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African clawed frog (Xenopus laevis) in Baja California: a confirmed population and possible ongoing invasion in Mexican watersheds.

The African clawed frog (Xenopus laevis) is a smooth-skinned frog with a flattened body, small head, blunt snout, and small upturned eyes with no lids (Stebbins, 2003; Dodd, 2013). This frog is well known as a model organism in laboratories for ecotoxicological studies and cellular, molecular, and developmental biology and has long been the most widely used amphibian in research (Gurdon, 1996; Measey et al., 2012; Dodd, 2013). Research and pet trade activities have been the main causes of the spread of X. laevis worldwide (Gurdon and Hopwood, 2000; Dodd, 2013). Along with the American bullfrog (Lithobates catesbeianus) and cane toad (Rhinella marina), the African clawed frog is probably one of the most invasive amphibians, and has the greatest worldwide nonindigenous distribution (Kraus, 2009; Measey et al., 2012). its fecundity and physiological adaptations allow it to colonize different types of water bodies, resulting in its success, particularly in Mediterranean climatic regions (Tinsley and McCoid, 1996; Lobos and Measey, 2002; Lillo et al., 2011; Measey et al., 2012). Populations or individuals have been reported in Germany, the Netherlands, France, Spain, Portugal, Italy, United Kingdom, Japan, Indonesia, Ascension Island, Israel, Sweden, United States, Chile, and Mexico (Kraus, 2009; Measey et al., 2012). Within its native range in southern Africa, this species rapidly invades human-made water bodies and anthropogenically disturbed areas, aided by its high adaptability and high reproductive success. it can reproduce in massive numbers in favorable habitats ([congruent to]0.25 individuals [m.sup.-2]; McCoid and Fritts, 1993; Lobos and Measey, 2002; Dodd, 2013). In Mexico, researchers have documented X. laevis only in the state of Baja California (Fig. 1), dispersing from nearby California, USA (Stebbins, 2003), although its current status has been questioned (Measey et al., 2012). The first record was an observation on the Tijuana River (Murphy, 1983; Flores-Villela, 1993; Tinsley and McCoid, 1996). Mahrdt et al. (2003) observed an adult from Rio Las Palmas in Cafion El Alamo. It was not until 2012 that Ruiz-Campos and Valdez-Villavicencio collected the first voucher specimen at Cantamar, Baja California (Ruiz-Campos and Valdez-Villavicencio, 2012).

In May 2013, we discovered a population of the African clawed frog at Puente El Morro, Canada El Morro, (32[degrees] 15.74'N, 116[degrees] 59.418'W; elevation 5 m) in the municipality of Rosarito (Fig. 1). The site is located about 7.5 km northwest of the nearest record at Cantamar (Ruiz-Campos and Valdez-Villavicencio, 2012). Canada el Morro is a small watershed with intermittent drainage and water flowing only in winter. However, a small pond located 115 m from the seashore persists year-round. We found several individuals on this small pond of 48 [m.sup.2] (12 x 6 m), which is surrounded by California bulrush (Schoenoplectus californiens) and southern cattail (Typha dominguensis) below the bridge (Puente El Morro) on Highway 1D. Several days later, we revisited the site and placed three unbaited minnow traps in the pond for 1 h. We measured the captured specimens for snout-vent length and weight, using precision calipers (mm) and a digital balance ([+ or -] 0.1 g). Individual age class was assigned based on snout-vent length, where juveniles are <65 mm (Alvarez-Romero et al., 2005). We assigned sex based on protruding labial lobes in females. Nine specimens were deposited in the herpetological collections at Universidad Autonoma de Baja California (UABC 2062-2065) in Ensenada and Centro de Investigaciones Biologicas del Noroeste (CIBNOR 1501-1505) in La Paz, Baja California Sur. We recorded water temperature, pH, conductivity, total dissolved solids, and salinity using a multiparameter tester (model 35, Eutech/Oakton Instruments, Vernon Hills, IL) and dissolved oxygen with a dissolved oxygen meter (YSI model 55, YSI Inc., Yellow Springs, OH).

We captured 106 individuals during 1 h of trapping (1810-1915h). We identified these as 33 females, 47 males, and 26 juveniles. Snout-vent length measurements are listed in Table 1. We did not see tadpoles or evidence of reproductive activity, i.e., mating calls or sexual characters (nuptial pads on males and prominent labia on the cloaca of females). The pond was 2 m deep, with turbid water and aquatic vegetation. Parameters of the water were 22.5[degrees]C, 6.5 pH, conductivity of 1,791 mS [cm.sup.-1], 1.27 ppt dissolved solids, 954 ppm salinity, and 82.6 mg [L.sup.-1] dissolved oxygen. We did not find native amphibians at the site, such as the western toad (Anaxyrus boreas) or the California tree frog (Pseudacris cadaverina), nor did we find the Baja California tree frog Pseudacris hypochondriaca, which is very common in other watersheds and stagnant pools in northwestern Baja California (pers. observ. of the authors). We took skin swabs from 10 individuals for future detection of the fungus Batrachochytrium dendrobatidis.

The X. laevis population at El Morro pond has larger snout-vent lengths and body masses than those found in native populations, the latter of which measure 53-63 mm and 17-29 g in males and 66-72 mm and 35-45 g in females (Du Preez et al., 2005). This indicates that pond conditions were favorable for the species, allowing them to grow larger individuals than indigenous populations. Xenopus reproductive activity is usually linked to the rainy season and food resources, but under favorable conditions, females and males show sexual characters all year (Lobos and Measey, 2002; Dodd, 2013). Despite the apparent suitable pond conditions and large population, we did not see any males with sexual characters present, hear mating calls, or see eggs or tadpoles in or near the pond. Cannibalism is known to occur in introduced populations in California, especially when available prey base is depleted (McCoid and Fritts, 1993), and might explain the lack of eggs and tadpoles. Based on the range in length and body mass (44-103 mm, 12.5-133.8 g), this population has been reproducing for more than 1 y, since it takes males 2-4 y to reach 80 mm and females about 5 y to reach 119 mm (McCoid and Fritts, 1989, 1993).

Xenopus laevis are able to migrate long distances in search of available habitat, especially through irrigation channels (Lobos and Jaksic, 2005; Lobos et al., 2013). If they have been established in this pond for several years, they might have dispersed to other localities, perhaps including those previously recorded at Cantamar (Ruiz-Campos and Valdez-Villavicencio, 2012), which is [congruent to]7.5 km south of El Morro. At this earlier site, only one individual was captured after setting six traps for 18 h. Migration rates of introduced X. laevis in Chile are 3.1-5.4 km [y.sup.-1] , with overland migrations without water (Lobos and Jaksic, 2005). However, we cannot discount the possibility that the specimen at Cantamar was a pet escape or release from a nearby condominium complex.

Introductions of exotic species are known to cause severe negative effects on biodiversity, promote ecosystem instability, and cause declines of native amphibian populations (Simberloff, 2005; Lillo et al., 2011). Native species were absent from this pond, including the most common species in the region (P. hypochondriaca). Perhaps X. laevis displaced the native species that used the pond as a reproduction or foraging site. Xenopus also has been proposed to be the origin of the spread of the fungus B. dendrobatidis, which is implicated in the worldwide decline of amphibian populations (Weldon et al., 2004; Vredenburg et al., 2013) and is known to carry a wide variety of diseases and parasites (Tinsley et al., 2012; Dodd, 2013). Currently, there is no record of B. denrobatidis in Baja California (Frias-Alvarez et al., 2008); however, there has not been a thorough study of its presence in Baja California amphibians. Few studies provide details of the impact of X. laevis on host ecosystems, particularly local populations of amphibians, and more empirical data are required (Fouquet and Measey, 2006; Dodd, 2013).

The confirmation of an established population of Xenopus in Mexico should be considered a serious concern for the conservation of native amphibians. This pond is located within one of Mexico's Terrestrial Conservation Priority Zones (Arriaga et al., 2000); these areas have unique biodiversity and high rates of plant endemism. Instituto Mexicano de Tecnologia del Agua et al. (2007) included X. laevis in the list of high-risk exotic species without verified presence in Mexico that require preventative actions. The population at El Morro in this section of the state of Baja California might represent a dispersion point to other sites, based on the high suitability for the expansion of this invasive species thoroughout the Mediterranean climatic region in Baja California (Measey et al., 2012). This reflects the need for conservation actions to prevent its dispersal and to promote eradication plans, especially in this small and easily accessible locality.

We thank I. Fogel of Centro de Investigaciones Biologicas del Noroeste for editorial services. L. A. Somma, N. Ford and one anonymous reviewer made valuable comments and suggestions on the manuscript. Financial support for the project was provided by the JiJi Foundation. A. Peralta-Garcia. is a recipient of a doctoral fellowship from Consejo Nacional de Ciencia y Tecnologia (CVU 221150). Collecting permits where issued by the Secretaria de Medio Ambiente y Recursos Naturales to P. Galina-Tessaro (SGPA/DGVS/01458/13).

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Submitted 7 December 2013.

Acceptance recommended by Associate Editor, NeilB. Ford, 24 July 2014.

Anny Peralta-Garcia, * Jorge H. Valdez-Villavicencio, and Patricia Galina-Tessaro

Centro de Investigaciones Biologicas del Noroeste, La Paz, Baja California Sur 23096, Mexico (APG, PGT)

Conservacion de Fauna del Noroeste, La Paz, Baja California Sur 23205, Mexico (JHVV)

* Correspondent: annyperaltagarcia@yahoo.com.mx

Table 1--Measurements of captured individuals of Xenopus laevis in
El Morro, Baja California, Mexico, in May 2013.

Age and sex     n              SVL (mm)

                      Mean [+ or -] SD     Range

Juveniles       26   51.8 [+ or -] 6.49    44-64
Adult females   33   78.1 [+ or -] 10.32   66-103
Adult males     47   61.9 [+ or -] 6.09    51-84

Age and sex                 Mass (g)

                 Mean [+ or -] SD       Range

Juveniles       19.9 [+ or -] 6.35    12.5-34.3
Adult females   52.7 [+ or -] 21.03   32.9-133.8
Adult males     31.6 [+ or -] 6.52    18.7-57
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Author:Peralta-Garcia, Anny; Valdez-Villavicencio, Jorge H.; Galina-Tessaro, Patricia
Publication:Southwestern Naturalist
Article Type:Report
Geographic Code:1MEX
Date:Sep 1, 2014
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