telemetry data contributors, including staff
of the FACT and ACT Networks. We are grateful to A.
Galloway, A. Bland, C. Morgan, D. Edmunds, C. Innis, and
R. Knotek. Additionally, we thank M. Janech, L. Burnett,
7 Promjinda, S., S. Siriraksophon, N. Darumas, and P. Chaidee.
2008. Efficiency of the circle hook in comparison with J- hook in
longline fishery. In The ecosystem- based fishery management in
the Bay of Bengal, p. 167–180. Dep. Fish., Minist. Agric. Coop.,
Bangkok, Thailand. [Available from website.]
and both the anonymous reviewers for their comments
on previous versions of this manuscript. This work was
supported by the NOAA Cooperative Research Program
(grant no. NA16NMF4540081), the American Elasmo-
branch Society, and the Slocum- Lunz Foundation. This
paper is contribution 829 of the South Carolina Marine
Resources Center.
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