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BioInvasions Records (2017) Volume 6, Issue 2: 99103

DOI: [Link]
Open Access
2017 The Author(s). Journal compilation 2017 REABIC

Rapid Communication

First genetically confirmed record of the invasive devil firefish


Pterois miles (Bennett, 1828) in the Mexican Caribbean

Irn A. Guzmn-Mndez 1 , Renata Rivera-Madrid 2 , Pndaro Daz-Jaimes 3 , Mara del C. Garca-Rivas 4 ,


Margarita Aguilar-Espinosa 2 and Jess E. Arias-Gonzlez 1, *
1
Laboratorio de Ecologa de Ecosistemas de Arrecifes Coralinos, Departamento de Recursos del Mar, Centro de Investigacin y de
Estudios Avanzados del I.P.N.- Unidad Mrida, Ant. Carr. A Progreso km 6, A.P. 73, Cordemex, 97310 Mrida, Yucatn, Mxico
2
Centro de Investigacin Cientfica de Yucatn, A.C. Calle 43 No. 130, Col. Chuburn de Hidalgo, C.P. 97205 Mrida, Yucatn, Mxico
3
Instituto de Ciencias del Mar y Limnologa, Universidad Nacional Autnoma de Mxico, Apartado Postal 70-305, Mxico D.F.
04510, Mxico
4
Comision Nacional de reas Naturales Protegidas, Parque Nacional Arrecifes de Puerto Morelos. Av. Javier Rojo Gmez,
Mz. 8 Lote 4, C.P. 77580, Puerto Morelos, Quintana Roo, Mxico
*Corresponding author
E-mail: earias@[Link]

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 1980s. 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 that these two species diverged from a common


ancestor 2.4 to 8.3 million years ago, and the
Devil firefish Pterois miles (Bennett, 1828) is a separation of their lineages is relatively recent
species native to the Indo-Pacific, described by (Kochzius et al. 2003). Morris et al. (2011) observed
Bennett in 1828 (Schultz 1986). Historically, there that both species have similar morphological charac-
have been several discussions over the taxonomic teristics, life cycles, habits, and dispersal potential.
status of Pterois volitans (Linnaeus, 1758) and These similarities may cause confusion in the
Pterois miles (Smith 1957; Beaufort and Briggs 1962; identification of the two species and hinder
Randall 1983). However, the most recent taxonomic population studies. Molecular studies based on the
treatment defines them as separate species based on use of mitochondrial DNA are very useful in
statistical analysis of meristic and morphometric addressing species identification (Freshwater et al.
characters (Schultz 1986). A genetic analysis revealed 2009a; Hamner et al. 2007; Kochzius et al. 2003).

99
I.A. Guzman-Mendez et al.

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 Figure 2. Specimen collected on Baliza reef and identified as
was first confirmed in 2004 (Hamner et al. 2007). Pterois miles using molecular analysis. Photograph by Irn A.
To date, genetic evidence had shown that Pterois Guzmn-Mndez.
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 study at LEEAC (Laboratorio de Ecologa de
morphologically similar to Pterois volitans, and Ecosistemas de Arrecifes Coralinos, CINVESTAV-
most individuals collected in the Caribbean have not Merida Unit). Measurements of fish length and weight
been analyzed using molecular markers to confirm were obtained using a standard protocol (Hubbs and
species identification. The main objective of this Lagler 1958). Additionally, a piece of muscle from
study was to determine if the Devil firefish has the caudal peduncle of each specimen was collected,
expanded its distribution into the Caribbean. Our preserved individually in 70% alcohol, and stored at
findings provide new insights into the population 4 C for subsequent analysis in the laboratory.
distribution of the two invasive Pterois species. Genomic DNA was extracted from muscle tissue
using the DNeasy Blood and Tissue Kit (Qiagen-
Methods 69506) following the manufacturers instructions. A
fragment of the mtDNA-cyt b was amplified by PCR
We collected 77 specimens of Pterois spp. from the reaction using cytb L (Schmidt and Gold 1993) and
Chinchorro Bank Reef (Figure 1) by scuba diving and R1063 (Hamner et al. 2007) primers, under the
hand spears as part of our regional genetic connectivity conditions described in Hamner et al. (2007). The cyt b

100
First genetically confirmed record of Pterois miles in the Mexican Caribbean

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

101
I.A. Guzman-Mendez et al.

Results Table 1. Morphometric measurements of Pterois miles and


P. volitans of similar size. NA = data not available due to loss
Of the 77 specimens collected near Chinchorro Bank, during capture.
our analyses revealed 76 Pterois volitans and one Morphological traits P. miles P. volitans
individual of Pterois miles. The P. miles specimen
Weight 0.576 kg 0.562 kg
was found in a place known as Baliza
Total length 36.5 cm 36.6 cm
(183521.00N; 872458.70W; Figure 1) at a depth Fork length 78 % 76.5 %
of 27 m, and was an adult (Figure 2). In comparing Head length 25.6 % 25.7 %
specimens of similar size, morphometric measure- Pectoral fin length 41.9 % 42.4 %
ments showed strong similarity between the two Length of the pelvic fins 29 % 30 %
Pterois species (Table 1). The partial mtDNA-cyt b Max body height 29.3 % 22.7 %
sequence generated from the Pterois miles specimen Min body height 7.2 % 7.7 %
Max height of anal fin 19.3 % 14.1 %
was 783 bp (Genbank accession no. KU833279). This
Length of dorsal fin NA 13.9 %
sequence was 99% similar to the complete mitochon- Length second dorsal fin 23.4 % 16.8 %
drial genome of a Red Sea Pterois miles specimen Eye diameter 4.1 % 4.3 %
(Genbank accession no. LK022697.1), 100% similar Length of mouth 9.8 % 10.2 %
to the partial cyt b sequence from North Carolina Snout length 14.1 % 13.5 %
specimens (Genbank accession no. EF209676.1), but
only 94% similar to the partial cyt b sequence
haplotype AA of Pterois volitans (Genbank accession and consistency is through molecular analysis
no. DQ482606.1). The phylogenetic tree showed (Freshwater et al. 2009a, 2009b; Hamner et al. 2007)
that the sequence KU833279 corresponded to the as demonstrated here by our findings. Second, based
Pterois miles clade (Figure 3). Average genetic distance on the sample size of lionfish collected from
(Kimura 2-parameter model) between Pterois miles Chinchorro Bank (77 individuals), the abundance
and Pterois volitans was 0.075. of P. miles may be very low (1.3%) relative to that
of P. volitans. It remains unclear whether this result
Discussion reflects the persistence of P. miles at small
population levels or alternatively, the recent arrival
The invasion of lionfish into the Western Atlantic of a species that has yet to increase in abundance.
and the Caribbean has been unprecedented and rapid Additional molecular studies are needed to fully
(Schofield 2009). While Pterois volitans has been understand each species distribution, the connectivity
reported widely, P. miles has gone nearly undetected, between populations, and the dynamics of dispersal
except for a few records in North Carolina and throughout the invaded range. For example, our cyt
Bermuda (Hamner et al. 2007; Freshwater et al. b results show that the mitochondrial haplotype of
2009a; Betancur-R et al. 2011). To date, P. miles the sample found in Chinchorro Bank corresponds
had never been documented in the Caribbean. And 100% to the cyt b sequences of P. miles collected in
prior to this study, there had been only one lionfish North Carolina. Although it remains uncertain, the
reported anecdotally from Chinchorro Bank, but the arrival of this species to Chinchorro Bank may be
record was without supporting evidence, and the highly influenced by currents and mesoscale
individual was not identified to species (USGS 2016). processes that have fostered larvae transport, slowly
Our results provide the first scientifically verified broadening the distribution of both species.
and molecularly identified records of P. volitans and
P. miles from Chinchorro Bank, and the first
confirmed report of P. miles in the Caribbean. Acknowledgements
The presence of P. miles in the Mexican Caribbean We thank the Consejo Nacional de Ciencia y Tecnologia
is a significant expansion of its previously known (CONACyT) for financial support (Grant 215434) and the National
distribution along the east coast of the United States Commission of Natural Protected Areas (CONANP) for logistical
support in the sampling at Chinchorro Bank, as well as ECORED
and Bermuda (Betancur-R et al. 2011). There are two (194539). Our special gratitude to the staff of Banco Chinchorro
reasons why this species may have gone undetected Biosphere Reserve and to the fishermen who participated in the
until now. First, it is extremely difficult to differen- collection of samples. A special mention to Javier Salas and his
tiate P. miles and P. volitans, given their striking XTC Dive Center team who provided us with the boat and diving
equipment. We are much obliged to Dr. D. Wilson Freshwater for
morphological similarity. The USGS-NAS (2016) his valuable contributions, suggestions, and critical review of the
lists the two species together as Pterois volitans/ manuscript. The authors would also like to thank anonymous
miles for this very reason. The only way to identify reviewers for improving the manuscript.
the species in their non-native range with accuracy

102
First genetically confirmed record of Pterois miles in the Mexican Caribbean

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