Spatial and temporal distribution of the
invasive lionfish Pterois volitans in coral
reefs of Tayrona National Natural Park,
Colombian Caribbean
Elisa Bayraktarov1,4 , Javier Alarcón-Moscoso2 , Andrea Polanco F.2 and
Christian Wild1,3
1 Coral Reef Ecology Group (CORE), Leibniz Center for Tropical Marine Ecology, Bremen,
Germany
2 Instituto de Investigaciones Marinas y Costeras ‘José Benito Vives de Andréis’ (Invemar),
Santa Marta, Colombia
3 Faculty of Biology and Chemistry (FB2), University of Bremen, Bremen, Germany
4
Current affiliation: Global Change Institute, The University of Queensland, Brisbane, Australia
ABSTRACT
Submitted 3 March 2014
Accepted 7 May 2014
Published 22 May 2014
Corresponding author
Elisa Bayraktarov,
elisa.bayraktarov@uni-bremen.de
Academic editor
Robert Toonen
The lionfish Pterois volitans is an invasive species throughout the Western Atlantic
that disturbs functioning of local ecosystems such as coral reefs via fast and intense
consumption of small fish and invertebrates. In 2009, lionfish populated the bays of
Tayrona National Natural Park (TNNP), a biodiversity hotspot in the Colombian
Caribbean that is strongly influenced by changing environmental conditions due to
a rainy and dry season. So far, the spatial and temporal distribution of P. volitans in
the bays of TNNP is unknown. Therefore, this study assessed the abundance and
body lengths of P. volitans during monthly surveys throughout the year 2012 in four
bays (thereof two bays where lionfish removals were undertaken) of TNNP at 10 m
water depth in coral reefs using transect tools. Findings revealed lionfish abundances
of 2.9 ± 0.9 individuals ha−1 with lengths of 20–25 cm for TNNP, hinting to an
established, mostly adult local population. Actual TNNP lionfish abundances are
thereby very similar to those at Indo–Pacific reef locations where the invasive lionfish
formerly originated from. Significant spatial differences for lionfish abundances
and body lengths between different bays in TNNP suggest habitat preferences of
P. volitans depending on age. Lionfish abundances were highly variable over time, but
without significant differences between seasons. Removals could not reduce lionfish
abundances significantly during the period of study. This study therefore recommends improved management actions in order to control the already established
invasive lionfish population in TNNP.
Additional Information and
Declarations can be found on
page 11
Subjects Aquaculture, Fisheries and Fish Science, Conservation Biology, Marine Biology
Keywords Invasive lionfish, Colombian Caribbean, Tayrona National Natural Park, Spatial and
DOI 10.7717/peerj.397
temporal distribution, Removals effects, Body lengths
Copyright
2014 Bayraktarov et al.
Distributed under
Creative Commons CC-BY 4.0
OPEN ACCESS
INTRODUCTION
The Indo–Pacific lionfish Pterois volitans belongs to the family Scorpaenidae and is an
invasive marine fish that was introduced in the Western Atlantic during the 1980’s
(Whitfield et al., 2002; Morris & Whitfield, 2009; Schofield, 2010; Albins & Hixon, 2011;
How to cite this article Bayraktarov et al. (2014), Spatial and temporal distribution of the invasive lionfish Pterois volitans in coral reefs
of Tayrona National Natural Park, Colombian Caribbean. PeerJ 2:e397; DOI 10.7717/peerj.397
Arias-González et al., 2011). Lionfish in invaded areas have many advantages over native
fauna e.g., their generalist diet on a variety of smaller fishes, shrimps and small mobile
invertebrates (Morris & Akins, 2009), defensive venomous spines (Morris & Whitfield,
2009; Albins & Hixon, 2011), rapid growth (Albins & Hixon, 2011), low parasite load
(Morris, 2009), and habitat generality (Barbour et al., 2010; Albins & Hixon, 2011). These
characteristics make lionfish dramatically decrease local populations in invaded areas
(Albins & Hixon, 2008; Arias-González et al., 2011) with strong implications for the
trophic web structures of the marine ecosystem (Mack et al., 2000). Additional features
of lionfish such as high fecundity (Morris, 2009; Morris & Whitfield, 2009), effective larval
dispersal mechanisms (Morris & Whitfield, 2009), and efficient predation (Albins & Hixon,
2008; Albins & Hixon, 2011; Côté & Maljković, 2010) increase their probability of invasion
success.
In Colombia, lionfish arrived to the oceanic islands of San Andrés and Providencia
in 2008 and invaded the entire continental coast of the country in the course of the
following year. For the Tayrona National Natural Park (TNNP; Fig. 1) on the northeast
Colombian coast, the presence of P. volitans was first recorded in May–July 2009 at water
depths between 12 and 20 m over coral patches (González et al., 2009). In 2010, juvenile
P. volitans (3–10 cm lengths) were observed in the mangrove ecosystem of Chengue
Bay (Arbeláez & Acero P, 2011). The ecological consequences of lionfish are of particular
interest for the TNNP area due to its major coastal biodiversity (Garzón-Ferreira & Cano,
1991). The TNNP is a fishing restricted area administrated by the National Natural Parks
of Colombia dealing with all territories of marine parks and reserves. Generally, the TNNP
includes different coastal bays with complex structural bottoms offering heterogeneity of
habitats suitable for a high marine biodiversity. A record diversity was reported especially
for macroalgae (Bula-Meyer & Norris, 2001; Diaz-Pulido & Garzón-Ferreira, 2002; Diaz
Pulido & Dı́az Ruiz, 2003) but also for other marine organisms (e.g., mollusks; Dı́az, 1995;
Diaz-Pulido, 1998).
So far, little is known about the spatial and temporal distribution of lionfish in TNNP.
Therefore, the aim of the present study was to assess monthly P. volitans abundances
and estimated body lengths throughout one year (2012) for four bays within TNNP. The
first objective was to compare lionfish data from TNNP with other invaded areas and
also with its native locations in the Indo–Pacific. The second objective was to determine
whether lionfish abundances change over time and if differences between a rainy and dry
season, coinciding with a seasonal upwelling, exist. This objective focused on possible
effects of strong seasonal variation in physicochemical parameters (temperature, salinity,
wind, water currents, surplus of inorganic nutrients; Bayraktarov et al., 2013; Bayraktarov,
Pizarro & Wild, 2014) during seasonal upwelling on lionfish distribution, as concluded
for the factor temperature by the experimental study of Kimball et al. (2004) indicating
ceased feeding of lionfish at 16 ◦ C with lethal consequences at 10 ◦ C. The third objective
addressed the efficiency of management actions (removals) that started in May 2012 in two
TNNP bays by comparing lionfish abundances before removals with data collected after
removals for two of the four bays. The present study provides recent and comprehensive
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Figure 1 Area of survey in the Tayrona National Natural Park (TNNP). The points indicate the
sampling locations at the western and eastern flank of each bay. Source: Laboratorio de Sistemas de
Información LabSIS, INVEMAR, 2013.
lionfish distribution data and establishes an actual baseline with high temporal and spatial
resolution for TNNP reefs in the Colombian Caribbean. Further needs of management
actions to control the already established invasive lionfish population in TNNP are
discussed.
MATERIALS AND METHODS
Study site
All necessary permits were obtained for the described study by Instituto de Investigaciones
Marinas y Costeras ‘José Benito Vives de Andréis’ (Invemar) in Santa Marta, Colombia
which complied with all relevant regulations (decree # 302 and # 309).
The Tayrona National Natural Park (TNNP) is located on the northeastern coast of
Colombia, between 11◦ 17′ –11◦ 22′ N and 73◦ 53′ –74◦ 12′ W (Fig. 1). The region contains
a rocky coastline with capes, inlets and bays with sandy beaches covering over 40 km
(Garzón-Ferreira & Cano, 1991; Dı́az et al., 2000; Martı́nez & Acosta, 2005). The area of
survey included the main TNNP bays Chengue, Gayraca, Neguanje, and Cinto (Fig. 1)
which experience strong seasonal changes due to a rainy season (>80% of the annual
rainfall, May–November) and a dry season (December–April) characterized by a seasonal
upwelling with strong changes in temperature (decrease from 28 to 21 ◦ C), salinity
(increase from 33 to 38), increased wind and water currents (Salzwedel & Müller, 1983;
Mesa, Poveda & Carvajal, 1997; Bayraktarov et al., 2013; Bayraktarov, Pizarro & Wild,
2014). Increased concentration of inorganic nutrients and chlorophyll a during periods of
upwelling (dry season) result in mesotrophic conditions, compared with oligotrophic
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settings during the non-upwelling periods (rainy season; Franco-Herrera et al., 2007;
Arévalo-Martı́nez & Franco-Herrera, 2008; Bayraktarov, Pizarro & Wild, 2014).
Coral reef formations can be found growing on both sides of each bay between water
depths of 5 to 20 m (Werding & Erhardt, 1976; Werding & Sánchez, 1989; Garzón-Ferreira
& Cano, 1991) and represent a habitat for over 180 reef fish species (Olaya-Restrepo,
Reyes-Nivia & Rodrı́guez-Ramı́rez, 2008). Additionally, the bays harbor mangrove
ecosystems and seagrass beds (Fig. 1; Garzón-Ferreira & Cano, 1991).
Lionfish assessment in space and time
In order to address the goals of the study, P. volitans abundances were monitored monthly
in four bays of TNNP. Surveys comprised monitoring along line transects of 50 m length
and 5 m width in triplicates that were located at the western and eastern flank of each bay
(Fig. 1) in order to encompass a representative area for lionfish distribution. Transects
were located at water depths between 9 and 11 m, parallel to the coastline, and were
separated by >5 m to ensure independence between samples. The investigated area covered
1500 m2 per bay and a total of 6000 m2 within the TNNP. The method of visual census
was applied by SCUBA (English, Wilkinson & Baker, 1997; Lang et al., 2010). The total
number of P. volitans observed during a time of 25 min per replicate was counted (Morris,
2009). Places where lionfish may hide such as holes and cavities between rocks and coral
framework were carefully examined. Estimated total body lengths (TL) of lionfish were
recorded in situ in 5 cm intervals for each localized individual from the tip of the snout
to the tip of the caudal fin. The surveys were performed between the second and the third
week of each month, between 8:00 am and 3:00 pm.
We were informed that lionfish removals were planned to start in May 2012 as a joint
project between Universidad Nacional de Colombia, Universidad Jorge Tadeo Lozano,
Universidad del Magdalena, Instituto de Investigaciones Marinas y Costeras ‘José Benito
Vives de Andréis’ (Invemar) and the National Natural Parks of Colombia. Removals were
performed monthly by spearing and netting at variable depths (5–25 m) by SCUBA diving,
and to our knowledge, exclusively in the TNNP bays Chengue and Cinto. Additional
unregistered removals of lionfish by dive centers or fishermen could not be considered in
the present survey.
Data analysis
Mean monthly abundances of P. volitans in the TNNP bays Chengue, Gayraca, Neguanje
and Cinto (Fig. 2A) were calculated from data collected over 12 months with a replication
of 6 transects per bay and month and were converted into individuals per hectare (ind
ha−1 ; Fig. 2A). Monthly abundance before onset of removals in May were estimated
by calculating the abundance for the time period January to April, whereas lionfish
data collected between May and December were used to determine the monthly mean
abundance after removals (Fig. 2B). For calculation of the temporal lionfish distribution,
all lionfish transect data were aggregated per month resulting in a replication of n = 24
transects (Fig. 3A). Annual mean abundance was determined for each bay and the whole
TNNP area by pooling the data collected over 12 months resulting in a transect replication
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Figure 2 Lionfish abundances in Tayrona National Natural Park before and after removal. (A) Abundances (monthly mean ± SE) of Pterois volitans in the bays Chengue, Gayraca, Neguanje and Cinto
throughout the months of 2012. The red line indicates the starting period of monthly removals (May
2012) from the bays Chengue and Cinto. Removal bays (Chengue and Cinto) are indicated by solid
symbols, while non-removal bays have open symbols. (B) Mean lionfish abundances (+SE) before
(January–April) and after removal (May–December). Abbreviations: Chengue, (Ch); Gayraca, (Ga);
Neguanje, (Ne); and Cinto, (Ci).
Figure 3 Monthly abundances of Pterois volitans. (A) Monthly mean + SE; aggregate of four bays for
Tayrona National Natural Park and (B) estimated body lengths for the bays Chengue, Gayraca, Neguanje,
and Cinto. Missing error bars represent sample sizes which did not allow the calculation of a mean and
SE at some locations and months.
of n = 69 transects for Chengue and Neguanje, and n = 72 for Gayraca and Cinto (total
of 282 transects). Mean estimated sizes of lionfish (Fig. 3B) were calculated from total
estimated body lengths of fishes observed along the transects in the respective bay.
Differences in P. volitans abundances between bays and months were tested by a
Generalized Linear Model (GLM) for Poisson-distributed data and the software R
(R Development Core Team, 2008). Multiple comparisons between bays (Chengue,
Gayraca, Neguanje and Cinto) and months were performed by a Tukey’s Honestly
Significant Difference (HSD) post hoc test on data before (January–April; 93 transects)
and after onset of removal (May–December; 189 transects). For a quantification of possible
removal effects, GLMs for Poisson-distributed data and Tukey’s HSD post hoc tests were
performed before and after removal in the bays Chengue and Cinto, individually.
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RESULTS
Spatial distribution of lionfish in TNNP
Throughout the year 2012, 123 individuals of Pterois volitans were counted during 12
months in four bays over a total monitored area of 6000 m2 . Before removals, lowest
mean lionfish abundance was found in Chengue Bay with 1.7 ± 1.0 ind ha−1 (monthly
mean ± SE for the months January–April), followed by Cinto with 2.5 ± 0.3, and Neguanje
with 3.9 ± 1.0 ind ha−1 . Highest numbers of monthly lionfish were present in Gayraca
with 5.8 ± 3.6 ind ha−1 . Significant differences in lionfish abundances during the months
before removal were present between the bays Chengue and Gayraca (GLM, Tukey’s HSD
post hoc, p = 0.033) with higher lionfish abundance in Gayraca. After onset of monthly
removal in May, lowest monthly lionfish abundance was observed in Neguanje with
0.8 ± 0.5 ind ha−1 , followed by Chengue with 1.3 ± 0.6 and Cinto with 3.9 ± 2.0 ind ha−1 .
Highest monthly lionfish abundance was still observed in Gayraca Bay with 4.4 ± 1.7
ind ha−1 . After removal, significant differences were found between Chengue and Cinto
(p = 0.017), Chengue and Gayraca (p = 0.004), Gayraca and Neguanje (p < 0.001) and
Neguanje and Cinto (p = 0.003).
Our monthly lionfish censuses demonstrated temporal and spatial variability in lionfish
abundances among TNNP bays, which varied between 0 and 16.7 ind ha−1 (Fig. 2A).
In Chengue (a removal bay), lionfish abundances were below 5 ind ha−1 (monthly
mean ± SE) until July and disappeared thereafter completely until December, where
1.1 ± 1.1 ind ha−1 were registered. Highest abundances were observed in Gayraca during
January with 16.7 ± 10.3 ind ha−1 and August with 12.2 ± 4.6 ind ha−1 , while intermediate abundances were present during September with 10.0 ± 5.6 ind ha−1 and December
with 7.8 ± 6.5 ind ha−1 within this bay. In Neguanje, highest lionfish abundances were
recorded in January with 5.6 ± 5.6 ind ha−1 and February with 5.6 ± 3.6 ind ha−1 .
Here, no lionfish were observed between July and December, except for September when
2.2 ± 2.2 ind ha−1 were registered. In Cinto, lionfish abundances peaked during September
with 16.7 ± 5.6 ind ha−1 and June with 6.7 ± 2.4 ind ha−1 , but were otherwise below
5 ind ha−1 . Mean lionfish abundance before removal was 10.0 ± 5.8 ind ha−1 for
Chengue, 35.0 ± 21.8 ind ha−1 for Gayraca, 21.7 ± 6.9 ind ha−1 for Neguanje, and
15.0 ± 1.7 ind ha−1 for Cinto (Fig. 2B). Lionfish abundance for the months during which
removal actions were performed changed the values to 5.0 ± 3.3, 28.3 ± 9.8, 5.0 ± 2.7, and
23.3 ± 12.1 ind ha−1 , respectively (Fig. 2B).
Temporal distribution of lionfish in TNNP
On the temporal scale, highest abundance of lionfish was observed in September with
7.2 ± 2.4 ind ha−1 (monthly TNNP mean ± SE; Fig. 3A) and January with 6.4 ± 3.0
ind ha−1 ; lowest during November with 0.3 ± 0.3 ind ha−1 and July with 0.8 ± 0.6
ind ha−1 . Significant differences between months were present between September and
April (GLM, Tukey’s HSD post hoc, p = 0.05), July and January (p = 0.04), September
and July (p = 0.02), September and May (p = 0.03), and between September and October
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Table 1 Comparison of Pterois volitans abundance in Tayrona National Natural Park (TNNP) with worldwide reports on invaded and native
habitats.
Region and year
Habitat for lionfish
Reported abundance
(ind ha−1 )
Source
Chengue Bay (TNNP, Colombian Caribbean), 2012
Gayraca Bay (TNNP, Colombian Caribbean), 2012
Neguanje Bay (TNNP, Colombian Caribbean), 2012
Cinto Bay (TNNP, Colombian Caribbean), 2012
TNNP, Colombian Caribbean, 2012
New Providence, Bahamas, Western Atlantic, 2008
Coast off North Carolina, USA, Western Atlantic, 2004
Coast off North Carolina, USA, Western Atlantic, 2008
Palau Archipelago, Western Pacific, 2008
Gulf of Aqaba, Red Sea, 1997
invasive
invasive
invasive
invasive
invasive
invasive
invasive
invasive
native
native
1.4 ± 0.6
4.9 ± 1.3
1.8 ± 0.6
3.4 ± 0.8
2.9 ± 0.9
393.3 ± 144.4
21.2 ± 5.1
150
2.2
∼80
this study
this study
this study
this study
this study
Green & Côté (2009)
Whitfield et al. (2007)
Morris & Whitfield (2009)
Grubich, Westneat & McCord (2009)
Fishelson (1997)
(p = 0.03). However, lionfish abundances were not significantly different between rainy
(May–November) and dry season (December–April).
Largest estimated lionfish body lengths of 40 cm were registered for Cinto in January
and August, and Neguanje in September (Fig. 3B). Largest body lengths were present in
Gayraca and Cinto with mean sizes of 20–25 cm, followed by Neguanje with 15–20 cm,
and smallest in Chengue with 10–15 cm. A total of 75% of all lionfish observed had a
body length larger than 17.5 cm TL (20–25 cm) representing the size of 50% maturity for
females (Morris, 2009). Before removal, mature lionfish accounted for 80%, and 72% after
initiation of removal efforts. Adults were distributed as 13% in Chengue, 51% in Gayraca,
21% in Neguanje, and 15% in Cinto before removal which changed to 4%, 49%, 8%, and
40% after removal, respectively.
The effect of fish removal
Individual GLM analyses showed no significant differences in lionfish abundance before
(January–April) and after removal (May–December) for both removal bays, Chengue
(GLM, Tukey’s HSD post hoc, p = 0.53) and Cinto (p = 0.25). Since no significant
differences were observed before and after removal, transect data were pooled to calculate
an annual mean of 2.9 ± 0.9 ind ha−1 (annual mean ± SE) for the TNNP region. The
annual mean for Chengue was 1.4 ± 1.3 ind ha−1 , 4.9 ± 1.3 ind ha−1 for Gayraca,
1.8 ± 0.6 ind ha−1 for Neguanje, and 3.4 ± 0.8 ind ha−1 for Cinto, respectively (Table 1).
DISCUSSION
Spatial and temporal distribution of P. volitans
Our data on P. volitans distribution in Tayrona National Natural Park (TNNP; Colombian
Caribbean) show that a local population with mean body length of 20–25 cm has
developed in the bays Chengue, Gayraca, Neguanje and Cinto. These lionfish total body
lengths (TL) hint to a population mostly dominated by adult fishes that are able to sexually
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reproduce, based on Morris (2009) who reported 17.5 cm TL as the size of 50% maturity
for females.
With an annual mean of 2.9 ind ha−1 , lionfish abundance in TNNP was similar to
some locations in the Indo–Pacific where it originated from, e.g., Palau Archipelago with
2.2 ind ha−1 (Grubich, Westneat & McCord, 2009), but below ∼80 ind ha−1 reported
for the Gulf of Aqaba/Red Sea (Fishelson, 1997). Table 1 shows a comparison of lionfish
abundance in TNNP to other invaded and native habitats worldwide, however data
should be considered as estimates as methods of monitoring were not always comparable
(e.g., rotenone-sampling over small areas; Fishelson, 1997). Lionfish abundances in TNNP
were below the values reported for other invaded areas of the Western Atlantic such
as the Bahamas with 393 (Green & Côté, 2009) or the coast of North Carolina/USA
with 150 ind ha−1 (Morris & Whitfield, 2009) which may be due to the relatively recent
invasion of TNNP in 2009 (González et al., 2009) vs. an invasion of the Bahamas in 2004
(Schofield, 2009). High abundances of lionfish in invaded areas are likely the result of
unrestricted growth and reproduction due to the availability of food sources and lack of
natural predators. Some predators obviously learned to target lionfish as potential prey
(Bernadsky & Goulet, 1991; Maljković, Leeuwen & Cove, 2008). So far, two Caribbean
large-bodied grouper species, Epinephelus striatus and Mycteroperca tigris, were captured
with lionfish in their stomach contents (Maljković, Leeuwen & Cove, 2008). However,
E. striatus is one of the species categorized as endangered in the Colombian Caribbean
red list of marine fishes (Mejı́a & Acero, 2002). Mumby, Harborne & Brumbaugh (2011)
presented data on the reduction of lionfish biomass by groupers which may thus serve
as natural biocontrol of growing lionfish populations. However, the lack of these natural
lionfish predators in TNNP (Olaya-Restrepo, Reyes-Nivia & Rodrı́guez-Ramı́rez, 2008)
and the wider Caribbean Sadovy (2005) is alarming. In contrast to Mumby, Harborne &
Brumbaugh (2011), the study of Hackerott et al. (2013) concluded that the abundance of
lionfish was not influenced by interaction with native predators in 71 reefs and different
biogeographic regions in the Caribbean. The hypothesis of groupers as natural biocontrol
against invasive lionfish is currently a subject of active debate (Bruno et al., 2013; Green et
al., in press; Mumby et al., 2013). These conflicting results once more stress the necessity
of immediate and improved management actions to control further lionfish reproduction
and invasion.
Our monthly P. volitans distribution data over four bays in TNNP showed no seasonal
pattern between a rainy and a dry season, characterized by seasonal upwelling. The
consequently altered environmental conditions (temperature, salinity, water currents,
and surplus of inorganic nutrients; Salzwedel & Müller, 1983; Bayraktarov et al., 2013;
Bayraktarov, Pizarro & Wild, 2014) did not appear to affect the abundance of lionfish in
TNNP. An effect of seawater temperature decrease from 28 to 21 ◦ C (Bayraktarov, Pizarro
& Wild, 2014) on lionfish distribution within the area could not be detected. This finding
is supported by the laboratory study by Kimball et al. (2004) showing that the critical
temperature at which lionfish ceases feeding was 16 ◦ C with lethal consequences at 10 ◦ C,
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which is more than 10 ◦ C lower that the coldest temperature so far reported for the TNNP
upwelling region (20 ◦ C, Bayraktarov, Pizarro & Wild, 2014).
Effect of lionfish removal
Abundances and body lengths of P. volitans for Chengue Bay, in which removals were
performed, were smaller than for the uncontrolled Gayraca and Neguanje. However,
removals could not effectively reduce lionfish abundances in Cinto which were lower
than abundances in Gayraca but higher than in Neguanje. Body lengths found in Cinto
corresponded to those in Gayraca. The smallest body lengths observed in Chengue indicate
that a mostly juvenile population may have developed in this bay and thereby may indicate
a habitat preference dependent on age. However, it cannot be excluded that the smaller
body lengths of lionfish in Chengue are a consequence of removal during management
actions targeting predominantly larger adult individuals which are easier to observe and
catch. Smaller juveniles may hide between the roots of mangroves (Arbeláez & Acero P,
2011) or in crevices and holes of the reef framework which are especially extensive for
Chengue Bay (Bayraktarov E, pers. obs., 2010). Additionally, Chengue Bay comprises a
highly developed mangrove ecosystem (Garzón-Ferreira & Cano, 1991) which may serve as
nursery for lionfish larvae and juveniles. This is further supported by the study of Arbeláez
& Acero P (2011), who found lionfish juveniles of 3–10 cm lengths at the submerged roots
of the mangroves bordering the entrance to the southern lagoon in Chengue Bay.
Factors affecting fish populations that cannot be excluded are the differences in coral
reef complexity between the bays and the potential food sources for lionfish. These
important points need to be addressed in further studies.
Our study suggests that management actions for the TNNP require further improvement in terms of removal frequencies and a larger removal area in order to significantly
reduce the established lionfish population. Targeted removals were shown to represent a
viable strategy in reducing the direct impacts of invasive lionfish on marine ecosystems
(Frazer et al., 2012). Frazer et al. (2012) further suggest that management actions should
involve long-term monitoring of lionfish distribution, data on recruitment, growth, and
reproduction as well as studies on the direct and indirect effects by invasive lionfish on
other fish assemblages. The implementation and improvement of management actions
in order to preserve the condition of TNNP coral reef ecosystems during P. volitans
invasion are crucially essential. The national plan to control and manage lionfish invasion
in Colombia is focused on three focal strategy points: (1) realization of fundamental
research, (2) implementation of management actions and (3) focus on education and
control (MADS et al., 2013). Whereas the first two points are addressed by research groups
of universities and institutes, the third point is coordinated by the National Natural Parks
of Colombia dealing with all territories of marine parks and reserves. The removal of
lionfish outside the marine parks territories lies in the hands of regional environmental
officers confronted by an environmental and societal challenge.
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Recommendations
Considering the national plan to control and manage lionfish invasion, potential
management actions required for the Colombian Caribbean region may further focus
on raising the community’s awareness by introducing the lionfish problem and the
consequences of its invasion. Removals on a wider scale can be promoted by consumption
of lionfish on a local and commercial scale. Public outreach should focus especially on
lionfish as a good candidate for human nutrition. Morris et al. (2011) reported a relatively
high content of lionfish fillet yield (30.5%) comparable to groupers, graysbys, and coneys.
Lionfish meat had also higher content of essential n-3 fatty acids and a relatively low
amount of saturated fatty acids as compared to other marine reef fish species (e.g., red
snapper, dolphinfish, blue fin tuna, triggerfish, grouper and tilapia; Morris et al., 2011). The
authors suggested that public outreach should especially focus on education about lionfish
invasion, handling and cleaning of P. volitans in order to minimize risks for envenomation
(Morris et al., 2011).
The establishment of marine reserves can effectively protect larger fishes (Halpern, 2003)
such as groupers that could prey on lionfish as reported for the fishing-restricted Exuma
Cays Land and Sea Park/Bahamas by Mumby, Harborne & Brumbaugh (2011). As long
as it is not clear whether native predators are able to effectively prey on lionfish, further
controlled fishing restrictions especially on native apex predator populations will become
imperative for lionfish invasion control.
The invasion of P. volitans in the Western Atlantic and the Caribbean is considered as
one of the top global threats to conservation of biodiversity (Sutherland et al., 2010). Local
lionfish populations may disturb functioning of coral reefs through high consumption of
small herbivorous fishes, including parrotfishes (Albins & Hixon, 2008; Morris & Akins,
2009), thus indirectly promote the outcompeting of corals by naturally uncontrolled
growth of seaweeds (Mumby et al., 2006; Mumby & Steneck, 2008; Lesser & Slattery, 2011).
Under the combined effects of overfishing, lionfish invasion (Albins & Hixon, 2011),
global climate change (Hoegh-Guldberg, Ortiz & Dove, 2011), and local environmental
degradations, the future of coral ecosystems is severely endangered (Jackson, 2010) in the
Western Atlantic and Caribbean.
ACKNOWLEDGEMENTS
We acknowledge Juan F. Lazarus-Agudélo, Corvin Eidens, Christian M. Dı́az-Sanchez,
Johanna C. Vega-Sequeda, and particularly Julian Rau for SCUBA diving and assistance
during the field trips. We thank the staff of Instituto de Investigaciones Marinas y
Costeras ‘José Benito Vives de Andréis’ (Invemar) in Santa Marta, Colombia, especially
Diana I. Gómez-López and Carolina Jaramillo-Carvajal for organizational support.
We acknowledge the administration of the Tayrona National Natural Park for the kind
collaboration.
Bayraktarov et al. (2014), PeerJ, DOI 10.7717/peerj.397
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ADDITIONAL INFORMATION AND DECLARATIONS
Funding
This study was supported by the German Academic Research Service (DAAD) through
the German–Colombian Center of Excellence in Marine Sciences (CEMarin) under the
coordination of Thomas Wilke. The funders had no role in study design, data collection
and analysis, decision to publish, or preparation of the manuscript.
Grant Disclosures
The following grant information was disclosed by the authors:
German Academic Research Service (DAAD) through the German–Colombian Center of
Excellence in Marine Sciences (CEMarin).
Competing Interests
Elisa Bayraktarov and Christian Wild are employees of the Leibniz Center for Tropical
Marine Ecology; Javier Alarcón-Moscoso, Andrea Polanco F. are employees of the Instituto
de Investigaciones Marinas y Costeras ‘José Benito Vives de Andréis’ (Invemar).
Author Contributions
• Elisa Bayraktarov conceived and designed the experiments, performed the experiments,
analyzed the data, contributed reagents/materials/analysis tools, wrote the paper,
prepared figures and/or tables, reviewed drafts of the paper.
• Javier Alarcón-Moscoso performed the experiments, contributed
reagents/materials/analysis tools, wrote the paper, reviewed drafts of the paper.
• Andrea Polanco F. performed the experiments, wrote the paper, reviewed drafts of the
paper.
• Christian Wild conceived and designed the experiments, wrote the paper, reviewed
drafts of the paper.
Field Study Permissions
The following information was supplied relating to field study approvals (i.e., approving
body and any reference numbers):
All necessary permits were obtained for the described study by Instituto de Investigaciones Marinas y Costeras ‘José Benito Vives de Andréis’ (Invemar) in Santa Marta,
Colombia which complied with all relevant regulations (decree #302 and #309).
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