First genetically confirmed record of the invasive devil firefish Pterois miles (Bennett, 1828) in the Mexican Caribbean

Abstract

Devil firefish Pterois miles (Bennett, 1828) is a species native to the Indo-Pacific that along with Pterois volitans (Linneaus, 1758) has been invading the western Atlantic since the 1980’s. Morphological characters, life cycle, habits, and dispersal potential of this species are very similar to those of Pterois volitans, to such extent that its taxonomic classification remains controversial. For example, the USGS database lists two species (Pterois volitans/miles) as a single one. Therefore, the probability of both species having been captured and confused is high because their identification by meristics and morphometrics is problematic. As a part of our investigation in genetic connectivity of invasive lionfish, we collected 77 specimens from Chinchorro Bank, Mexico. Identifying the samples by analysis of partial mtDNA cyt b sequences, we found that one sample corresponded to Pterois miles. The sequence of this specimen had 100% similarity to the sequence of Pterois miles specimens collected off the coast of North Carolina in 2004. This indicates that the species has extended its distribution into the Caribbean basin, but its current geographical distribution is unknown. Our results show that the presence of Pterois miles in the Caribbean appears low, approximately 1.3% of that of Pterois volitans. This study reveals the progress of the invasion of Pterois miles in the Caribbean and advocates for genetically confirmed identification and management of Pterois species.

Full text

BioInvasions Records (2017) Volume 6, Issue 2: 99–103
DOI: https://doi.org/10.3391/bir.2017.6.2.02
© 2017 The Author(s). Journal compilation © 2017 REABIC
Open Access
99
Rapid Communication
First genetically confirmed record of the invasive devil firefish
Pterois miles (Bennett, 1828) in the Mexican Caribbean
Irán A. Guzmán-Méndez
1
, Renata Rivera-Madrid
2
, Píndaro Díaz-Jaimes
3
, María del C. García-Rivas
4
,
Margarita Aguilar-Espinosa
2
and Jesús E. Arias-González
1,
*
1
Laboratorio de Ecología de Ecosistemas de Arrecifes Coralinos, Departamento de Recursos del Mar, Centro de Investigación y de
Estudios Avanzados del I.P.N.- Unidad Mérida, Ant. Carr. A Progreso km 6, A.P. 73, Cordemex, 97310 Mérida, Yucatán, México
2
Centro de Investigación Científica de Yucatán, A.C. Calle 43 No. 130, Col. Chuburná de Hidalgo, C.P. 97205 Mérida, Yucatán, México
3
Instituto de Ciencias del Mar y Limnología, Universidad Nacional Autónoma de México, Apartado Postal 70-305, México D.F.
04510, México
4
Comision Nacional de Áreas Naturales Protegidas, Parque Nacional Arrecifes de Puerto Morelos. Av. Javier Rojo Gómez,
Mz. 8 Lote 4, C.P. 77580, Puerto Morelos, Quintana Roo, México
*
Corresponding author
E-mail: earias@cinvestav.mx
Received: 6 July 2016 / Accepted: 17 January 2017 / Published online: 8 March 2017
Handling editor: Melissa Frey
Abstract
Devil firefish Pterois miles (Bennett, 1828) is a species native to the Indo-Pacific that along with Pterois volitans (Linneaus,
1758) has been invading the western Atlantic since the 1980’s. Morphological characters, life cycle, habits, and dispersal
potential of this species are very similar to those of Pterois volitans, to such extent that its taxonomic classification remains
controversial. For example, the USGS database lists two species (Pterois volitans/miles) as a single one. Therefore, the
probability of both species having been captured and confused is high because their identification by meristics and morpho-
metrics is problematic. As a part of our investigation in genetic connectivity of invasive lionfish, we collected 77 specimens
from Chinchorro Bank, Mexico. Identifying the samples by analysis of partial mtDNA cyt b sequences, we found that one
sample corresponded to Pterois miles. The sequence of this specimen had 100% similarity to the sequence of Pterois miles
specimens collected off the coast of North Carolina in 2004. This indicates that the species has extended its distribution into
the Caribbean basin, but its current geographical distribution is unknown. Our results show that the presence of Pterois miles
in the Caribbean appears low, approximately 1.3% of that of Pterois volitans. This study reveals the progress of the invasion
of Pterois miles in the Caribbean and advocates for genetically confirmed identification and management of Pterois species.
Key words: Pterois volitans, invasive species, cyt b, Coral reefs
Introduction
Devil firefish Pterois miles (Bennett, 1828) is a
species native to the Indo-Pacific, described by
Bennett in 1828 (Schultz 1986). Historically, there
have been several discussions over the taxonomic
status of Pterois volitans (Linnaeus, 1758) and
Pterois miles (Smith 1957; Beaufort and Briggs 1962;
Randall 1983). However, the most recent taxonomic
treatment defines them as separate species based on
statistical analysis of meristic and morphometric
characters (Schultz 1986). A genetic analysis revealed
that these two species diverged from a common
ancestor 2.4 to 8.3 million years ago, and the
separation of their lineages is relatively recent
(Kochzius et al. 2003). Morris et al. (2011) observed
that both species have similar morphological charac-
teristics, life cycles, habits, and dispersal potential.
These similarities may cause confusion in the
identification of the two species and hinder
population studies. Molecular studies based on the
use of mitochondrial DNA are very useful in
addressing species’ identification (Freshwater et al.
2009a; Hamner et al. 2007; Kochzius et al. 2003).

I.A. Guzman-Mendez et al.
100
Figure 1. Site where Pterois
miles was captured on
Chinchorro Bank. The
georeferenced map shows the
location of “Baliza” reef where
the specimen was caught.
The invasion of Pterois species has been remar-
kably rapid in the Western Atlantic. Since first
reported in 1985 (Schofield 2009), Pterois volitans
has successfully established itself on most Caribbean
reefs, with a geographical distribution that ranges
from the coast of New York to Brazil (Ferreira et al.
2015). Its ability to tolerate low salinity, shallow to
deep depths, and long periods of fasting make the
probability of invasion success high in a variety of
marine and coastal environments (Kimball et al. 2004).
Similarly, Pterois miles also has a history as an inva-
sive species. During the 1950s, Pterois miles invaded
the Mediterranean Sea via the Suez Canal (Golani
and Sonin 1992). Its presence in the Western Atlantic
was first confirmed in 2004 (Hamner et al. 2007).
To date, genetic evidence had shown that Pterois
miles was restricted to the east coast of the United
States and Bermuda (Betancur-R et al. 2011;
Freshwater et al. 2009b). However, Pterois miles is
morphologically similar to Pterois volitans, and
most individuals collected in the Caribbean have not
been analyzed using molecular markers to confirm
species identification. The main objective of this
study was to determine if the Devil firefish has
expanded its distribution into the Caribbean. Our
findings provide new insights into the population
distribution of the two invasive Pterois species.
Methods
We collected 77 specimens of Pterois spp. from the
Chinchorro Bank Reef (Figure 1) by scuba diving and
hand spears as part of our regional genetic connectivity
Figure 2. Specimen collected on “Baliza” reef and identified as
Pterois miles using molecular analysis. Photograph by Irán A.
Guzmán-Méndez.
study at LEEAC (Laboratorio de Ecología de
Ecosistemas de Arrecifes Coralinos, CINVESTAV-
Merida Unit). Measurements of fish length and weight
were obtained using a standard protocol (Hubbs and
Lagler 1958). Additionally, a piece of muscle from
the caudal peduncle of each specimen was collected,
preserved individually in 70% alcohol, and stored at
4 °C for subsequent analysis in the laboratory.
Genomic DNA was extracted from muscle tissue
using the DNeasy Blood and Tissue Kit (Qiagen-
69506) following the manufacturer’s instructions. A
fragment of the mtDNA-cyt b was amplified by PCR
reaction using cytb L (Schmidt and Gold 1993) and
R1063 (Hamner et al. 2007) primers, under the
conditions described in Hamner et al. (2007). The cyt b

First genetically confirmed record of Pterois miles in the Mexican Caribbean
101
Figure 3. Phylogenetic tree generated using the Neighbor-Joining method (Saitou and Nei 1987), with sum branch lengths = 0.136082
(branch lengths noted above each branch).
fragment obtained was purified with QIAquick PCR
Purification Kit (Qiagen-28106) and sent for sequen-
cing at the Clemson University Genomics Institute,
(CUGI, USA). The generated sequences were compared
and species identifications confirmed using the Basic
Local Alignment Search Tool (BLAST) program in
the GenBank public database.
A phylogenetic tree was generated using the
Neighbor-Joining method (Saitou and Nei 1987).
Evolutionary distances were computed using the
Maximum Composite Likelihood method (Tamura
et al. 2004) and are in units of the number of base
substitutions per site. The analysis involved 43
nucleotide sequences. Codon positions included were
1st+2nd+3rd+noncoding (all gaps and missing data
were eliminated), resulting in 726 bp in the final
dataset. All evolutionary analyses were conducted in
MEGA7 (Kumar et al. 2016).

I.A. Guzman-Mendez et al.
102
Results
Of the 77 specimens collected near Chinchorro Bank,
our analyses revealed 76 Pterois volitans and one
individual of Pterois miles. The P. miles specimen
was found in a place known as “Baliza”
(18º35′21.00″N; 87º24′58.70″W; Figure 1) at a depth
of 27 m, and was an adult (Figure 2). In comparing
specimens of similar size, morphometric measure-
ments showed strong similarity between the two
Pterois species (Table 1). The partial mtDNA-cyt b
sequence generated from the Pterois miles specimen
was 783 bp (Genbank accession no. KU833279). This
sequence was 99% similar to the complete mitochon-
drial genome of a Red Sea Pterois miles specimen
(Genbank accession no. LK022697.1), 100% similar
to the partial cyt b sequence from North Carolina
specimens (Genbank accession no. EF209676.1), but
only 94% similar to the partial cyt b sequence
haplotype AA of Pterois volitans (Genbank accession
no. DQ482606.1). The phylogenetic tree showed
that the sequence KU833279 corresponded to the
Pterois miles clade (Figure 3). Average genetic distance
(Kimura 2-parameter model) between Pterois miles
and Pterois volitans was 0.075.
Discussion
The invasion of lionfish into the Western Atlantic
and the Caribbean has been unprecedented and rapid
(Schofield 2009). While Pterois volitans has been
reported widely, P. miles has gone nearly undetected,
except for a few records in North Carolina and
Bermuda (Hamner et al. 2007; Freshwater et al.
2009a; Betancur-R et al. 2011). To date, P. miles
had never been documented in the Caribbean. And
prior to this study, there had been only one lionfish
reported anecdotally from Chinchorro Bank, but the
record was without supporting evidence, and the
individual was not identified to species (USGS 2016).
Our results provide the first scientifically verified
and molecularly identified records of P. volitans and
P. miles from Chinchorro Bank, and the first
confirmed report of P. miles in the Caribbean.
The presence of P. miles in the Mexican Caribbean
is a significant expansion of its previously known
distribution along the east coast of the United States
and Bermuda (Betancur-R et al. 2011). There are two
reasons why this species may have gone undetected
until now. First, it is extremely difficult to differen-
tiate P. miles and P. volitans, given their striking
morphological similarity. The USGS-NAS (2016)
lists the two species together as “Pterois volitans/
miles” for this very reason. The only way to identify
the species in their non-native range with accuracy
Table 1. Morphometric measurements of Pterois miles and
P. volitans of similar size. NA = data not available due to loss
during capture.
Morphological traits P. miles P. volitans
Weight 0.576 kg 0.562 kg
Total length 36.5 cm 36.6 cm
Fork length 78 % 76.5 %
Head length 25.6 % 25.7 %
Pectoral fin length 41.9 % 42.4 %
Length of the pelvic fins 29 % 30 %
Max body height 29.3 % 22.7 %
Min body height 7.2 % 7.7 %
Max height of anal fin 19.3 % 14.1 %
Length of dorsal fin NA 13.9 %
Length second dorsal fin 23.4 % 16.8 %
Eye diameter 4.1 % 4.3 %
Length of mouth 9.8 % 10.2 %
Snout length 14.1 % 13.5 %
and consistency is through molecular analysis
(Freshwater et al. 2009a, 2009b; Hamner et al. 2007)
as demonstrated here by our findings. Second, based
on the sample size of lionfish collected from
Chinchorro Bank (77 individuals), the abundance
of P. miles may be very low (1.3%) relative to that
of P. volitans. It remains unclear whether this result
reflects the persistence of P. miles at small
population levels or alternatively, the recent arrival
of a species that has yet to increase in abundance.
Additional molecular studies are needed to fully
understand each species distribution, the connectivity
between populations, and the dynamics of dispersal
throughout the invaded range. For example, our cyt
b results show that the mitochondrial haplotype of
the sample found in Chinchorro Bank corresponds
100% to the cyt b sequences of P. miles collected in
North Carolina. Although it remains uncertain, the
arrival of this species to Chinchorro Bank may be
highly influenced by currents and mesoscale
processes that have fostered larvae transport, slowly
broadening the distribution of both species.
Acknowledgements
We thank the Consejo Nacional de Ciencia y Tecnologia
(CONACyT) for financial support (Grant 215434) and the National
Commission of Natural Protected Areas (CONANP) for logistical
support in the sampling at Chinchorro Bank, as well as ECORED
(194539). Our special gratitude to the staff of Banco Chinchorro
Biosphere Reserve and to the fishermen who participated in the
collection of samples. A special mention to Javier Salas and his
XTC Dive Center team who provided us with the boat and diving
equipment. We are much obliged to Dr. D. Wilson Freshwater for
his valuable contributions, suggestions, and critical review of the
manuscript. The authors would also like to thank anonymous
reviewers for improving the manuscript.

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103
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