Regional Studies in Marine Science 31 (2019) 100793

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Regional Studies in Marine Science

journal homepage: www.elsevier.com/locate/rsma

Life history, genetics, range expansion and new frontiers of the lionfish
(Pterois volitans, Perciformes: Pteroidae) in Latin America
∗
Edgardo E. Díaz-Ferguson a , , Margaret E. Hunter b
a
Coiba Scientific Station (COIBA AIP), City of Knowledge, Clayton, Panama, Republic of Panama
b
U.S. Geological Survey, Wetland and Aquatic Research Center, 7920 NW 71st Street, Gainesville, FL 32653, USA

article info a b s t r a c t

Article history: Pterois volitans (lionfish) is a midsize predatory fish commonly found in waters of the western Pacific
Received 17 April 2019 and Indian Ocean. The species was first documented in Dania Beach, Florida (northwestern Caribbean)
Received in revised form 6 August 2019 in 1985. Since that time the species has expanded its range rapidly to the Northwestern Atlantic Ocean,
Accepted 7 August 2019
Gulf of Mexico, and Caribbean Sea. Since its introduction P. volitans has changed community structure
Available online 11 August 2019
and biodiversity of Caribbean reef communities and other coastal tropical ecosystems. Continuous
Keywords: introductions (accidental or intentional), limited natural predators, naïve-range prey behavior, high
Aquatic invasive species predation rates on competitors, continuous reproduction, and an extended period of larval dispersal
Caribbean sea have been the keys for successful invasion and rapid range extension of P. volitans. This invasion has
Atlantic ocean become so severe that it has been recognized as one of the world’s top conservation issues. Here,
Connectivity we review the life history, behavior, and historical and contemporary genetic patterns that facilitate
Management expansion and the colonization process. A greater understanding of lionfish biology, ecology, and
the changes related to its present condition as a super-invader could improve current and future
management strategies and new detection and response methodologies. We also examine new invasion
frontiers that this species has the potential to colonize such as the eastern Pacific. This information will
provide managers, the scientific community, and the civil society better tools for eradication, control
and management of future invasions of this and other invasive species.
© 2019 Published by Elsevier B.V.

Contents

1. Introduction........................................................................................................................................................................................................................... 1
2. Taxonomy, ecology, life history and invasion success of Pterois volitans...................................................................................................................... 3
3. Phylogeography, genetic structure and demographic history of Pterois volitans ......................................................................................................... 4
4. Molecular detection methods ............................................................................................................................................................................................. 4
5. Management strategies for control and future invasions ............................................................................................................................................... 4
6. New frontiers for expansion ............................................................................................................................................................................................... 5
6.1. Northern and southern population expansion of the Atlantic ......................................................................................................................... 5
6.2. Colonization of the eastern tropical Pacific via the Panama Canal ................................................................................................................... 5
Acknowledgments ................................................................................................................................................................................................................ 6
References ............................................................................................................................................................................................................................. 6

1. Introduction considered one of the main threats to biodiversity and commu-

nity structure in the marine environment (Pimentel et al., 2005).
Invasive species introductions are growing in frequency and Although less frequent and successful than freshwater invasions,
magnitude around the globe and the challenges surrounding marine invasions have rapidly increased in the Caribbean Sea dur-
their management are considered a primary conservation issue ing the last century, due to a number of factors including ocean
(Carballo-Cardenas, 2015). The introduction of invasive species is warming (Stachowicz et al., 2002; Canning-Clode et al., 2011). In
1985, the Pacific Red Lionfish (Pterois volitans) [Linnaeus, 1758]
∗ Corresponding author. was first collected in Dania Beach, Florida (Schofield, 2009). Sub-
E-mail addresses: ediaz@coiba.org.pa (E.E. Díaz-Ferguson), sequently, the species arrived in North Carolina, Bermuda, and the
mhunter@usgs.gov (M.E. Hunter). Bahamas. From the Bahamian archipelago, the species expanded

https://doi.org/10.1016/j.rsma.2019.100793
2352-4855/© 2019 Published by Elsevier B.V.
2 E.E. Díaz-Ferguson and M.E. Hunter / Regional Studies in Marine Science 31 (2019) 100793

Fig. 1. Sightings distribution map of Pterois volitans from 1985–2018.

Source: Data source: U.S. Geological Survey, Nonindigenous Aquatic
Species Database, NAS.er.usgs.gov. The sighting from Brazil is not
shown.

its range to the Caribbean Sea (Whitfield et al., 2002, 2007;
Morris and Akins, 2009; Schofield, 2009). In the last decade as a
consequence of the ocean’s surface warming, lionfishes extended
their geographical range in the Caribbean region, (Canning-Clode
et al., 2011). In 2007, the species was first reported in Cuba
(Chevalier et al., 2008) and in 2008 in Dominican Republic (Guer-
rero and Franco, 2008). In southern Caribbean waters available
data suggest the arrival of the species to Panama, Colombia
and Venezuela between 2009 and 2010 (Gonzalez et al., 2009;
Schofield, 2009; Agudo and Klein-Salas, 2014). Currently, P. voli-
tans identified southern limit is reported at the border between
Brazil and Uruguay in South America (Ferreira et al., 2015), and
to the north the species has a presence along the East coast of
the United States from Florida to Rhode Island (Whitfield et al.,
2002; Schofield, 2009; Fig. 1).
Invasive predators have some of the most dramatic impacts
on community structure and native fish biodiversity, reducing
recruitment, density, biomass, and genetic diversity of local pop-
ulations that eventually could experience extinction (Helfman,
2007; Albins and Hixon, 2008; Ballew et al., 2016; Chappell and
Smith, 2016; Palmer et al., 2016). The effectiveness of the P.
volitans Western Hemisphere colonization has resulted in it being
considered one of the greatest marine invasions in history and
of global conservation concern (Sutherland et al., 2011; MacIsaac
et al., 2016). The extreme nature of the P. volitans invasion has
provided a unique opportunity to investigate the ecological forces
controlling or favoring the invasion–expansion process and its
further colonization along with the resilience and stability of
the native community related to community structure, diversity,
and heterogeneity. To implement common measures of control,
surveillance and management, this invasion has required scien-
tists and managers from Caribbean countries and governments
to integrate different cultural, social, technological, and financial
support mechanisms. Along with historical sightings (Schofield,
2009, 2010) and modeling (Johnston and Purkis, 2011), one of the
main research tools implemented range-wide have been genetic
studies to inform diversity, relatedness, and invasion histories
(Betancur-R et al., 2011; Butterfield et al., 2015; Johnson et al.,
2016).
Primarily, P. volitans is considered a midsize predator of coral
reef communities consuming crustaceans and small fishes of the
Pomacentridae and Trichonotidae families (Cure et al., 2012).
Pterois volitans is also a prey for a few predators such as: groupers,
cornetfishes, sharks, spotted moray eel and eagle rays (Bernadsky
and Goulet, 1991; Majkovic et al., 2008; Mumby et al., 2011;
Pimiento et al., 2013; Cure et al., 2014). In its native range,
the species is not an apex predator, counter to its new role of
controlling reef communities in the Caribbean (Lönnstedt and
McCormick, 2013). Therefore, three questions are raised in this
review: (1) what strategies has this midsize predator used to be
the first species to colonize the broad and diverse ecosystem of
the Caribbean Basin? (2) How can range-wide genetic information
help to predict and manage marine invasions? and (3) What
methods are best suited to help prevent future invasions? To ad-
dress these questions, we summarize P. volitans life history traits
and discuss those that may have led to the successful invasion
 E.E. Díaz-Ferguson and M.E. Hunter / Regional Studies in Marine Science 31 (2019) 100793
of this species. We provide a review of the hybridization pro-
cess, phylogeography, genetic diversity and genetic connectivity
patterns that influence colonization and current distribution pat-
terns. Finally, we discuss current and future detection methods
and new threats and concerns that will be important to consider
in order to predict and reduce future invasions by other species.
2. Taxonomy, ecology, life history and invasion success of
Pterois volitans
Lionfishes are part of the Scorpaeniformes order, character-
ized by bottom dwelling fishes commonly found in tropical and
temperate waters where they are active predators of inverte-
brates and fishes (Hamner et al., 2007; Freshwater et al., 2009;
Morris, 2009; Betancur-R et al., 2011). The subfamily Pteroinae
comprise 27 species in 5 genera: Pterois (12 species), Dendrochirus
(6 species), Ebosia (4 species), Brachypterois (3 species), and Para-
pterois (2 species) (Matsunuma et al., 2013; Wilcox et al., 2018).
Hybridization was recently reported between two members of
the genera (P. miles and P. volitans) within their invasive range
(Morris and Whitfield, 2009). Pterois volitans is the most common
of the two species in the Caribbean (>90%) (Freshwater et al.,
2009). Recently, Wilcox et al. (2018) proposed a reevaluation of
both lionfish taxonomy and the nature of the Atlantic invasion.
The authors provided genetic evidence that P. volitans originated
from a hybridization between P. lunulate and P. russelli since these
three species were indistinguishable from one another.
Most of Pterois species are iteroparous and broadcast spawners
producing up to 10,000 eggs per female in each spawning period
(Morris, 2009). In particular, the average P. volitans female can
spawn up to 2 million eggs each year (Morris and Whitfield,
2009; Côté et al., 2013), and during each spawning event, fe-
males produce buoyant masses of eggs that are dispersed by
wind and currents for 25–35 days prior to settlement and re-
cruitment (Morris, 2012). Lionfish populations are composed of
five size classes based on AGRRA protocols (surveys and materi-
als) (Ginsburg et al., 1998; Agudo and Klein-Salas, 2014). Small
sizes are difficult to observe and therefore population studies
reported reduced densities of small size classes in recently colo-
nized areas (Agudo and Klein-Salas, 2014). Also, the recruitment
process is controlled by multiple factors in marine organisms,
such as: substrate (composition and distribution), physical pa-
rameters (temperature, salinity, tides and currents), seasonality,
and temperature being the most relevant (Whitfield, 1980).
Among physical factors, temperature seems to be the primary
limiting factor for successful recruitment (temperatures below
10 ◦ C), which has resulted in a very large, invaded geographic
region that includes temperate, subtropical and tropical waters
(Kimball et al., 2004). Temperature also is an important func-
tional parameter showing a positive relationship with feeding and
growth rates (South et al., 2017). Due to its generalist nature,
settlement and recruitment success of P. volitans larvae is high
and apparently not limited by substrate or depth (Perez-Portela
et al., 2018). Pterois volitans habitat preference has not been
identified and the species can be found in sea grasses, mangroves,
hard bottom substrates, and corals (Barbour et al., 2010; Jud et al.,
2011). The species has also been found in very shallow water
and at depths of more than 300 ft (Perez-Portela et al., 2018).
Thus, spatial patterns of distribution could be related to structural
complexity of the ecosystem, ocean connectivity, availability of
refuges and abundance of prey as limiting or shaping factors of
adult populations. Once established, P. volitans’ populations show
rapid growth. Distinct cohorts have been observed at the same
time suggesting continuous recruitment in a relative short time
period.
Other life history factors of P. volitans are also are likely to
contribute to the invasion success including high reproductive
3
output, rapid growth, generalist diet, prey naiveté behavior, and
hybrid origin (Côté et al., 2013; Wilcox et al., 2018). Prey naïveté
has been widely indicated as a possible key factor for P. voli-
tans success (Cure et al., 2012; Albins, 2013; Côté et al., 2013;
Albins and Hixon, 2013; Black et al., 2014; Kindinger, 2014; Eddy
et al., 2016; Ingeman, 2016). Evolutionary prey naiveté occurs
when there is an absence of exposure to a novel predator over
evolutionary time. This can result in nonexistent or ineffective
antipredator behavior in their presence (Côté et al., 2013). How-
ever, there still seems to be a lack of conclusive data on prey
naiveté concerning lionfish in the wild (Black 2014; Kindinger,
2014). Behavioral studies addressing the interactions between
P. volitans and Stegastes planifrons (Tree Spot Damselfish) and
Stegastes leucostictus (Beaugregory) have suggested some form
of naiveté to lionfish (Kindinger, 2014; Black, 2014; Cure et al.,
2012). However, additional observational studies are necessary to
better understand the phenomenon of prey naiveté to P. volitans
to corroborate findings by previous researchers (Sih et al., 2010).
Pterois volitans are considered generalist predators and have
been documented preying upon more than 50 species of fish,
crustaceans and shrimp within the invasive range (Albins and
Hixon, 2013; South et al., 2017). Lionfish are sedentary ambush
predators who use their large pectoral fins to corner their prey
(Morris, 2012). In their invaded range, P. volitans have been
shown to consume twenty-one families of teleosts, four families
of crustaceans, and one family of mollusk, with the majority (78%
by volume) being teleosts (Morris and Akins, 2009; Barbour et al.,
2010; Ballew et al., 2016; Pimiento et al., 2013, 2015). While
typically nocturnal predators in their native range, in the invasive
range lionfish are active during the day and have been found
with full stomachs (Pimiento et al., 2013). In a reef matrix in
the Bahamas, compared to predator-free controls, it has exper-
imentally been shown that a single lionfish reduced the average
abundance of fish per reef by 93.7%, a negative effect 2.6 times
stronger than that of a native grouper (Albins, 2013). Predation
on juvenile fish in nursery environments (estuaries, bays and
mangrove areas) increases the pressure on their populations by
reducing reproductive success in the native species (Albins and
Hixon, 2008; Palmer et al., 2016; Ballew et al., 2016). Ecological
impacts of lionfish on native species occur through multiple
pathways within the ecosystem affecting juveniles of other fish
species during the early stage of development in estuary areas
acting as nurseries (Albins and Hixon, 2008).
Lionfishes use coloration and large pectoral fins, along with
venomous spines, to discourage potential predators from feeding
on them (Pimiento et al., 2013). Predation of P. volitans has been
documented by groupers and eels (Bernadsky and Goulet, 1991;
Diller et al., 2014; Majkovic et al., 2008; Jud et al., 2011; Pimiento
et al., 2013). However, this predation by native species does not
appear to be at a frequency that reduces the P. volitans population
numbers in the Caribbean, likely due to the overexploitation of
native apex predators that occurs in this region. Thus, biodiver-
sity, abundance and density of native species have been reduced
from cascade effects in marine communities. Further, elevated
predation of herbivorous grazers such as parrotfish have been
shown to reduce their ecological control of algae and seaweed
in coral reef areas leading to phase shifts affecting corals and
associated diversity throughout the food web (Cure et al., 2013;
Palmer et al., 2016; Lesser and Slattery, 2011).
In addition to the high rates of native species predation and
lack of natural predators, P. volitans appears to be resistant to
infectious disease, pH, and salinity changes (Kindinger, 2014).
There have been no reports of diseases affecting lionfish and very
low levels of endo- and ecto-parasites (Kindinger, 2014). This, in
conjunction with their natural history and phenology (Hixon et
al., 2016), has led to rapid increases in abundance on many reefs
and the potential to convert reef-fish biomass to lionfish biomass,
leaving reefs void of native fish (Albins and Hixon, 2013).
4 E.E. Díaz-Ferguson and M.E. Hunter / Regional Studies in Marine Science 31 (2019) 100793
3. Phylogeography, genetic structure and demographic history
of Pterois volitans
Understanding population connectivity and genetic structure
of an invasive species, provides essential information on parental
populations, genetic relationships between neighboring popula-
tions and gene flow patterns. This information is also important
to track dispersal and identify possible introduction locations and
source of recruits (Butterfield et al., 2015). Native distribution
range of P. volitans extends from the western Pacific (southern
Japan to western Australia) to the South Pacific (Côté et al., 2013;
Cure et al., 2014) and there are also established populations along
the Red Sea (Bariche et al., 2017; see https://www.fishbase.de/
summary/Pterois-volitans.html). No reports of expansion from its
natural range to Eastern Tropical Pacific or Northeastern Pacific
areas have been recorded to date.
Wide scale standardized genetic surveys can be used to de-
termine population structure, abundance and dynamics that are
important for the establishment of accurate management policies
(Frankham et al., 2002). Currently, lionfish population surveys
have been conducted in nine countries and territories along the
Caribbean basin and the United States (Betancur-R et al., 2011;
Butterfield et al., 2015; Johnson et al., 2016). In addition, ge-
netic assessments and biogeographic studies show connectivity
and patterns of genetic diversity that provide clues for colo-
nization, expansion, and future management in the countries
and territories where the species has been reported (Betancur-
R et al., 2011). Assessments of genetic diversity are important to
determine fitness of invasive species because populations with
increased diversity may be better able to adapt to the novel
environments or withstand environmental change (Hunter et al.,
2018; Reed and Frankham, 2003; Roman and Darling, 2007). In
theory, invasive species are expected to have smaller genetic
variation than native populations as result of the founder ef-
fect. However, multiple introductions, transoceanic shipping and
globalization acting as vectors can play an important role on
invasion success and population expansion (Roman and Darling,
2007). Introduced lionfish populations are an example of this. The
species has experienced multiple introductions and is frequently
exposed to new diversity from larval input and successful re-
cruitment. This augmentation of individuals and diversity could
help to reduce lionfish susceptibility to disease and keep larval
recruitment high despite reduced variation and selection forces
acting against their effective population size e.g., genetic drift
effect is stronger in populations with reduced genetic diversity
and small effective size (Kliman et al., 2008; Bors et al., 2019).
Lionfish have very low genetic diversity off the Atlantic coast
of the United States, indicating a strong founder effect stem-
ming from a small group of P. volitans or multiple releases of
individuals in southern Florida (Côté et al., 2013). It has been
suggested that the vector for introduction into Florida waters
was the aquarium trade (Cure et al., 2012; Côté et al., 2013).
Northwestern Caribbean P. volitans populations have experienced
multiple introductions which is likely increasing their diversity.
However, this variation may be increasing through ocean currents
transporting larvae from southern locations to the north.
Many studies have continuously built upon published datasets
to assess connectivity and previous phylogeographic breaks in the
Caribbean for fishes, corals, and marine gastropods (Taylor and
Hellberg, 2003; Baums et al., 2005; Díaz-Ferguson et al., 2010).
Thus, since the lionfish introduction, many researchers have ex-
plored the consistency of these breaks with contemporary ge-
netic structure and connectivity patterns (Freshwater et al., 2009;
Betancur-R et al., 2011; Butterfield et al., 2015). Four regions of
connectivity were identified for P. volitans based on genetic dif-
ferentiation and gene flow values (northern Caribbean-Bahamas,
southern and eastern Caribbean, and northwestern Caribbean
Betancur-R et al., 2011; Butterfield et al., 2015). Recently a fifth
region of connectivity within the Gulf of Mexico was confirmed
(Johnson et al., 2016; Perez-Portela et al., 2018; Bors et al., 2019).
In addition to connectivity patterns and gene flow breaks the
numerous studies confirmed colonization routes, identified the
possibility of multiple introductions and determined lower values
of genetic diversity in the Caribbean (only 9 haplotypes) in con-
trast to the 37 haplotypes reported in their native range (Fresh-
water et al., 2009; Butterfield et al., 2015; Perez-Portela et al.,
2018). Interestingly, the haplotype H03 was detected uniquely
in Panama. This haplotype is only present in Puerto Rico, Cay-
man Islands and the locations in the northern region (Bahamas,
Bermuda and North Carolina). Thus, it is likely present in Panama
through recent introductions and may not be detected in other
areas due to its low frequency. Lionfish assessed using RADseq to
identify single nucleotide polymorphism (SNPs) have indicated a
single metapopulation without any geographic population struc-
ture (Freshwater et al., 2009; Perez-Portela et al., 2018; Bors et al.,
2019).
4. Molecular detection methods
Assessments of invasive populations have been traditionally
conducted by population dynamic studies that usually require the
direct observation and quantification of the focal species (Riccia-
rdi and MacIsaac, 2000). This traditional approach is particularly
difficult to use at the initial- or lag-phase of the invasion because
populations with lower densities are difficult to observe and col-
lect. The lag-phase of the invasion is the phase of little abundance
or no increase in species occurrence (Roman and Darling, 2007).
With the advent of molecular methods such as eDNA, detec-
tion of organisms without visually sighting them is possible using
sloughed cells and nucleic acids present in organic components of
the environment such as: water, soil and sediments (Armstrong
and Ball, 2005; Goldberg et al., 2016). This method is based on
the retrieval of genetic material naturally released by organisms
in their environment that can be detected by quantitative PCR
or Next Generation Sequencing genetic markers (Díaz-Ferguson
and Moyer, 2014; Boussarie et al., 2018). Therefore, molecular
methods and in particular eDNA have been shown to improve
the detection of invasive species in comparison to traditional
methods (Díaz-Ferguson and Moyer, 2014; Hunter et al., 2019).
Environmental DNA markers developed for P. volitans could be
highly useful for detection of the species and the calculation of
occurrence and detection estimates (Moyer et al., 2014; Hunter
et al., 2015; Takahara et al., 2019).
Metabarcoding is an alternative eDNA method to species-
specific detection that allows for a highly conserved locus to be
sequenced for many species that are present in the environmental
sample (Gillet et al., 2018; Klymus et al., 2017). This method
is preferred when novel non-native species may be dispersing
to an area but are not readily identified. It allows for detection
of cryptic species that species-specific eDNA markers might be
missing. Hybridization and cytonuclear discordance resulting in
highly divergent mitochondrial sequences could potentially cre-
ate mispriming sites on the eDNA marker locations (Hunter et al.,
2018).
5. Management strategies for control and future invasions
Due to the high fecundity of invasive lionfish, control strate-
gies targeting population reduction or elimination have proven
challenging. The removal of individual fish has been primarily
used as a mechanism for population control of lionfishes in the
Caribbean (Frazer et al., 2012; Barbour et al., 2011). Therefore,
 E.E. Díaz-Ferguson and M.E. Hunter / Regional Studies in Marine Science 31 (2019) 100793
many countries have adopted lionfish removal plans and host
events, often called ‘roundups’ or ‘derbies’ to remove large num-
bers of the population at once (i.e., in South Florida https//www.
heraldgtribune.com/news; in Panama http://laestrella.com.pa/vid
a-de-hoy/planeta/panama-declara-guerra-leon).
The ambush feeding style of lionfish limits the ability to catch
this species using hook and line fishing gear. Therefore, the main
mechanisms for catching the species includes hand netting tech-
niques and harpooning by free diving or scuba diving. Specialized
traps could also be a method use to trap fish. Innovative detection
methods such as eDNA identification, could inform the locations
divers search for lionfish or the placement of traps. Environ-
mental DNA methods have been utilized to estimate relative
abundance, although those calculations will prove challenging in
the open ocean with transport of eDNA through currents (Díaz-
Ferguson and Moyer, 2014; Díaz-Ferguson et al., 2014; Moyer
et al., 2014; Lacoursière-Roussel et al., 2016; Jo et al., 2017;
Carraro et al., 2018).
Due to the high fecundity of lionfish and long larval trans-
port period, complete eradication by fishing range-wide would
be difficult and substantial reduction of adult abundance will
require a long-term commitment (Barbour et al., 2011). Eradica-
tions in small, localized areas may be more feasible where annual
overexploitation can be intense over multiple consecutive years
(De Leon et al., 2013). Removal success would likely increase with
concurrent and coordinated removal programs in connected areas
and across the invasive range. For example, along Central Amer-
ica, southern and northern countries could coordinate efforts
to remove lionfish from the region and reduce new invasions.
Further, leveraging population genetic information could help to
inform source and sink dynamics for the targeted removal of
source populations to prevent further propagule dissemination.
However, the control efforts would likely be constantly chal-
lenged by genetic connectivity and rapid recolonization promoted
by continuous reproduction and strong larval dispersal run-on.
Eradication through individual removals would require large
investments and a multinational effort that might be financially
or logistically burdensome to some countries. If a reduction can
be made on the density of lionfish in a given population, this may
allow for juvenile prey fish to increase in size, improving their
likelihood of survival from lionfish predation and to reproduce.
The adoption of new technologies is also an option; i.e., the
use of cages or guardian robots for lionfish removal have been
successfully assessed. Also, genetic methodologies such as the
‘‘Trojan Y’’, which uses sex-reversed females with two Y chromo-
somes, could be tested in lionfish in order to produce a population
decline or loss (Chapman and Funicelli, 2016). Trojan Y tech-
niques result in a biased sex determination process which results
in the inheritance of one sex over another across generations.
As one sex becomes more dominant in the population, fewer
offspring are produced eventually driving the population to ex-
tinction (Wedekind, 2017). This method is currently being tested
in other invasive species like Oreochromis niloticus (Nile Tilapia)
(Stelkens and Wedekind, 2010; Diaz-Ferguson et al., 2019 in
preparation). A new technique that could also be considered for
control of lionfish populations is CRISPR gene-drive technology.
This technique has been proposed as a potential gene editing
tool that could be used as a non-lethal alternative to reduce pest
animal populations (Moro et al., 2018). Like the Trojan Y tech-
nique, this can lead to skewed sex ratios, decreased fertility and
fecundity, and ultimately population suppression or extirpation
(Gantz and Bier, 2015). Other control strategies include the use of
biological tools and RNA interference (RNAi) methods to inhibit
gene expression critical for survival (Baldacchino et al., 2015).
5
6. New frontiers for expansion
Due to the high fecundity of lionfish, expansion and colo-
nization of the population has happened rapidly over the past
30 years. This expansion could continue into three regions, (1)
the northwest Atlantic, (2) the southwest Atlantic, (3) the Panama
Canal and eastern Pacific.
6.1. Northern and southern population expansion of the Atlantic
Northern expansion of the population has been documented
along the East coast of the United States in the last 10 years
(Côté et al., 2013). During the summer months, there have been
reports of P. volitans in Rhode Island and New Jersey waters (Côté
et al., 2013). While this may only happen during the months
of warmer water (e.g., increased prey, recruitment success, etc.),
adaptation of invasive species can be rapid. In the future, lionfish
may adapt to the habitat to become year-round residents (Card
et al., 2018, Kimball et al., 2004). Range expansion has also been
documented in the southern limits of the invasive population into
Brazil (Ferreira et al., 2015; Luiz et al., 2013). The broad habitat
tolerance of lionfish could lead to further colonization in southern
Brazil and further along the coast of South America (Kimball et al.,
2004). Increases in water surface temperature because of climate
change could also facilitate this expansion.
6.2. Colonization of the eastern tropical Pacific via the Panama Canal
Invasive species have been identified using canal systems to
disperse previously (Gunter, 1979). It now has been reported that
lionfish are migrating from the Red Sea to the Mediterranean
through the Suez Canal (Johnston and Purkis, 2014; Bariche et al.,
2017). This use of canal systems opens the possibility of southern
Caribbean lionfish migrating through the Panama Canal into the
eastern Tropical Pacific. So far there is no evidence in the Panama
Canal of lionfishes or other scorpaeniform fish. However, there
are more than 57 identified fish that have moved into the Panama
Canal (Gunter, 1979). The eight species that are reported to have
moved across the length of the canal (Atlantic to Pacific or Pacific
to Atlantic) include the tarpon, a pipefish, three blennies and
three gobies (Gunter, 1979), with more species likely migrat-
ing since the publication of that review article. Physiologically,
lionfishes have shown to be relatively tolerant of thermal and
salinity changes and to adapt well in estuarine environments
(Jud et al., 2011, 2012; Schofield et al., 2015). Lionfish can sur-
vive low salinities for about a month (Schofield et al., 2015).
As discussed previously, lionfishes have numerous biological fea-
tures that promote demographic connectivity, colonization and
expansion, such as a long period of larval development and con-
tinuous recruitment. Therefore, movement of lionfish through
the Panama Canal and further invasion to the eastern tropical
Pacific is geographically, biologically and physiologically feasible.
Crossing of lionfish through the Panama Canal is an important
threat to prepare for because lionfish populations are currently
present in the Caribbean near the Panama Canal in the Colon
province at Buenaventura and in Portobello (57 and 42 km from
the Atlantic entrance to the Canal respectively). Pterois spp. are
also present in Guna Yala and in Bocas del Toro, Panama (First
author personal observation).
Final considerations
Considering the globalization of our world, non-native species
will continue to be released intentionally or accidentally
(Carballo-Cardenas, 2015). Biological invasions are best halted at
the beginning of the invasion curve (Ricciardi and Cohen, 2007).
To improve the chances of successfully thwarting an invasion, we
can learn from the lionfish invasion to be prepared to coordinate
6 E.E. Díaz-Ferguson and M.E. Hunter / Regional Studies in Marine Science 31 (2019) 100793
efforts for rapid response. Understanding the patterns of marine
connectivity of an invasive species within the ocean system and
the putative implications for native species will be essential for
controlling their populations.
When a new non-native species is found in Caribbean waters,
strategies should be focused on rapid removal of adults and new
recruits that are sourced from connected areas. Also, in areas
that have been identified as recruitment areas, a surveillance
plan should be established for: (1) continuous monitoring, (2)
regular assessment of genetic diversity, and (3) eDNA detection
using metagenomics if possible. Population structure and genetic
diversity could inform management, as these variables determine
population success and fitness. Understanding genetic insights
from the lionfish invasion may inform new patterns of expansion
and colonization by other potential invasive species with similar
periods of larval development. It is also important to assess
gene flow, because connectivity (unique haplotypes and numbers
of migrants per generation throughout different regions of the
colonized range) could improve removal of lionfish by targeting
source populations in order to prevent continuous replenishment.
To develop effective bio-security and -risk plans, as well inva-
sive species control and surveillance strategies, national records
(by country) of potential invasive species are needed. Local au-
thorities in Atlantic and Caribbean countries may need to work
together and establish lists of partners and stakeholders that
could expedite these processes. Finally, the implementation of
citizen scientist programs, educational programs, and applica-
tion of modern technology if available (i.e. molecular detection
methodologies, innovative marine technologies) could be system-
atically applied.
Acknowledgments
We would like to thank colleagues and former lab mates
at the University of Florida, University of Georgia and Auburn
University and the U.S. Geological Survey who contributed to
this manuscript with ideas and interesting research questions
regarding the invasive biology of Pterois volitans. We also want to
thank Coiba Scientific Station (COIBA AIP) and the Secretariat of
Science, Technology and Innovation of the Republic of Panama for
supporting EEDF’s time and dedication while writing this review
paper. To EEDF’s, School of International Training (SIT), Ichthyol-
ogy students who worked in 2017 and 2018 final projects related
to Pterois volitans behavior, microplastic ingestion, population
structure, feeding ecology and ecology of this species. To EEDF’s
friends and colleagues of the Faculty of Science, University of the
Republic in Uruguay for supporting this research with interesting
comments. We would like to thank Dr. Pamela Schofield and Amy
Benson (U.S. Geological Survey, Wetland and Aquatic Research
Center) for providing the sightings distribution map. Any use of
trade, firm, or product names is for descriptive purposes only and
does not imply endorsement by the United States Government.
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