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First record of the genus Leptodactylus (Anura:
Leptodactylidae) in Cuba: Leptodactylus fragilis, a biological
invasion?
Tomás M. Rodríguez-Cabrera
a
, L. Yusnaviel García-Padrón
b
, Andrés R. Acosta Galvis
c
,
Rafael O. de Sá
d
and Roberto Alonso Bosch
e
a
Sociedad Cubana de Zoología, La Habana, Cuba;
b
Departamento de Museología, Museo de Historia
Natural “Tranquilino Sandalio de Noda”, Pinar del Río, Cuba;
c
Departemento de Colecciones Biológicas,
Subdirección de Investigaciones, Instituto de Investigación de Recursos Biológicos Alexander von
Humboldt, Villa de Leyva-Boyacá, Colombia;
d
Department of Biology, University of Richmond, Richmond,
USA;
e
Museo de Historia Natural “Felipe Poey”, Facultad de Biología, Universidad de La Habana, La
Habana, Cuba
ABSTRACT
The Neotropical genus Leptodactylus is currently represented by three
species in the West Indies (Leptodactylus albilabris,Leptodactylus fallax
and Leptodactylus validus). Based on morphological, acoustic and mole-
cular evidence, we document the presence of a fourth species in the
Caribbean region, Leptodactylus fragilis (Brocchi, 1877). The species was
found at two localities in western Cuba, and molecular data suggest a
northern South American origin, possibly Venezuela, for these popula-
tions. We discuss the potential invasive status of L. fragilis,basedonits
known distribution, relative abundance, behaviour and possible
impacts on native species of Cuban amphibians.
ARTICLE HISTORY
Received 4 May 2018
Accepted 3 July 2018
KEYWORDS
Advertisement call; 16S
mitochondrial DNA; Greater
Antilles; introduced species;
range extension
Introduction
The arrival of exotic species is currently recognized as one of the most important threats
to local biodiversity, second only to habitat loss and modification by anthropogenic
activities, particularly if the species has the potential to be invasive (McGeoch et al. 2010;
Simberloffand Rejmánek 2011). Invasive species appear to increase extinction risk in
geographically and evolutionarily isolated systems such as island communities
(Courchamp et al. 2003; Simberloffet al. 2013). About 95% of bird, 90% of reptile and
70% of mammal extinctions have occurred on islands; these extinctions are primarily the
result of human activities, i.e. hunting, deforestation, agriculture, introduction of non-
native species (Keitt et al. 2011).
Invasive species are those that have been transferred from their native geographic
range, with evidence of subsequent release or escape into the wild or human environ-
ments (transport, or introduction, is the first step in the invasion process). They have
successfully colonized and currently exist in the wild or around human settlements and
CONTACT Roberto Alonso Bosch ralonso@fbio.uh.cu;ralonso@fbio.uh.cu
Supplemental data for this article can be accessed here.
JOURNAL OF NATURAL HISTORY
2018, VOL. 52, NOS. 29–30, 1883–1892
https://doi.org/10.1080/00222933.2018.1498549
© 2018 Informa UK Limited, trading as Taylor & Francis Group
Published online 03 Aug 2018
have increased in abundance (establishment and possibly a lag phase). Moreover, the
species spread beyond the release or escape point (spread) and could represent a
serious threat for ecosystems and biodiversity causing ecological or economic damage
and socio-economic harms (impacts) (Sakai et al. 2001; Marsico et al. 2010). A number of
species have been deliberately or accidentally introduced in the Caribbean islands (e.g.
rats, dogs, cats, mice, mongooses, birds, lizards, snakes, amphibians, fishes) with con-
sequent ecological and evolutionary impacts on native species (Kairo et al. 2003;
Engeman et al. 2006; Borroto-Páez 2009; Medina et al. 2011; Powell et al. 2011).
The number of known herpetological introductions continues to grow around the
world. More than 780 species have been involved in thousands of successful introduc-
tion events; almost half of them have become invasive (Kraus 2015). In the greater
Caribbean, the arrival of 130 species (25 amphibians and 105 reptiles) has been pre-
viously documented (Powell et al. 2011) with some populations established for a short
period and others exerting long-term and severe impacts on native species and ecosys-
tems. At least 26 species (five amphibians and 21 reptiles) arrived on the Cuban
Archipelago as a result of more than 35 different introduction events (Borroto-Páez
et al. 2015). These authors reported that one amphibian and ten reptile species were
established, nine of which became invasive. The American Bullfrog, Lithobates catesbeia-
nus (Shaw, 1802), widely distributed throughout the main island of Cuba and the Isla de
la Juventud, was the only invasive amphibian considered in their review.
The Neotropical frog genus Leptodactylus Fitzinger, 1826 is represented by two
endemic species in the West Indies: Leptodactylus albilabris (Günther, 1859)
(Hispaniola, Puerto Rico and the Virgin Islands) and Leptodactylus fallax Müller, 1926
(Lesser Antilles) (de Sá et al. 2014). A third species, Leptodactylus validus Garman, 1888,
occurs in northern South America, Trinidad, Tobago and the southern Lesser Antilles
(Grenada, Grenadines and St Vincent) (Camargo et al. 2009; Henderson and Powell 2009;
Powell and Henderson 2012). Herein, we add a fourth species to this list, Leptodactylus
fragilis, a member of the Leptodactylus fuscus species group, recently found at two
localities in western Cuba.
Materials and methods
On 23 and 24 August 2016, approximately 8 km west of Guane, on the road to Mantua
between the villages of Santa Rosa and Veinte de Mayo, Guane Municipality, Pinar del Río
Province (10 m above sea level, 22.19777 N, −84.17564 W, WGS84), we heard and collected a
series of active individuals of a leptodactylid frog, never recorded from Cuba (Figure 1). A
year earlier, in July 2015, one of us (LYG) heard an unknown frog call in the vicinity of
Sandino, also in Pinar del Río Province in western Cuba. The specimen was not collected or
recorded on that occasion. Recently, the species was again found and collected in Sandino
(30 m above sea level, 22.078767 N, −84.202868 W, WGS84), approximately 13.5 km airline
distance south-southwest of the previous locality (Figure 1). Based on external morphology
and acoustic features,the frogs correspond to the same species as those collected in Guane.
We recorded vocalizations using a Sony PCM-M10 Digital Recorder incorporated with
Electret Condenser internal microphones from active choruses that started after heavy
afternoon rains We recorded the advertisement calls (at 44.1-kHz sampling frequency
and 24-bit resolution) of one male at each of the above localities. Sound analysis was
1884 T.M. RODRÍGUEZ-CABRERA ET AL.
performed with Raven 1.3 software (Bioacoustics Research Program, Cornell Laboratory
of Ornithology, 2012), using Hanning window, FFT size 2048, overlap 95%. We used the
terminology of Köhler et al. (2017) for description of calls. The following temporal and
spectral features were measured from a sequence of 10 consecutive calls from each
individual: call duration was measured at zero amplitude level on the oscillogram
(error = 0.1 ms), call rate was calculated as the reciprocal of the intercall interval
(± 0.1 ms), and the pulse rate as the ratio between the number of pulses per call and
call duration. Dominant frequency was measured to the nearest 0.02 kHz at the peak of
maximum amplitude in the power spectrum of each call. Individual and chorus record-
ings were deposited at the Fonozoo sound archive (Fonoteca Zoologica, Madrid, Spain,
www.fonozoo.org). Air temperature (± 0.5°C) and relative humidity (± 5%) were mea-
sured at the recording site using a thermohygrometer (HANNA Instruments,
Woonsocket, Rhode Island, USA) in Sandino. For the Guane locality, we used data
from the nearest Meteorological Station (Figure 1) of the national network of stations
of the Cuban Institute of Meteorology (INSMET). The recorded adult male from Sandino
(recording voucher) and six individuals from Guane (three adult females and three sub-
adult males) were collected and their snout–vent lengths were measured to the nearest
0.01 mm with a caliper. These animals were euthanized, fixed and preserved in 70%
ethanol. The specimens were deposited at the Museum of Natural History ‘Tranquilino
Sandalio de Nodas’, Pinar del Río (accession no. LYG-529), and also at the Museum of
Natural History ‘Felipe Poey’, Faculty of Biology, University of Havana, Cuba (accession
no. MFP11608-11613).
The external morphology, acoustic features and behaviour allowed us to identify the
specimens as members of the genus Leptodactylus; tissue samples were obtained from
Figure 1. Geographic records of Leptodactylus fragilis in Pinar del Río Province Western Cuba. The
expanded topographic map shows the two known records (red triangles). 1. West of Guane. 2.
Vicinity of Sandino. Red contours represent protected areas and the blue square indicates the
location of the nearest Meteorological Station of the national network of stations of the Cuban
Institute of Meteorology (INSMET).
JOURNAL OF NATURAL HISTORY 1885
toe clips or thigh muscles of the specimens collected from Guane as a third source of
data for species identification. Total genomic DNA was extracted from muscle tissues of
four of the ethanol-preserved specimens using Qiagen DNeasy kit (Valencia, CA, USA).
We used the standard 16S barcoding marker with protocols and polymerase chain
reaction profiles previously published (de Sá et al. 2012,2014). GenBank Accession
numbers are given in the Supplementary material (Appendix S1). We also included all
16S sequences for L. fragilis available at GenBank. Outgroups were chosen based on an
extensive phylogenetic hypothesis of Leptodactylus by including representatives of the
four Leptodactylus species groups (i.e. Leptodactylus latrans species group: Leptodactylus
bolivianus and Leptodactylus macrosternum;Leptodactylus melanonotus species group:
Leptodactylus colombiensis and L.validus;Leptodactylus pentadactylus species group:
L.myersi, and L.fuscus species group: Leptodactylus bufonius and L.fuscus) and two
species of Hydrolaetare that had previously been recovered as the sister clade of
Leptodactylus (de Sá et al. 2014). Phylogenetic analysis was conducted using RaxML
(evolution model GTRGamma and 1000 bootstrap replicates) implemented in CIPRES
Science Gateway V.3.3 (Stamatikis 2006; Miller et al. 2010).
Results
The dorsal coloration in life of the specimens encountered in the field was spotted or
blotched with dark markings, which were often chevron-shaped and sometimes con-
fluent (Figure 2a). The specimens examined lack dorsal folds, have a pair of dorsolateral
folds extending from the edge of the eye posteriorly, and a pair of interrupted lateral
folds extending from the dorsal edge of the tympanum to the anterior first third of the
flanks; no toe fringes; the upper shank barred has white tubercles; the posterior surface
Figure 2. Leptodactylus fragilis from Guane, Pinar del Río, Cuba. (a) Dorsolateral view of an adult
female. (b) Male vocalizing at the entrance of small burrow in the flooded area. Photos by R. López-
Silvero. (c) Oscillogram and spectrogram of one advertisement call of L. fragilis from Sandino, Pinar
del Río, Cuba, recorded on 12 April 2017, 2150 h, air temperature 23.1°C. (FZ SOUND CODE 11168).
1886 T.M. RODRÍGUEZ-CABRERA ET AL.
of thighs has a light, longitudinal stripe; an immaculate venter or with small spots on
anterior and lateral areas. A light lip stripe extends from the tip of the snout, under the
eye and tympanum, and continues over the commissural gland; the commissural gland
is present in all examined specimens. All individuals from Guane are small size: females
X = 34.03 ± 1.59 mm (n= 3) and sub-adult males X = 24.63 ± 0.32 mm (n= 3). The
voucher specimen of the recordings from Sandino was 34.3 mm snout–vent length.
At Guane, calling activity began close to sunset (1900 h) and extended at least until
midnight after heavy rains during the previous afternoons (1600–1800 h). The rain filled
the roadside ditches and formed many temporary ponds within rice fields, where several
males (> 40 individuals) were calling in dense choruses. Calling males were observed
vocalizing from or very close to the water, usually 50 cm or less. These males were
positioned at the entrance of small burrows dug at the base of grass clumps in roadside
ditches or under lumps in the flooded rice fields (Figure 2b). They were spaced at least
1 m apart. The females were observed wandering over the area where males were
calling. Air temperature and relative humidity during vocalizations (two nights) were
25.9–27.3°C and 90–96%, respectively. At Sandino, frogs were observed vocalizing in a
small ditch next to a sewer within a village; a chorus of at least eight males was heard
and the vocal activity extended from 2030 h until just after 2300 h. At Sandino most
specimens were hiding and difficult to find under branches, leaves and logs.
Advertisement calls of one individual (LYG-529) were recorded at 21:50 h, air tempera-
ture of 23.1°C and 71% relative humidity.
Calls of the two males recorded (one from each locality) exhibited little variation in most
acoustic characteristics; overall, the calls had the same temporal and spectral structure. The
call is amplitude modulated with an increase in energy and consists of a single pulsed note
with 20–23 pulses [pulse rate (PR) at Guane: PR = 136.2 ± 4.4 pulses/s, and at Sandino:
PR = 113.8 ± 2.8 pulses/s], although at the end of the call, two or three indistinct pulses could
be added. The advertisement call has a harmonic structure and is emitted at a rate of 77–85
calls/min and lasts 0.17–0.21 s (Figure 2c). Spectrally the call starts at about 600–699 Hz and
has a rapid rise in frequency at the end of the call. The dominant frequency (DF) is the
fundamental frequency which was 1119.7–1808.8 Hz (at Guane: DF = 1136.94 ± 36.34 Hz; at
Sandino: DF = 1722.68 ± 57.43 Hz).
Overall, we recovered a well-supported clade [bootstrap value (bv) = 96] that includes
most of the samples (28 of 30 individuals included) assigned to L. fragilis. This larger
clade consists of three subclades: 1. all available samples, except one, from Colombia
(bv = 89); 2. all samples from Panama (bv = 90); and 3. a clade (bv = 80) comprising the
four specimens from Cuba grouped (bv = 100) and with closer relationships to a clade
(bv = 100) consisting of one sample from Colombia and Venezuela, respectively
(Figure 3). Two samples identified as L. fragilis from Belize are closer to L. bufonius
Boulenger, 1894, than to other L. fragilis samples (bv = 80).
Discussion
The overall morphology, measurements and call characteristics of the specimens found
in Cuba agree with previous descriptions of the species L. fragilis (Heyer et al. 2006;de
Sá et al. 2014). Furthermore, the molecular analysis also supported the identity of the
species as L. fragilis. That species is known to range from southernmost Texas (USA) on
JOURNAL OF NATURAL HISTORY 1887
the Atlantic coast and Colima, Mexico on the Pacific coast through Middle America to
northern Colombia including the Cauca and Magdalena valleys, the Río Arauca and Río
Apure drainages in Colombia and northern Venezuela extending as far as the
Venezuelan State of Sucre (de Sá et al. 2014). Our contribution represents the first report
of this species in Cuba and the Greater Antilles.
It is not clear if the species arrived in Cuba through natural dispersal mechanisms or if
it was a human-mediated introduction to the island. However, interviews with local
people regarding the occurrence of this species of frog suggest a relatively recent arrival.
Most of the interviewed people at the Guane locality were able to recognize the
presence of this species by sightings or listening to its calls. Sightings of the species
go back at least 2 or 3 years. It is interesting that the samples from Cuba are more
closely related to a sample from the state of Casanare, which corresponds to our
easternmost sample from Colombia and a sample from the western state of Tachira,
Venezuela, which corresponds to part of the northeastern boundaries between the two
countries. We are uncertain of the introduction pathway of L. fragilis to Cuba; however,
Figure 3. Molecular analysis. RaxML tree of Leptodactylus fragilis, values on branches indicate
bootstrap support. Samples from Cuba clustered in well-supported clades with samples of
L. fragilis and are more closely related to populations of L. fragilis in northeastern Colombia and
northwestern Venezuela.
1888 T.M. RODRÍGUEZ-CABRERA ET AL.
considering the frequent commercial and cargo exchanges, including agricultural pro-
ducts, between Venezuela and Cuba, the species could have accidentally arrived via
cargo shipments from Venezuela. We have no evidence to support either a single or
multiple introduction events.
Although L. fragilis could become an invader in Cuba, at this time, the introduction
would qualify as being at Stage 3–Stage 4 of a five-stage process for introduced species
(Hoogmoed and Avila-Pires 2015). Stage 3 is defined as when a non-indigenous species
survives and establishes (= reproduces) in the new suitable environment, but remains
uncommon and localized. Whereas Stage 4 is considered when a non-indigenous
species becomes either widespread, but remains uncommon, or dominant in abundance
or density but remains localized. The impact of this introduced species on the native
biodiversity of the island is unknown. During our observations, L. fragilis was found in
syntopy with other native riparian or aquatic-breeding anurans of three different families
(Eleutherodactylidae, Hylidae, Bufonidae), i.e. Eleutherodactylus riparius Estrada and
Hedges, 1998,Osteopilus septentrionalis (Duméril and Bibron, 1841) and Peltophryne
empusa (Cope, 1862); all of which stopped their vocalizations when the chorus of
L. fragilis became more intense. Considering the natural history and adaptability of
L. fragilis in its native range, particularly its ability to exploit a variety of habitats, local
abundance and breeding activity (Heyer 1978; Heyer et al. 2006; de Sá et al. 2014),
different types of impacts could be expected on Cuban amphibian populations.
Consequently, it will be of paramount importance to initiate a programme to monitor
L. fragilis in Cuba and any changes in native fauna, e.g. decrease in abundance, popula-
tion extinction or contraction, change in behaviour, reproductive interference (by inter-
fering in their acoustic niche) and change in spatial ecology (Kraus 2015). The localities
where L. fragilis was found in Cuba are very close to at least three important protected
areas in the western part of the main island. The record from Guane is just 10.6 km
westward of the Ecological Reserve ‘Guane-Paso Real de Guane’and 15 km northwest of
the Floristic Reserve ‘San Ubaldo-Sabanalamar’. The population from Sandino is just
5.9 km northeast of the Biosphere Reserve ‘Guanahacabibes’and 15.5 km northwest of
the Floristic Reserve ‘San Ubaldo-Sabanalamar’. The Biosphere Reserve ‘Guanahacabibes’
is one of the most significant protected areas of Cuba. This region is home to 14 native
amphibians, 12 of them endemic species (86%), including the local endemic
Eleutherodactylus guanahacabibes Estrada and Novo, 1985 (Rodríguez–Schettino et al.
2009; Rivalta et al. 2014). The Floristic Reserve ‘San Ubaldo-Sabanalamar’protects an
important population of the endemic and endangered toad Peltophryne cataulaciceps
(Schwartz, 1959) (Bufonidae), which reproduces in temporary ponds and lagoons formed
during the rainy season (Díaz and Cádiz 2008; Alonso 2011) and could also be particu-
larly vulnerable to direct ecological competition with L. fragilis.
This is the first species of Leptodactylus reported from the West Indies outside its
natural distribution range; attempts to introduce L. fallax to Grenada, Martinique and
Puerto Rico were not successful (Kaiser 1994). Additional fieldwork in the lowlands of
Western Cuba is required to determine if any other population of L. fragilis has been
established and to understand the distribution and relative abundance of the species in
Cuba. Other tools, such as ecological niche modelling, could also help us to predict its
potential spread in the near and long-term future. Detailed studies are needed to
JOURNAL OF NATURAL HISTORY 1889
understand the interaction and impact of L. fragilis on native species in Cuba and to
assess its potential invasive status.
Acknowledgements
We thank Raimundo López-Silvero and Alejandro M. Rodríguez for their valuable field assistance
and photographs. The expedition to Guane was made under the project ‘Ecology and conserva-
tion of the endemic scorpion genus Tityopsis in native forests of western Cuba (II)’, funded by The
Rufford Foundation to the senior author (project #19261-2). Jorge L. Perez provided the meteor-
ological data from station 313 at Isabel Rubio, Pinar del Río province, Cuba. Rafael Borroto, Sheila
Rodríguez, Natan Medeiros and Thiago R. de Carvalho provided constructive suggestions on the
earlier version of the manuscript. The manuscript also benefitted from helpful comments from two
anonymous reviewers. Molecular work was done under Research Agreement 15-276 between
Instituto de Investigación de Recursos Biológicos Alexander von Humboldt (IAvH) and the
University of Richmond. We also thank Maria Estefanía López for help at the Colección de
Tejidos (IAvH-CT) of the Instituto de Investigación de Recursos Biológicos Alexander von
Humboldt.
Disclosure statement
No potential conflict of interest was reported by the authors.
Funding
This work was supported in part by the The Rufford Foundation (www.rufford.org) to the senior
author under Grant 19261-2 (“Ecology and conservation of the endemic scorpion genus Tityopsis
in native forests of western Cuba II”).
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