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First record of the invasive greenhouse frog (Eleutherodactylus planirostris) in the Mexican Caribbean
Primer registro de la rana de invernadero invasora (Eleutherodactylus planirostris) en el Caribe mexicano
José Rogelio Cedeño-Vázquez1, Javier González-Vázquez2, Arely Martínez-Arce1, Luis Canseco-Márquez3
1 Departamento de Sistemática y Ecología Acuática. El Colegio de la Frontera Sur, Unidad Chetumal, Av. Centenario Km 5.5, 77014 Chetumal, Quintana Roo, Mexico
2 Aviario Xamán Ha, Paseo Xamán Ha Mz13-A, Fracc. Playacar, 77710 Playa del Carmen, Quintana Roo, Mexico
3 Departamento de Biología Evolutiva, Laboratorio de Herpetología, Facultad de Ciencias. Universidad Nacional Autónoma de México, Av. Universidad 3000, Ciudad Universitaria, Coyoacán, 04510, México, D.F., Mexico
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          "en" => "<p id="spar0010" class="elsevierStyleSimplePara elsevierViewall">The greenhouse frog&#44; <span class="elsevierStyleItalic">Eleutherodactylus planirostris</span>&#46; Specimens found in Playa del Carmen&#44; Quintana Roo&#44; Mexico&#46; Vouchers MZFC 27464-66 &#40;up to down order&#41;&#46; Photos by H&#46; Bahena-Basave&#46;</p>"
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    "textoCompleto" => "<span class="elsevierStyleSections"><p id="par0005" class="elsevierStylePara elsevierViewall">Biological invasions are widely recognized as a significant component of human-caused global environmental change&#44; often resulting in the loss of biological diversity and ecosystem function &#40;<a class="elsevierStyleCrossRef" href="#bib0040">Hulme&#44; 2003</a>&#41;&#46; The greenhouse frog <span class="elsevierStyleItalic">Eleutherodactylus planirostris</span> has direct development &#40;no aquatic stage&#41; and deposits its eggs in moist soil&#44; which facilitate human-mediated colonization &#40;<a class="elsevierStyleCrossRef" href="#bib0020">Christy et al&#46;&#44; 2007</a>&#41; through transportation in potted plants &#40;e&#46;g&#46; <a class="elsevierStyleCrossRef" href="#bib0050">Kraus et al&#46;&#44; 1999</a>&#59; <a class="elsevierStyleCrossRef" href="#bib0055">Kraus and Campbell&#44; 2002</a>&#41;&#46;</p><p id="par0010" class="elsevierStylePara elsevierViewall">The greenhouse frog is native to the Caribbean islands of Cuba&#44; Bahamas and Cayman Islands &#40;<a class="elsevierStyleCrossRef" href="#bib0030">D&#237;az and C&#225;diz&#44; 2008</a>&#59; <a class="elsevierStyleCrossRef" href="#bib0090">Olson et al&#46;&#44; 2012a</a>&#41;&#44; but it has a wide non-native distribution in the United States&#44; Mexico&#44; Jamaica&#44; Grenada&#44; Caicos Islands&#44; the Miskito Cays of Nicaragua&#44; Honduras&#44; Panama City&#44; Panama&#44; and the Pacific islands of Hawaii and Guam &#40;<a class="elsevierStyleCrossRef" href="#bib0030">D&#237;az and C&#225;diz&#44; 2008</a>&#59; <a class="elsevierStyleCrossRef" href="#bib0080">McCrane et al&#46;&#44; 2008</a>&#59; <a class="elsevierStyleCrossRef" href="#bib0050">Kraus&#44; 2009</a>&#59; <a class="elsevierStyleCrossRef" href="#bib0035">Heinicke et al&#46;&#44; 2011</a>&#59; <a class="elsevierStyleCrossRef" href="#bib0025">Crawford et al&#46;&#44; 2011</a>&#59; <a class="elsevierStyleCrossRefs" href="#bib0090">Olson et al&#46;&#44; 2012a&#44; 2012b</a>&#41;&#46;</p><p id="par0015" class="elsevierStylePara elsevierViewall">Empirical observations indicate that the greenhouse frog is a highly successful invasive species &#40;<a class="elsevierStyleCrossRef" href="#bib0010">Bomford et al&#46;&#44; 2009</a>&#41;&#46; For instance&#44; after natural and human-assisted introductions occurred in the early 1900s in Florida USA&#44; the greenhouse frog is now found throughout the state&#46; It is suspected that human-assisted introductions often occur by hitch-hiking on commercial nursery plants &#40;<a class="elsevierStyleCrossRef" href="#bib0035">Heinicke et al&#46;&#44; 2011</a>&#59; <a class="elsevierStyleCrossRef" href="#bib0050">Kraus et al&#46;&#44; 1999</a>&#41; and probably this is the way the greenhouse frog arrived in Mexico&#46; Here&#44; we report the first record of <span class="elsevierStyleItalic">E&#46; planirostris</span> in the Mexican Caribbean confirmed by morphological and molecular data&#46;<a name="p651"></a></p><p id="par0020" class="elsevierStylePara elsevierViewall">On 19 November 2010 at 14&#58;00 h following a heavy rain&#44; 3 small frogs were collected &#40;field numbers JGV 303&#8211;305&#59; 16&#44; 20 and 21<span class="elsevierStyleHsp" style=""></span>mm snout-vent length &#91;SVL&#93;&#44; respectively&#41; around a swimming pool at a condominium built in 1993 in the urban zone of Playa del Carmen&#44; Quintana Roo&#44; Mexico&#44; 20&#176;37&#39; 52&#8221; N&#44; 87&#176;04&#39; 21&#8221; W &#40;<a class="elsevierStyleCrossRef" href="#fig0005">Fig&#46; 1</a>&#41;&#46; Living specimens were photographed &#40;<a class="elsevierStyleCrossRef" href="#fig0010">Fig&#46; 2</a>&#41;&#44; sacrificed and preserved in 96&#37; ethanol&#44; and then deposited in the herpetological collection of the Museo de Zoolog&#237;a Alfonso L&#46; Herrera of the Facultad de Ciencias&#44; Universidad Nacional Aut&#243;noma de M&#233;xico &#40;UNAM&#41; with catalogue numbers MZFC 27464&#8211;27466&#46;</p><elsevierMultimedia ident="fig0005"></elsevierMultimedia><elsevierMultimedia ident="fig0010"></elsevierMultimedia><p id="par0025" class="elsevierStylePara elsevierViewall">After the literature review of local amphibians&#44; photographic comparisons&#44; and use of taxonomic keys&#44; we identified the specimens as belonging to the genus <span class="elsevierStyleItalic">Eleutherodactylus</span>&#44; but based on information in <a class="elsevierStyleCrossRefs" href="#bib0070">Lee &#40;1996&#44; 2000&#41;</a>&#44; <a class="elsevierStyleCrossRef" href="#bib0015">Campbell &#40;1998&#41;</a>&#44; and <a class="elsevierStyleCrossRef" href="#bib0045">K&#246;hler &#40;2011&#41;</a> morphological features of the collected frogs were inconsistent with any of the 9 species native to the Yucat&#225;n Peninsula&#46; In order to identify our specimens to the species level&#44; we conducted a genetic analysis using sequences from the mitochondrial gen Cytochrome Oxidase Subunit I &#40;COI&#41; &#40;&#62;600<span class="elsevierStyleHsp" style=""></span>bp&#41;&#46; Tissue samples were obtained from each specimen by toe clipping&#46;</p><p id="par0030" class="elsevierStylePara elsevierViewall">Molecular protocols &#40;DNA extraction&#44; amplification and sequencing&#41; were conducted in the barcoding laboratory of El Colegio de la Frontera Sur &#40;ECOSUR&#41; following the Canadian Center of DNA Barcoding &#40;CCDB&#41; public protocols &#40;<a id="intr0005" class="elsevierStyleInterRef" href="http://www.dnabarcoding.ca">http&#58;&#47;&#47;www&#46;dnabarcoding&#46;ca</a>&#41;&#46; To corroborate and compare our genetic material&#44; we obtained 3 additional sequences of <span class="elsevierStyleItalic">E&#46; planirostris</span>&#44; including 2 from Panama and 1 from Cuba &#40;<a class="elsevierStyleCrossRef" href="#bib0025">Crawford et al&#46;&#44; 2011</a>&#41;&#44; and 6 sequences of other species of <span class="elsevierStyleItalic">Eleutherodactylus &#40;E&#46; glamyrus&#44; E&#46; eileenae&#44; E&#46; bartonsmithi&#44; E&#46; principalis&#44; E&#46; mariposa</span> and <span class="elsevierStyleItalic">E&#46; ronaldi</span>&#41; &#40;<a class="elsevierStyleCrossRef" href="#bib0105">Rodr&#237;guez et al&#46;&#44; 2010</a>&#41;&#44; all downloaded from the Barcode of Life Database &#40;<a id="intr0010" class="elsevierStyleInterRef" href="http://www.boldystems.org">www&#46;boldystems&#46;org</a>&#41;&#46; A neighbor-joining &#40;NJ&#41; tree was reconstructed with a<a name="p652"></a> sequence of <span class="elsevierStyleItalic">Leptodactylus fragilis</span> as an outgroup &#40;<a class="elsevierStyleCrossRef" href="#fig0015">Fig&#46; 3</a>&#41; using the software MEGA v&#46; 4 &#40;<a class="elsevierStyleCrossRef" href="#bib0115">Tamura et al&#46;&#44; 2007</a>&#41;&#46; Also&#44; intra and interspecific <span class="elsevierStyleItalic">p</span> distances were calculated&#46; Genetic sequences and metadata were deposited at Barcode of Life Data Systems &#40;<a class="elsevierStyleCrossRef" href="#bib0100">Ratnasingham and Hebert&#44; 2007</a>&#41; under project <span class="elsevierStyleItalic">Eleutherodactylus</span> from Mexican Caribbean &#8220;EMC&#46;&#8221;</p><elsevierMultimedia ident="fig0015"></elsevierMultimedia><p id="par0035" class="elsevierStylePara elsevierViewall">Morphological characters described by <a class="elsevierStyleCrossRef" href="#bib0030">D&#237;az and C&#225;diz &#40;2008&#41;</a> confirmed that our specimens belong to <span class="elsevierStyleItalic">E&#46; planirostris</span>&#58; a small frog&#44; up to 27&#46;3<span class="elsevierStyleHsp" style=""></span>mm SVL&#59; long and thin toes with tubercles in the inferior surface&#44; not webbed and small digital discs&#59; dorsum variable overlaid with granules and tubercles&#46; There are 2 basic colour patterns&#58; <span class="elsevierStyleItalic">1&#41;</span> a mottled tan and brown&#44; and <span class="elsevierStyleItalic">2&#41;</span> a mottled tan and brown&#44; with 2 yellow dorsolateral stripes extending from the eye along the length of the body &#40;<a class="elsevierStyleCrossRef" href="#bib0075">Lynn and Grant&#44; 1940</a>&#41;&#46; The specimens we collected had the mottled tan and brown pattern &#40;<a class="elsevierStyleCrossRef" href="#fig0010">Fig&#46; 2</a>&#41;&#46; This identification was confirmed with the intra and interspecific genetic <span class="elsevierStyleItalic">p</span> distances &#40;1&#46;4&#37;&#44; and 25&#46;51&#37; average value&#44; respectively&#41;&#46;</p><p id="par0040" class="elsevierStylePara elsevierViewall">Clusters formed in our phenogram&#44; indicate that the 3 specimens from Mexico belong to <span class="elsevierStyleItalic">E&#46; planisrostris</span> and consist of 3 different haplotypes &#40;Mexico&#44; Panama and Cuba&#41;&#46; Both results &#40;morphological and genetic&#41; confirm for the first time the presence of the greenhouse frog in the state of Quintana Roo&#46;</p><p id="par0045" class="elsevierStylePara elsevierViewall">According to <a class="elsevierStyleCrossRef" href="#bib0060">Kraus et al&#46; &#40;1999&#41;</a>&#44; in Hawaii <span class="elsevierStyleItalic">E&#46; planirostris</span> potentially could eat indigenous&#44; endemic arthropods&#44; including species of insects and spiders of conservation concern&#46; In a recent study in Hawaii&#44; <a class="elsevierStyleCrossRef" href="#bib0085">Olson and Beard &#40;2012&#41;</a> found that this frog feeds mostly on leaf litter invertebrates&#44; and consumption was estimated be as great as 129&#44;000 invertebrates ha&#47;night&#46; Despite these possible ecological impacts&#44; the impacts of the greenhouse frog invasions remain largely unstudied &#40;<a class="elsevierStyleCrossRef" href="#bib0090">Olson et al&#46;&#44; 2012a</a>&#41;&#46;</p><p id="par0050" class="elsevierStylePara elsevierViewall">Ecological studies are therefore urgently needed to understand the effects of the greenhouse frog invasions&#46; In Mexico <span class="elsevierStyleItalic">E&#46; planirostris</span> was first reported in the state of Veracruz &#40;<a class="elsevierStyleCrossRef" href="#bib0110">Schwartz 1974</a>&#41;&#44; but subsequent records have not been forthcoming &#40;<a class="elsevierStyleCrossRef" href="#bib0005">&#225;lvarez-Romero et al&#46;&#44; 2008</a>&#41;&#46; In the case reported herein&#44; after a heavy rain&#44; on 18 June 2011 at 9&#58;00 h&#44; we collected another specimen &#40;25<span class="elsevierStyleHsp" style=""></span>mm SVL&#59; voucher deposited in the herpetological collection of the Museo de Zoolog&#237;a in ECOSUR campus Chetumal&#44; Cat&#46; Number ECO-CH 2949&#41; in the facilities of the Xaman Ha Aviary&#44; 20&#176;37&#39;6&#8221; N&#44; 87&#176;04&#39;50&#8221; W &#40;site 2&#59; <a class="elsevierStyleCrossRef" href="#fig0005">Fig&#46; 1</a>&#41;&#44; located ca&#46; 1650 m SW from the previous site&#44; confirming the distribution of <span class="elsevierStyleItalic">E&#46; planirostris</span> could be more widespread than previously thought&#46; Furthermore&#44; at the previous site we observed more adults &#40;including calling males&#41; and juveniles &#40;only mottled individuals were found in both sites&#41; in June 2013&#46; This indicates an established population of <span class="elsevierStyleItalic">E&#46; planirostris</span> now occurs in Playa del Carmen&#44; which could be present over a wider area&#44; and could spread beyond the urban zone in a short period of time&#46; To address this concern&#44; we strongly recommend that additional research be conducted to evaluate this invasion and its possible ecological impacts&#44; and determine if control measures are necessary&#46;</p><p id="par0055" class="elsevierStylePara elsevierViewall">Sometimes invasive species are difficult to identify using only traditional morphology&#44; and reference material for comparison often does not exist&#46; For this reason&#44; we suggest application of integrative taxonomy that includes<a name="p653"></a> morphological and molecular characters to correctly identify species as in this case&#46;</p><p id="par0060" class="elsevierStylePara elsevierViewall">We thank Samuel Pech Ram&#237;rez for his help finding frogs&#44; Humberto Bahena-Basave for the images&#44; and Janneth A&#46; Padilla Sald&#237;var for constructing the map&#46; We also thank Steven G&#46; Platt&#44; Larry D&#46; Wilson&#44; Karen H&#46; Beard&#44; and Fred Kraus for comments on the manuscript&#46;</p></span>"
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        "titulo" => "Abstract"
        "resumen" => "<p id="spar0020" class="elsevierStyleSimplePara elsevierViewall">Based on morphological identification and a molecular analysis of specimens collected in the urban zone of Playa del Carmen in the state of Quintana Roo&#44; we report the first record of the invasive greenhouse frog &#40;<span class="elsevierStyleItalic">Eleutherodactylus planirostris</span>&#41; in the Mexican Caribbean&#46; The presence of <span class="elsevierStyleItalic">E&#46; planirostris</span> in the Yucat&#225;n Peninsula suggests an urgent need for research to evaluate its invasion and ecological impacts&#46;</p>"
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        "resumen" => "<p id="spar0025" class="elsevierStyleSimplePara elsevierViewall">Con base en identificaci&#243;n morfol&#243;gica y an&#225;lisis molecular de ejemplares recolectados en la zona urbana de la ciudad de Playa del Carmen&#44; Quintana Roo&#44; informamos del primer registro de la rana de invernadero &#40;<span class="elsevierStyleItalic">Eleutherodactylus planirostris</span>&#41; en el Caribe mexicano&#46; La presencia de <span class="elsevierStyleItalic">E&#46; planirostris</span> en la pen&#237;nsula de Yucat&#225;n sugiere la necesidad de realizar urgentemente una investigaci&#243;n para evaluar su invasi&#243;n y los posibles impactos ecol&#243;gicos que puedan suscitarse&#46;</p>"
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          "en" => "<p id="spar0005" class="elsevierStyleSimplePara elsevierViewall">Collecting sites of <span class="elsevierStyleItalic">E&#46; planirostris</span> in the urban zone of Playa del Carmen&#44; Mexico&#46;</p>"
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          "en" => "<p id="spar0010" class="elsevierStyleSimplePara elsevierViewall">The greenhouse frog&#44; <span class="elsevierStyleItalic">Eleutherodactylus planirostris</span>&#46; Specimens found in Playa del Carmen&#44; Quintana Roo&#44; Mexico&#46; Vouchers MZFC 27464-66 &#40;up to down order&#41;&#46; Photos by H&#46; Bahena-Basave&#46;</p>"
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ISSN: 18703453
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