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Residency of bull sharks, Carcharhinus leucas
(Carcharhiniformes: Carcharhinidae), at San Pedrillo Islet
in Islas Murciélago, North Pacific of Costa Rica
Andrés López-Garro1; https://orcid.org/0000-0001-7834-5306
Ilena Zanella1; https://orcid.org/0000-0002-3820-7643
1. Asociación Conservacionista Misión Tiburón, Playas del Coco, Guanacaste, Costa Rica; alopez@misiontiburon.org,
izanella@misiontiburon.org
Received 21-XII-2020. Corrected 08-II-2021. Accepted 05-V-2021.
ABSTRACT
Introduction: The bull shark, Carcharhinus leucas, is particularly vulnerable to anthropogenic actions because
of its permanence in coastal ecosystems; populations depletion is registered in different places around the world.
Aggregations of bull sharks have been reported in the North Pacific of Costa Rica, at Islas Murciélago, within
the Guanacaste Conservation Area.
Objective: To study the residency of bull sharks at San Pedrillo islet, Islas Murciélago.
Methods: During the study period (June 2013 to February 2015) we used passive telemetry to tag 10 bull sharks.
Results: All the sharks tagged were females, they were detected on 59 798 occasions by the acoustic receiver
deployed in San Pedrillo. Acoustic signals from tagged sharks were received for a total period of 1 to 229 days
(mean = 73.9 ± 71.3 days), with the last detections occurring on 9 January 2015. The Residency Index for each
tagged shark across the entire monitoring period ranged from 0.41 to 1.00. The bull shark activity showed a
significant pattern throughout the day at the receiver that specifically corresponded with the daily light cycle.
Conclusions: This study concludes that San Pedrillo is an aggregation site (cleaning station) for bull sharks (C.
leucas), possibly related to reproduction and not feeding behaviors.
Key words: Carcharhinus leucas; Guanacaste; tagging; acoustic telemetry; aggregation site.
López-Garro, A., & Zanella, I. (2021). Residency of bull sharks,
Carcharhinus leucas (Carcharhiniformes: Carcharhinidae),
at San Pedrillo Islet in Islas Murciélago, North Pacific of
Costa Rica. Revista de Biología Tropical, 69(Suppl. 2),
S246-S255. https://doi.org/10.15517/rbt.v69iS2.48321
https://doi.org/10.15517/rbt.v69iS2.48321
The Archipelago of Islas Murciélago is
part of the Marine Sector of the Guanacaste
Conservation Area, in the north Pacific of
Costa Rica. One of the top predators of this
area is the bull shark, Carcharhinus leucas
(Valenciennes 1839), which is a cosmopolitan
tropical and subtropical species commonly
found in coastal ecosystems such as estuar-
ies, lagoons, and river mouths thanks to their
capacity to enter freshwater systems (Com-
pagno, 1984). Like other elasmobranchs, the
bull shark uses estuaries and river mouths as
nurseries. The fact that these systems are also
of high productivity could be one of the reasons
why adult female bull sharks prefer these sites
to give birth (Curtis, Parkyn, & Burgess, 2013).
Several authors have reported bull sharks using
coastal ecosystems for protection and food
during their early life stages (Simpfendorfer,
Greitas, Wiley, & Heupel, 2005; Werry &
Clua, 2013). Nursery grounds for bull sharks
have been documented in the Gulf of Mexico
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and the east coast of Florida (Curtis, Adams, &
Burgess, 2011). Bull shark juveniles can access
rivers to feed, preying on species that migrate
between rivers and oceans during tidal changes.
Numerous studies have also reported the pref-
erence or habitat fidelity of adult bull sharks to
shallow waters of coastal habitats, particularly
to those with a high input of freshwater, such as
river mouths and estuaries (Bangley, Paramore,
Shifman, & Rulifson, 2018; Brunnschweiler,
Queiroz, & Sims, 2010; Carlson, Ribera, Con-
rath, Heupel, & Burgess, 2010; Graham et al.,
2016; Heupel et al., 2015). The permanence of
bull sharks in coastal ecosystems makes them
vulnerable to anthropogenic actions like habitat
degradation, pollution, and fishing exploitation
(Curtis et al., 2013; Thorson, 1971; Werry &
Clua, 2013).
Bull shark population depletion is reported
in different places around the world, such as
the Gulf of Mexico and the southwest Atlantic
of Brazil (Almeida, McGrath, & Ruffino, 2001;
Powers et al., 2013). In Central America, spe-
cifically in Lake Nicaragua, exploitation of bull
sharks started in the 1960s, when they were
consumed domestically and exported overseas
(Thorson, 1982). In the 1970s an Asiatic shark
fin processing plant started to operate near
Granada. In Lake Nicaragua, the bull shark
fishery industry collapsed in the 1980s, yet the
population has still not recovered from overex-
ploitation (McDavitt, 2002).
Bull sharks currently have a higher eco-
nomic value as a tourist resource, related to
recreational diving, than as a commercial spe-
cies. For example, at Cabo Pulmo National
Park (CPNP), Mexico, the bull shark is one of
the main attractions for tourists. According to
Pasos-Acuña (2018), bull shark recreational
diving at CPNP represents more than $7.5 mil-
lion each year. Worldwide, it is estimated that
half a million people are interested in shark
diving, generating more than US$314 million
per year and more than 10 000 jobs. Further-
more, it is expected that in the next 20 years
shark tourism is going to double at a global
scale, potentially generating more than US$750
million annually (Cisneros, Barnes, Navarro, &
Rashidsumaila, 2013).
In Costa Rica, bull shark juveniles and
adults are occasionally caught by artisanal
fishermen (bottom line and gill nets) who fish
close to river mouths and estuaries (López,
Arauz, Zanella, & Le Foulge, 2009; López &
Zanella, 2015). The exploitation of bull sharks
in Costa Rica has been developed without
any specific management regulation. The San
Pedrillo islet, located at Islas Murciélago archi-
pelago, has been identified empirically as an
aggregation site for bull sharks, the only one
reported for the species in Costa Rica. During
the rainy season (May-November), local com-
munities such as Playas del Coco, Tamarindo,
and Cuajiniquil, directly benefit from SCUBA
diving with bull sharks in a completely natural
environment (Davis & Klapfer, 2018). In this
study, we used acoustic telemetry to monitor
the residence of adult bull sharks at the San
Pedrillo islet. This study will add new informa-
tion for the design of conservation strategies to
improve the protection of the bull shark popu-
lation at the Conservation Area of Guanacaste
and surrounding areas.
MATERIALS AND METHODS
Study area: The archipelago of Islas Mur-
ciélago is located in the north Pacific of Costa
Rica, 5 km off mainland Costa Rica, and is
comprised of five islands and ten islets, one
of them being San Pedrillo (10º51’12.4”N &
85º57’32.5” W) (Denyer, Cortés, & Cárdenes,
2005). As part of the Área de Conservación
Guanacaste (ACG, Guanacaste Conservation
Area), the Islas Murciélago belong to a UNES-
CO World Heritage Site; part of the Sistema
Nacional de Áras de Conservación (SINAC,
National System of Conservation Areas of
Costa Rica) from the Ministry of Environment
of Costa Rica (SINAC, 2013). The archipelago
is a no-take Marine Protected Area with an
extension of 43,000 ha where only tourism
activities are allowed. The marine biodiversity
of Islas Murciélago is influenced by a seasonal
upwelling (from December to March) that rises
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cold deep water masses that generate an intense
effect on the distribution of nutrients and
plankton (Jiménez, 2016; Rodríguez, Alfaro, &
Cortés, 2021).
Acoustic array and shark tagging: Tag-
ging was performed between June 2013 and
September 2014 at San Pedrillo islet between
18 and 30 m depth, where the aggregation of
adult bull sharks is known to occur (Davis
& Klapfer, 2018). An acoustic receiver was
deployed at the same site using SCUBA gear.
The tags or acoustic transmitters were V16-4H
with external cases (Vemco Ltd., Halifax, Nova
Scotia, Canada), which were tethered to stain-
less steel darts. Scuba divers inserted the darts
into the muscle of the bull sharks at the base of
the first dorsal fin. The researchers reported the
sex of each shark tagged (presence or absence
of claspers) and estimated the size (total length)
of the shark. The sharks were tagged during
the rainy season when the upwelling is not
occurring and ocean conditions favor diving
activities and underwater tagging. Transmitters
were set to be silent (delay) for a random-
ized period of 40 to 140 s between each pulse
train and had a battery life of approximately 4
years. Each transmitter tag conveyed a specific
code for an individual shark, and periodically
emitted a pulse train of closely spaced 69 kHz
pings detected by the receiver VR2W (Vemco
Ltd., Halifax, Nova Scotia, Canada), which
was deployed before tagging on the 12th
of June 2013. The receiver was placed at a
depth of 30-35 m in a sandy bottom close to
the aggregation site, next to the San Pedrillo
islet. The receiver was anchored on a 65 kg
cement block attached to a stainless-steel cable
and suspended in the water column (approxi-
mately 3-5m from the bottom) with a buoy. The
receiver stored the information emitted from
the transmitters (date, time of the detection,
and transmitter number for each individual
pulse train) along a 250-300 m radius, veri-
fied via range tests. The detection of the tags
decreased abruptly after 250 m, and tags were
not detected at distances greater than 300 m.
Receiver data was downloaded approximately
every 5 months, for 1.5 years (June 2013 to
February 2015).
Data analysis: The data recorded by the
acoustic receiver in San Pedrillo was down-
loaded using the software VUE version 2.0.6.
Shark detections during the study period were
plotted using the ‘ggplot’ package in R version
3.6.3 (R Development Core Team R, 2014).
To determine whether an individual was pres-
ent on any day close to the receiver, we set a
minimum of three detections as a metric. The
detections were compared: a) between indi-
viduals using the no-parametric test Kruskall
Wallis; b) between months of the rainy season
(May-November) and months of the dry season
(December-April) using the no-parametric test
Wilcoxon (Infostat, 2008). The Residency
Index (RI) was further calculated for each bull
shark tagged to better examine occurrence
patterns across the array. RI was defined as
the number of days a bull shark was detected
within the receiver array, divided by the num-
ber of days monitored (i.e. number of days
from the tagging date to the last date detec-
tions were received for all transmitters) (Espi-
noza, Farrugia, & Lowe, 2011; Papastamatiou,
Friedlander, Caselle, & Lowe, 2010; Zanella,
López, & Cure, 2019); RI values range from
0 to 1, with a value of 1 indicating the highest
possible residency at the receiver array. The
average number of detections per individual
tagged shark throughout a daily cycle was plot-
ted using ‘ggplot’ and ‘plyr packages in R
version 3.6.3 (R Development Core Team R,
2014). The environmental variables of Sea Sur-
face Temperature, SST (°C) and Chlorophyll-α
concentrations (mg/m3) were downloaded from
NASAs OceanColor platform (www.ocean-
color.nasa.org), with a resolution of 4 km,
whose source is the National Oceanic and
Atmospheric Administration (NOAA). Those
files were downloaded in HDF format. Data
was downloaded monthly from June 2013 to
February 2015. Processed data was exported
as an ASCII file using the QGIS and DIVAGIS
software, these layers were used to extract the
information from at least 6 points around the
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Islas Murcielago, to an optimal representation
of the area. Residual normality test (Shapiro)
and homoscedasticity of variances test (Lev-
ene) were conducted. Since data was normal
and homoscedastic, comparisons were made
between seasons of the year (dry and rainy)
with paired t-student tests, performed with 95
% confidence (Infostat, 2008). We compared
the detections of tagged sharks at the receiver
between day (06:00-17:00) and night hours
(18:00-5:00), using the Wilcoxon nonpara-
metric test (Infostat, 2008), and we described
the average number of detections per indi-
vidual tagged shark at the receiver throughout
a daily cycle.
Research Permit: All the activities related
to this study were done in compliance with
the resolution of scientific permits Nº ACG-
PI-004-2013, Nº ACG-PI-017-2014 and Nº
ACG-PI-030-2015. Such permits were autho-
rized by the Área de Conservación Guana-
caste (ACG, Guanacaste Conservation Area)
of the SINAC, Ministry of Environment of
Costa Rica.
RESULTS
Between June 2013 and September 2014,
we tagged ten adult female bull sharks (C. leu-
cas) at San Pedrillo, Islas Murciélago. Based on
the approximate size of the individuals (> 2 m
total length) we classified them as “adults” fol-
lowing the maturity size estimation determined
in the Gulf of México and Northern Brazil
(Cruz-Martínez, Chiappa-Carrara, & Arenas-
Fuentes, 2004; Niella, Afonso, & Hazin, 2017).
During the study period (June 2013 to February
2015) a total of 59,798 detections were record-
ed by the acoustic receiver. Acoustic signals
from tagged sharks were received for a total
period of 1 to 229 days (mean = 73.9 ± 71.3
days), with the last detections occurring on 9
January 2015 (Table 1). The number of detec-
tions was not significantly different between
individuals (H = 9.00, P > 0.05).
The detections of tagged bull sharks
recorded in the receiver were higher during the
rainy season (May-November) compared with
the detections recorded during the dry season
(December-April) (W = 1593.00, P < 0.05), as
more than 80% of the detections were recorded
between May and November. The months of
July and August together provided almost 50%
of all detections, therefore they are considered
the most outstanding months for bull sharks
in this area. Even though some sharks were
detected during the dry season (December-
February), less than 20% of detections were
registered for the first months of the year (Fig.
1, Table 2).
TABLE 1
Residency of Carcharhinus leucas monitored in San Pedrillo, Islas Murciélago, Costa Rica. Sex: F=females;
Residency Index (RI): the number of days a shark was detected within the receiver array divided by
the number of days monitored. All sharks were detected at the receiver
Tag # Tag ID Tagging
date
Last d
etection Sex Size
(m)
No of
detections
Days
monitored
Days
detected RI
1 30322 20-06-13 04-02-14 F >2 16127 229 193 0,84
2 58967 12-06-14 26-09-14 F >2 10520 75 68 0,91
3 25468 27-09 -14 09-01-15 F >2 16804 135 135 1,00
4 25466 27-09-14 09-01-15 F >2 5715 135 59 0,44
5 58968 12-06-14 21-07-14 F >2 5170 39 33 0,85
6 25465 27-09-14 13-10-14 F >2 1766 48 43 0,90
7 25467 15-06-14 10-07-14 F >2 1744 25 14 0,56
8 30321 20-06-13 12-07-13 F >2 1238 22 9 0,41
9 30320 15-06-14 15-07-14 F >2 707 30 28 0,93
10 30319 12-06-14 12-06-14 F >2 7 1 1 1,00
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Regarding environmental variables (SST
and Chlorophyll-α concentrations), the tem-
perature was significantly higher during the
months of the rainy season compared with the
months of the dry season (t = 8.82, P < 0.0001);
whereas the Chlorophyll-α concentrations were
significantly lower during the months of the
rainy season compared with the months of the
dry season (t = -7.79, P < 0.0001; Table 2).
The Residency Index for each tagged shark
across the entire monitoring period ranged from
0.41 to 1.00 (Table 1) and there wasn´t a clear
tendency to monthly variation in residency
metrics (Fig. 2). During the time of this study,
bull shark activity showed a significant pattern
throughout the day at the receiver that specifi-
cally corresponded with the daily light cycle.
Detections were significantly highest from the
early morning to late afternoon (6:00 h to 18:00
h) (W = 6862.50, P < 0.0001) (Fig. 3).
DISCUSSION
This study confirmed that adult bull sharks
use San Pedrillo as an aggregation site. This
islet, located in the Marine Protected Area of
the ACG, is a site where bull sharks remain
for long periods, especially during the rainy
season (May-November), mostly with short
absences of 1 to 3 days. Even though some
bull sharks visited San Pedrillo during the dry
TABLE 2
Average monthly detections of Carcharhinus leucas, Sea Surface Temperature (SST, °C) and Chlorophyll-α
concentrations (mg/m3) monitored in San Pedrillo, Islas Murciélago, Costa Rica
Month Average of Detections ± SD Average of SST (ºC) ± SD Average of Chlorophyll-α (mg/m3) ± SD
June 517.66 ± 424.15 27.89 ± 0.01 0.22 ± 0.08
July 2 673 ± 2 126.69 28.83 ± 0.01 0.41 ± 0.00
August 2 486.40 ± 2 268.54 29.24 ± 0.03 0.42 ± 0.01
September 1 550 ± 942.33 29.44 ± 0.02 0.31 ± 0.05
October 1 089.50 ± 1 054.40 28.92 ± 0.02 0.32 ± 0.00
November 1 817.00 ± 1 553.30 28.66 ± 0.02 0.74 ± 0.00
December 2 899.00 ± 1 951.07 27.87 ± 0.01 1.36 ± 0.07
January 1 170.33 ± 922.91 27.31 ± 0.01 2.36 ± 0.03
Febraury 5 ± 0 26.97 ± 0.18 4.75 ± 0.03
March 0.00 28.52 ± 0,06 0.89 ± 0,00
April 0.00 28.35 ± 0,01 0.65 ± 0,00
May 0.00 30.02 ± 0,37 0.21 ± 0,06
Fig. 1. Number of detections per month of bull sharks
(Carcharhinus leucas) tagged at San Pedrillo, Islas
Murciélago, ACG, Costa Rica during the study period
(June 2013-Febraury 2015).
Fig. 2. Residency Index of bull sharks (Carcharhinus
leucas) tagged at San Pedrillo, Islas Murciélago, ACG,
Costa Rica during the study period (June 2013-Febraury
2015).
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months, less than 20% of total detections cor-
respond to December to February. This study
also confirmed that during the dry season the
marine area around Islas Murcielago experi-
ment a significant decrease of the temperature
and a significant increment of Chlorophyll con-
centration, as a result of the seasonal upwelling
reported for the North Pacific of Costa Rica,
produced by strong winds from the Caribbean
(Jiménez, 2016; Rodríguez et al., 2021). These
changes in environmental variables correspond
to a significant decrease in the detections of bull
sharks in the study area. Such behavior patterns
of temporary residence by bull sharks have
also been reported in South Africa, Mexico and
Fiji, where authors make a close connection
between residence and change in water tem-
perature and food availability (Brunnschweiler
& Barnett, 2013; Brunnschweiler, Queiroz,
& Sims, 2010; Daly et al., 2014). Daly et al.
(2014) described a site known as “Pinnacle
reef” in Mozambique, as an important aggrega-
tion site for adult bull sharks who reside there
for long periods, mainly during the summer
austral months (November-May).
Several studies have reported local migra-
tions of bull sharks, which is correlated to
seasonal changes (Daly et al., 2014; Niella,
Afonso, & Hazin, 2017). Satellite tags on
bull sharks have revealed important coastal
migrations, thus contradicting many theories
that this species is sedentary in coastal waters,
such is the case in the Gulf of Mexico, where
tagged bull sharks covered between 2 to 1 500
km in only 85 days, using primarily temper-
ate shallow waters (> 20 m depth) (Carlson
et al., 2010). Another example is a male bull
shark who covered more than 3 000 km in
75 days, mostly waters > 20 m depth along
the Brazilian coast (Niella, Afonso, & Hazin,
2017). Similarly, off the coast of Australia,
Heupel et al. (2015) described migration pat-
terns of bull sharks with a range greater than
1 700 km. Some authors suggest that the Great
Barrier Reef plays an important ecological
role for adult bull sharks off the east coast of
Australia, where sharks move between differ-
ent coastal habitats primarily in the search for
warmer waters.
At San Pedrillo, the lowest number of
detections were reported during the night, sug-
gesting that the bull sharks take part in local
migrations outside of San Pedrillo, possibly for
feeding purposes. The data also revealed that
most of the tagged sharks in San Pedrillo made
daily migrations during the entire study period.
Such results can be compared to other studies
like the one off the east coast of Africa (Daly
et al., 2014), which showed bull sharks’ loyalty
to “Pinnacle reef” was higher during daytime
than at nighttime. Brunnschweiler and Barnett
(2013), conclude that bull sharks move during
the daytime at a local scale mainly for feeding
purposes, utilizing different coastal habitats
based on the different times of the day.
All the sharks tagged in this study were
females, no males were observed during the
dives for tagging. Local divers reported the
presence of mostly females in the study area
and they observed some of them with scars
from bites along their body’s sides (Fig. 4), and
in few occasions, divers have reported a chas-
ing behavior of male individuals to females.
At the same time, cleaner fishes around rocky
reefs are constantly observed in San Pedrillo
dive site (pers. comm. Vallejos E., Rojas E.,
Berrocal D., 2019).
Fig. 3. Average number of detections per individual tagged
shark at the receiver throughout a daily cycle, San Pedrillo,
Islas Murciélago, Costa Rica, during the study period (June
2013-February 2015).
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In Costa Rica, aggregations of sharks’
adult females were reported for the scalloped
hammerhead shark (Sphyrna lewini) in the
oceanic Isla del Coco (Cocos Island), where the
sharks aggregate in specific cleaning stations
(Nalesso et al. 2019). Nalesso et al. (2019) con-
cluded that the scalloped hammerhead sharks
in Isla del Coco were more resident compared
with other oceanic islands (RI = 0.52 ± 0.31),
demonstrating that the sharks are strongly
associated with that island. The residence of
the bull shark (RI = 0.77 ± 0.21) in San Pedrillo
suggests that the site is an important aggrega-
tion site for the species. The values of RI (0.44-
1.00) reported in this study are higher than the
reported for “Pinnacle reef” in Mozambique,
where the sharks showed an RI influenced by
different factors such as reproductive activity,
environmental fluctuations, prey availability,
among others (Daly et al., 2014).
We concluded that San Pedrillo is a tem-
porary residence for the bull shark, and it is an
important aggregation site related to reproduc-
tion, not feeding behaviors. It is also impor-
tant to highlight that diving activities at San
Pedrillo are carried out during the day (between
8:00 and 12:00) in the rainy season when
environmental conditions allow the arrival of
tourist boats to the site. The higher detection
of bull sharks during daytime hours and their
interaction with recreational divers makes it
necessary to promote good practices for recre-
ational diving in San Pedrillo. At the moment,
no shark attacks have occurred at the study site,
but it has already been shown that the greatest
impact between divers and bull shark occurs
when divers perform irresponsible practices
(Pasos-Acuña, 2018).
San Pedrillo islet is a critical site for the
bull shark, however, more studies are needed
to identify feeding and nursery grounds in the
Guanacaste Conservation Area and surround-
ing areas. The identification and protection
of critical habitats for this iconic species will
bring environmental and social-economic ben-
efits to local communities of Guanacaste.
Management recommendations
1. Long residence periods of bull sharks in
the islet of San Pedrillo, as well as their
local migrations, make them a vulnerable
Fig. 4. Bull shark (Carcharhinus leucas) female with bite scars observed at San Pedrillo, Islas Murciélago, Costa Rica.
Photography credit: Daniel Berrocal, Okeanos Aggressor.
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species to fishing pressures and habitat
loss. Therefore, we recommend increasing
conservation and protection efforts at Islas
Murciélago, especially at San Pedrillo, a
site considered essential and critical for
the species.
2. It is important to expand the knowledge
and understanding of bull shark habitat use
in San Pedrillo. Efforts should also focus
on the identification of nursery and fee-
ding grounds for the creation of effective
conservation measures that guarantee the
protection of the species during all its life
cycle. The boundary of the MPA is located
less than 2 km from San Pedrillo, therefo-
re, we recommend the creation of a buffer
zone to decrease the impact of fisheries on
the species. The bull shark is a top predator
and an umbrella species, the conservation
of its critical habitats will improve the pro-
tection of other marine species.
3. Its urgent to involve local communities
in the protection of bull sharks through
the implementation of training and edu-
cational environmental programs. The
protection of the species will bring envi-
ronmental and socio-economic benefits
to the local communities that base their
economy on tourism.
4. Demonstrating the socio-economic bene-
fits of bull shark conservation will be
essential to improve the involvement of
local stakeholders and governmental ins-
titutions, thus is necessary to estimate the
economic value that bull sharks represent
to the local communities, especially for
Playas de Coco and Cuajiniquil.
Ethical statement: authors declare that
they all agree with this publication and made
significant contributions; that there is no con-
flict of interest of any kind; and that we
followed all pertinent ethical and legal proce-
dures and requirements. All financial sources
are fully and clearly stated in the acknowled-
gements section. A signed document has been
filed in the journal archives.
ACKNOWLEDGMENTS
The study was successfully carried out
thanks to the collaboration and support of
various organizations, institutions, divers, and
ocean lovers. Thanks to the team of Seamaster
Costa Rica, (especially to Cristiano Paoli for
helping during the tagging), Área de Conser-
vación Guanacaste (ACG, Guanacaste Con-
servation Area), Carlos Hiller Submarine Arts,
Fallas family, Consorcio Primos Titin, Veerle
Roelandt, and Rufford Small Grants.
RESUMEN
Residencia del tiburón toro, Carcharhinus leucas,
(Carcharhiniformes: Carcharhinidae) en
el islote de San Pedrillo, Islas Murciélago,
Pacífico Norte de Costa Rica
Introducción: El tiburón toro (Carcharhinus leucas) es
una especie tropical y subtropical que habita ríos, estuarios
y aguas costeras.
Objetivo: Estudiar la residencia del tiburón toro en
San Perdillo, Islas Murciélago, Área de Conservación
Guanacaste.
Métodos: Durante el período de estudio (junio de 2013 a
febrero de 2015) se marcaron 10 tiburones toro con teleme-
tría acústica en San Pedrillo.
Resultados: los tiburones marcados fueron todos hembras
y fueron detectados en 59 798 ocasiones por el receptor
acústico desplegado en San Pedrillo. Las señales acústi-
cas de los tiburones marcados se recibieron durante un
período total de 1 a 229 días (media = 73.9 ± 71.3 días), y
las últimas detecciones ocurrieron el 9 de enero de 2015.
El índice de residencia de cada tiburón marcado durante
todo el período de seguimiento osciló entre 0.41 y 1.00. La
actividad del tiburón toro mostró un patrón significativo a
lo largo del día en el receptor que se corresponde específi-
camente con el ciclo de luz diario.
Conclusiones: Este estudio concluyó que San Pedrillo es
un sitio de agregación (estación de limpieza) para el tibu-
rón toro, posiblemente relacionado con comportamientos
de reproducción y no de alimentación; y es un sitio crítico
para la especie. Se necesitan más estudios para identificar
áreas de alimentación y cría en el Área de Conservación de
Guanacaste y áreas circundantes.
Palabras clave: Carcharhinus leucas; Guanacaste; marca-
je acústico; telemetría pasiva; sitio de agregación.
REFERENCES
Acuña, D., Smith, A. N. H., Hammerschlag, N., Hearn, A.,
Anderson, M. J., Calich, H., … Salinas de León, P.
(2017). Residency and movement patterns of an apex
S254
Revista de Biología Tropical, ISSN: 2215-2075 Vol. 69(Suppl. 2): S246-S255, October 2021 (Published Oct. 30, 2021)
predatory shark (Galeocerdo cuvier) at the Galapagos
Marine Reserve. PLoS ONE, 12(8), e0183669.
Alfaro, E. J., Cortés, J., Alvarado, J., Jiménez, C., Sánchez,
C., Nivia, J., León, A., & Ruiz, E. (2012). Clima y
temperatura sub-superfical del mar en Bahía Culebra,
Costa Rica. Revista de Biología Tropical, 60(Supple-
ment 2), S159-S171.
Almeida, O. T, McGrath, D. G., & Ruffino, M. L. (2001).
The commercial fisheries of the lower Amazon: an
economic analysis. Fish Management Ecology, 8,
253-269.
Amador, J. A., Alfaro, E. J., Lizano, O. G., & Magaña, V.
O. (2006). Atmospheric forcing in the Eastern Tro-
pical Pacific: A review. Progress In Oceanography,
69(2),101-142.
Bangley, C., Paramore, L., Shifman, D., & Rulifson, R. A.
(2018). Increased abundance and nursery habitat use
of the bull shark (Carcharhinus leucas) in response to
a changing environment in a warm-temperate estuary.
Scientific Reports, 8, 6018.
Barnett, A., Abrantes, K. G, Seymour, J., & Fitzpatrick, R.
(2012). Residency and spatial use by reef sharks of an
isolated seamount and its implications for conserva-
tion. PLoS ONE ,7(5), e36574.
Brunnschweiler, J. M., & Barnett, A. (2013). Opportunistic
visitors: long-term behavioral response of bull sharks
to food provisioning in Fiji. PLoS ONE, 8(3), e58522.
Brunnschweiler, J. M., Queiroz, N., & Sims, D. W. (2010).
Oceans apart? Short-term movements and behavior
of adult bull sharks Carcharhinus leucas in Atlantic
and Pacific Oceans determined from pop-off sate-
llite archival tagging. Journal of Fish Biology, 77,
1343-1358.
Carlson, J. K., Ribera, M. M., Conrath, C. L., Heupel, M.
R., & Burgess, G. H. (2010). Habitat use and move-
ment patterns of bull sharks Carcharhinus leucas
determined using pop-up satellite archival tags. Jour-
nal of Fish Biology, 77, 661-675.
Cisneros, A. M., Barnes M., Navarro E., & Rashidsumaila,
U. (2013). Global economic value of shark ecotou-
rism: implications for conservation. Oryx, 47(3),
381-388.
Cruz-Martínez, A., Chiappa-Carrara, X., & Arenas-Fuen-
tes, V. (2004). Age and growth of the bull shark,
Carcharhinus leucas, from southern Gulf of Mexico.
Journal of Northwest Atlantic Fishery Science, 37,
367-374.
Compagno, L. J. V. (1984). FAO: Species Catalog Vol 4:
Sharks of the World. An Annotated and Illustrated of
Sharks Species Know to Date. Part 1 and 2. FAO Fish
Synopsis, 125.
Curtis, T. H., Adams, D. H., & Burgess, G. H. (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.
Curtis, T., Parkyn, D., & Burgess, G. (2013). Use of
human-altered habitats by bull sharks in a Florida
nursery area. Marine and Coastal Fisheries: Dyna-
mics Management and Ecosystem Science, 5, 28-38.
Daly, R., Smale, M. J., Cowley, P. D., & Froneman, P. W.
(2014). Residency patterns and migration dynamics
of adult bull sharks (Carcharhinus leucas) on the East
coast of southern Africa. PLoS ONE, 9(10), e10935.
Davis, G., & Klapfer, A. (2018). Costa Rica Blue: The
Underwater Guide. San José, Costa Rica: Blue
Publishing, S.A.
Denyer, P., Cortés, J., & Cárdenes, G. (2005). Hallazgo
de dunas fósiles de final del Pleistoceno en las Islas
Murciélago, Costa Rica. Revista Geológica de Amé-
rica Central, 33, 29-44.
Espinoza, M., Farrugia, T. J., & Lowe, C.G. (2011) Habitat
use, movements and site fidelity of the gray smooth-
hound shark (Mustelus californicus, Gill 1863) in a
newly restored southern California estuary. Journal
of Experimental Marine Biology and Ecology, 401,
63-74.
Garla, R. C., Chapman, D., Shivji, M. S., Wetherbeed,
B. M., & Amorim, A. F. (2006). Habitat of juveni-
le Caribbean reef sharks, Carcharhinus perezi, at
two oceanic insular marine protected areas in the
southwestern Atlantic Ocean: Fernando de Noronha
Archipelago and Atol das Rocas, Brazil. Fisheries
Research, 81, 236-241.
Graham, F., Rynne, P., Estevanez, M., Luo, J., Ault, J., &
Hammerschlag, N. (2016). Use of marine protected
areas and exclusive economic zones in the subtropical
western North Atlantic Ocean by large highly mobile
sharks. Diversity and Distributions, 22, 534-546.
Heupel, M. R., Simpfendorfer, C. H., Espinoza, M.,
Smoothey, A. F., Tobin, A., & Peddemors, V. (2015).
Conservation challenges of sharks with continental
scale migrations. Frontiers in Marine Science, 2, 12.
https://doi.org/10.3389/fmars.2015.00012
InfoStat (2008). InfoStat, versión 2008. Manual del Usua-
rio. Grupo InfoStat, FCA, Universidad Nacional de
Córdoba. Argentina: Editorial Brujas Argentina.
Jenson, N. H. (1976). Reproduction of the bull shark,
Carcharhinus leucas, in the Lake Nicaragua-Rio San
Juan System. Investigations of the Ichthyofauna of
Nicaraguan Lakes, 40, 539-559.
Jiménez, J. A. (2016). El Domo Térmico de Costa Rica: Un
oasis de productividad frente a las costas del Pacífico
S255
Revista de Biología Tropical, ISSN: 2215-2075, Vol. 69(Suppl. 2): S246-S255, October 2021 (Published Oct. 30, 2021)
Centroaméricano. San José, Costa Rica: Fundación
MarViva.
Lizano, O., & Alfaro, E. (2015). Dinámica atmosférica y
oceánica en algunos sitios del Área de Conservación
Guanacaste (ACG), Costa Rica. Revista de Biología
Tropical, 62(Supplement 4), S17-S31.
López, A., Arauz, R., Zanella, I., & Le Foulge, L. (2009).
Análisis anual de las capturas de tiburones y rayas
en las pesquerías artesanales de Tárcoles, Pacífico
Central de Costa Rica. Revista Ciencias Marinas y
Costeras, 1, 145-157.
López, A., & Zanella, I. (2015). Tiburones y rayas captura-
dos por pesquerías artesanales con línea de fondo en
el Golfo Dulce, Costa Rica. Revista Biología Tropi-
cal, 63(Supplement 1), 183-198.
McDavitt, M. T. (2002). Lake Nicaragua revisited: con-
versations with a former sawfish fisherman. Shark
News: Newsletter of the IUCN Shark Specialist
Group, 14, 5.
Niella, Y., Afonso, A. S., & Hazin, F. H. (2017). Bioeco-
logy and movements of bull sharks, Carcharhinus
leucas, caught in a long-term longline survey off
northeastern Brazil. Neotropical Ichthyology, 15(3),
e170106.
Pasos-Acuña, C. (2018) Efecto del buceo en el compor-
tamiento del tiburón toro (Carcharhinus leucas) y
evaluación económica de la especie en el Parque
Nacional Cabo Pulmo (Masters thesis). Centro de
Investigaciones Biológicas del Noroeste, S.C., La
Paz, Baja California, México.
Powers, S. P., Fodrie, F. J., Scyphers, S. B, Drymon, J.
M., Shipp, R. L., & Stunz, G.W. (2013). Gulf-wide
decreases in the size of large coastal sharks documen-
ted by generations of fishermen. Marine and Coastal
Fisheries: Dynamics, Management, and Ecosystem
Science, 5, 93-102.
Papastamatiou, Y., Friedlander, A., Caselle, J., & Lowe,
C. (2010). Long-term movement patterns and tro-
phic ecology of blacktip reef sharks (Carcharhinus
melanopterus) at Palmyra atoll. Journal of Expe-
rimental Marine Biology and Ecology, 386(1-2),
94-102.
R Development Core Team R. (2014). R: A Language and
Environment for Statistical Computing. Vienna, Aus-
tria: R Foundation for Statistical Computing. http://
www.R-project.org/
Rodríguez, A., Alfaro, E. J., & Cortés, J. (2021). Spatial
and temporal dynamics of the hydrology at Salinas
Bay, Costa Rica, Eastern Tropical Pacific. Revista de
Biología Tropical, 69(Suppl. 2), S105-S126.
Simpfendorfer, C. A, Greitas, G. G., Wiley, T. R., & Heu-
pel, M. R. (2005) Distribution and habitat partitioning
of immature bull sharks (Carcharhinus leucas) in a
southwest Florida estuary. Estuaries, 28, 78-85.
SINAC (Sistema Nacional de Áreas de Conservación).
(2013). Plan de Manejo Área de Conservación Gua-
nacaste 2014-2024. Guanacaste, Costa Rica: Área de
Conservación Guanacaste.
Thorson, T. B. (1971). Movement of bull sharks, Car-
charhinus leucas, between Caribbean Sea and Lake
Nicaragua demonstrated by tagging. Copeia, 1971,
336-338.
Thorson, T. B. (1972). The status of the bull shark, Car-
charhinus leucas, in the Amazon River. Copeia,
1972, 601-605.
Thorson, T. B. (1982). The impact of commercial exploi-
tation on sawfish and shark populations in Lake
Nicaragua. Fisheries, 7, 2-10.
Werry, J. M., & Clua, E. (2013). Sex-based spatial segre-
gation of adult bull sharks, Carcharhinus leucas, in
the New Caledonian great lagoon. Aquatic Living
Resources, 26, 281-288.
Zanella, I., López, A., & Cure, K. (2019). Golfo Dulce:
critical habitat and nursery area for juvenile scalloped
hammerhead sharks Sphyrna lewini in the Eastern
Tropical Pacific Seascape. Environmental Biology of
Fishes, 102, 1291-1300.