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Herpetological Review 48(4), 2017 Herpetological Review, 2017, 48(4), 734–739. © 2017 by Society for the Study of Amphibians and Reptiles Distribution and Activity Season of the Introduced Red-Eared Slider (Trachemys scripta elegans) in Colorado, USA Red-eared Sliders (Trachemys scripta elegans) are native to the central and southeastern United States (Powell et al. 2016). To the west, the natural range of this species extends into New Mexico, Oklahoma, Kansas, and extreme southeastern Nebraska, especially along major river systems (Powell et al. 2016). A local- ity in Wallace County, Kansas, is the most northwesterly natural occurrence of Red-eared Sliders, and is only 2.5 km E of the Colo- rado border (Collins 2007). However, many extra-limital popu- lations of this species have become established, not only in the United States but around the world, earning this species a rank- ing of among the World’s 100 Worst Invasive Alien Species (Lowe et al. 2004; Powell et al. 2016). No native occurrences have been reported from Colorado. The first record in the state, a specimen with a label stating “Denver, Colo.” was included on a list com- piled by Ellis and Henderson (1913). Since that time, additional specimens have been reported from Boulder, Denver, Mesa, and Rio Blanco counties (Livo et al. 1998). Despite its proven ability to establish extra-limital populations, this species continues to be sold at pet stores in Colorado and is considered an unregulated species by the Colorado Department of Natural Resources, so it “may be imported, sold, bartered, traded, transferred, possessed, propagated and transported in Colorado provided that all impor- tation, disease requirements and any other state, local or federal requirements are met” (Colorado Parks and Wildlife 2016). The present report provides updated information about the distribu- tion of T. s. elegans in Colorado and documents its activity season in the state. State agencies can use this information to deter- mine whether the import and sale of Red-eared Sliders should be prohibited in an effort to eliminate the release of unwanted pets and reduce the establishment of extra-limital populations in Colorado. MATERIALS AND METHODS We made observations of turtles opportunistically in publically accessible sites, usually using binoculars and cameras equipped with telephoto capabilities; we did not deploy turtle LAUREN J. LIVO* 1835 S. Van Gordon Street, Lakewood, Colorado 80228, USA COLE WILD 266 Green Teal Drive, Loveland, Colorado 80537, USA TODD L. WILCOX 865 Santa Fe Drive, Unit A, Denver, Colorado 80204, USA BRYON SHIPLEY 9005 E. Lehigh Avenue #37, Denver, Colorado 80237, USA BRAD LAMBERT Colorado Natural Heritage Program, Colorado State University, Campus Delivery 1475, Fort Collins, Colorado 80523-1475, USA JOSEPH EHRENBERGER Adaptation Environmental Services, P.O. Box 6030, Denver, Colorado 80206, USA TIMOTHY WARFEL 12528 West Arizona Place, Lakewood, Colorado 80228, USA JENN LOGAN Colorado Parks and Wildlife, 0088 Wildlife Way, Glenwood Springs, Colorado 81601, USA *Corresponding author; e-mail: [email protected]

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carretero, M. a. 2012. Measuring body temperatures in small lac-ertids: infrared vs. contact thermometers. Basic Appl. Herpetol. 26:99–105.

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Herpetological Review, 2017, 48(4), 734–739.© 2017 by Society for the Study of Amphibians and Reptiles

Distribution and Activity Season of the Introduced Red-Eared Slider (Trachemys scripta elegans) in Colorado, USA

Red-eared Sliders (Trachemys scripta elegans) are native to the central and southeastern United States (Powell et al. 2016). To the west, the natural range of this species extends into New Mexico, Oklahoma, Kansas, and extreme southeastern Nebraska, especially along major river systems (Powell et al. 2016). A local-ity in Wallace County, Kansas, is the most northwesterly natural occurrence of Red-eared Sliders, and is only 2.5 km E of the Colo-rado border (Collins 2007). However, many extra-limital popu-

lations of this species have become established, not only in the United States but around the world, earning this species a rank-ing of among the World’s 100 Worst Invasive Alien Species (Lowe et al. 2004; Powell et al. 2016). No native occurrences have been reported from Colorado. The first record in the state, a specimen with a label stating “Denver, Colo.” was included on a list com-piled by Ellis and Henderson (1913). Since that time, additional specimens have been reported from Boulder, Denver, Mesa, and Rio Blanco counties (Livo et al. 1998). Despite its proven ability to establish extra-limital populations, this species continues to be sold at pet stores in Colorado and is considered an unregulated species by the Colorado Department of Natural Resources, so it “may be imported, sold, bartered, traded, transferred, possessed, propagated and transported in Colorado provided that all impor-tation, disease requirements and any other state, local or federal requirements are met” (Colorado Parks and Wildlife 2016). The present report provides updated information about the distribu-tion of T. s. elegans in Colorado and documents its activity season in the state. State agencies can use this information to deter-mine whether the import and sale of Red-eared Sliders should be prohibited in an effort to eliminate the release of unwanted pets and reduce the establishment of extra-limital populations in Colorado.

Materials and Methods

We made observations of turtles opportunistically in publically accessible sites, usually using binoculars and cameras equipped with telephoto capabilities; we did not deploy turtle

LAUREN J. LIVO*1835 S. Van Gordon Street, Lakewood, Colorado 80228, USACOLE WILD266 Green Teal Drive, Loveland, Colorado 80537, USATODD L. WILCOX865 Santa Fe Drive, Unit A, Denver, Colorado 80204, USABRYON SHIPLEY9005 E. Lehigh Avenue #37, Denver, Colorado 80237, USABRAD LAMBERTColorado Natural Heritage Program, Colorado State University, Campus Delivery 1475, Fort Collins, Colorado 80523-1475, USAJOSEPH EHRENBERGERAdaptation Environmental Services, P.O. Box 6030, Denver, Colorado 80206, USATIMOTHY WARFEL12528 West Arizona Place, Lakewood, Colorado 80228, USAJENN LOGANColorado Parks and Wildlife, 0088 Wildlife Way,Glenwood Springs, Colorado 81601, USA

*Corresponding author; e-mail: [email protected]

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traps. When possible, we documented our observations with photographs. We obtained coordinates either from GPS devices (Garmin GPSMap 60) or GoogleEarth. Selected voucher photos were submitted to the Ancillary Collection at the University of Colorado Museum of Natural History or are available for viewing on the websites Herpetological Education & Research Project (H.E.R.P.; www.naherp.com) and iNaturalist (www.inaturalist.org). Beginning in 2015, we devoted most of our effort specifically to finding new localities, but also conducted follow-up visits to several documented sites to determine whether the turtles were still present.

results

Distribution.—We found T. s. elegans at numerous ponds, lakes, and reservoirs throughout Colorado, with the majority of observations in urban and suburban parks in the Denver Metropolitan area (Figs. 1, 2). A list of occupied localities with geographic coordinates, dates of observation, and voucher information is available by request from the senior author.

Only eight of the 101 localities summarized here were documented before 2000 and 11 were reported between 2000 and 2014. Our search efforts documented ten new localities in

2015, 16 in 2016, and 56 in 2017. Occupied sites are managed by a variety of entities and included urban parks, an aquatic golf course, a university campus, a business park, botanic gardens, county open space, state parks, state wildlife areas, an urban national wildlife refuge, and a wastewater storage pond.

We did not detect T. s. elegans during visits to park ponds in numerous communities in Colorado, although the lack of detection does not preclude the presence of Red-eared Sliders in these cities and towns. Painted Turtles (Chrysemys picta), a native species, were present at some of the ponds where we did not detect Red-eared Sliders.

Very little natural habitat suitable for Red-eared Sliders exists in Colorado. Occupied impoundments were usually constructed as part of an irrigation network, for water storage and flood control, or as reclamation areas after gravel operations; these lakes and ponds are unevenly distributed across the state. Two sites, a schoolyard parking area and a cold-water river, clearly were unsuitable habitat for Red-eared Sliders; in these two instances, turtles were found by members of the public and brought to a Colorado Parks & Wildlife office (JL, pers. observ.). Although we frequently encountered a single individual in a given body of water, about half of the sites contained multiple individuals, with one site having at least 14 individuals by direct count.

Fig. 1. Statewide distribution of Trachemys scripta elegans in Colorado, including nearby records in adjacent states (status of these records is discussed in the text). See Fig. 2 for detail of distribution in the Denver metropolitan area.

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Activity Season.— Red-eared Sliders have been observed every month of the year except for December and January. Based on an observation in February, Livo et al. (1998) believed that Red-eared Sliders were capable of overwintering in Colorado. We observed basking Red-eared Sliders in the Denver metropolitan area as early as 4 February 2017 (UCM AC-211), with several additional February observations at various sites. We re-visited selected sites that had observations of Red-eared Sliders made prior to 2017 and found these turtles at 28 of 34 sites. Red-eared Sliders have been observed at Varsity Pond, Boulder County, from 1991 (Livo et al. 1998) through 2016. Other sites with multiple years of occupancy by T. s. elegans are indicated in Figs. 1 and 2. Evidence from continued occupation by multiple individuals at numerous sites, including observations at many localities as early in the year as February, indicates regular overwintering.

As expected, we observed basking behavior throughout the spring, summer, and early fall at occupied sites. During an unusually warm and dry fall, Red-eared Sliders were observed basking at several sites into November, including Main Reservoir, Stone House, and Cottonwood Park in Jefferson County and Jewell Wetland in Arapahoe County, although the number of individuals declined as the season progressed. The latest sighting in the year at a site known to be occupied by this species was 20 November 2016 at Stone House in Jefferson County. These observations document an activity season of nearly ten months.

discussion

Additional surveys for Red-eared Sliders are needed to obtain a more complete picture of the distribution outside of the Denver Metropolitan area. Most observations reported here represent introduced individuals, with gaps between eastern Colorado and the nearest natural populations in the same drainage regions of 220–800 km or more. (For information about the most recent delineations of drainages, see https://nhd.usgs.gov/ for the Watershed Boundary Dataset.) The nearest natural populations in Nebraska are located in the extreme southeastern corner of the state (Ballinger and Lynch 1999), although records of introduced turtles in Nebraska include localities as far west as Buffalo County, ca. 250 km E of Colorado (Bartels 2010; Fogell 2010; Hubbs 2013; Bridger et al. 2014; Hubbs 2016; USGS 2016).

One observation in southeastern Colorado from below Two Buttes Reservoir in northern Baca County (elevation 1284 m) may have been an introduced individual, although it is possible that it is a natural occurrence. Two Butte Creek, an intermittent stream, enters the Arkansas River near Holly, Colorado. Although Painted Turtles (Chrysemys picta) have been reported from the Two Buttes area, herpetological surveys had not previously documented T. s. elegans from southeastern Colorado (Mackessy 1998; Colorado Division of Wildlife 2001). Compared to other records in Colorado,

Fig. 2. Distribution of Trachemys scripta elegans in the Denver metropolitan area.

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there is less of a distribution gap (ca. 160 km) between this site (in HUC8 11020013) and the nearest T. s. elegans observations in the Middle Arkansas-Lake McKinney drainage area (HUC8 11030001) in Finney County, southwestern Kansas (Taggart 2007).

In comparison, the most northwesterly and apparently natural population of T. s. elegans occurs in Wallace County, western Kansas. Two preserved specimens collected in 1910 from Wallace County (no specific locality) were corroborated by the 2007 specimen of a Red-eared Slider in Willow Creek, Wallace County, at 1165 m elevation, less than 2.5 km from the eastern border of Colorado in the Smoky Hill River drainage (Collins 2007). This record is isolated from the nearest records, which are approximately 200 km to the east in Trego County in the Smoky Hill drainage and 140 km southeast in Finney County in the Arkansas River drainage (T. W. Taggart, pers. comm.). Although the recent record from Wallace County, Kansas, is in a different drainage than the record from Baca County, Colorado, as discussed below there is evidence that T. s. elegans may be expanding its natural range in areas adjacent to southeastern Colorado, and if natural populations are not already present in Colorado, this species may at some point enter the state.

The distribution map in a recent field guide illustrates T. s. elegans localities in extreme western Kansas near the Colorado border (Powell et al. 2016). Earlier surveys in southwestern Kansas failed to detect T. s. elegans in Finney and Morton counties (Taggart 2007; Collins et al. 2011). More recently in Kansas, Red-eared Sliders were documented in Finney County in 2006 (Taggart 2007), in Morton County in 2012 and 2014 (Hubbs 2013; Taggart 2014), and in Grant County near Ulysses by 1989 (T. W. Taggart, pers. comm.). Whether records from southwestern Kansas represent recently introduced animals or natural occupation from westward expansion is unclear. Natural westward expansion of T. s. elegans may have been encouraged through changes in agricultural practices, construction of habitats such as sand borrow pits adjacent to rivers, and recent changes in minimum streamflow requirements in the Arkansas River (T. W. Taggart, pers. comm.).

New Mexico is an unlikely source for natural populations in southeastern Colorado. The closest record from New Mexico is from Union County (Painter and Christman 2000) and may represent an introduced individual. The drainage in which the locality is found, Upper Beaver (HUC8 code 11100101) does not drain into Colorado.

Drainages that have records of T. s. elegans from adjacent states (Kansas and Oklahoma) where the drainages enter Colo-rado include the Upper Cimarron (HUC8 11040002), the North Fork Cimarron (HUC8 11040003), and Smoky Hill Headwaters (HUC8 10260001), all outlined in red in Fig. 1. The natural distri-bution of T. s. elegans appears to exclude populations of this spe-cies from the Oklahoma Panhandle (Sievert and Sievert 2011). A field trip of four herpetological societies to the Oklahoma Pan-handle and vicinity in 1979 with approximately 50 individuals re-sulted in no observations of Red-eared Sliders among the 27 spe-cies observed (Irwin 1979). However, surveys in 2005 and 2006 resulted in observations of T. s. elegans in the Black Mesa area of the Oklahoma panhandle, where this species was regarded as rare (Periard 2007). Peter Lindeman (pers. comm.) observed four T. s. elegans basking at Lake Carl Etling in Black Mesa State Park in 2015. It is unknown whether these turtles represent introduc-tions or a recent natural range expansion. Although currently there are no records in the Colorado reaches of Upper Cimarron, North Fork Cimarron, and Smoky Hill Headwaters drainages, fu-ture records in these areas might represent natural occurrences.

There is no direct evidence of successful reproduction by this species in Colorado. Small individuals (estimated to be <7 cm) have been observed at several sites (LJL, pers. observ.). These individuals were well under the carapace length of 10.2 cm (4 inches) specified for the legal sale of turtles in the U.S. (Food and Drug Administration 2016), a size limit put into effect to reduce transmission of salmonella to humans, particularly children (Harris et al. 2010). However, in the past few years, sporadic roadside sales of hatchlings have been reported in the local media for the Pueblo, Colorado Springs, and Denver metropolitan areas, so it is possible that observations of small individuals might be from releases of illegally sold animals rather than from feral reproduction.

Possible Effects and Policy Implications.—Introduced species can have several negative effects on native species and ecosystems. Some observed and potential deleterious effects from introduced Red-eared Sliders include the possibility of transmission of parasites and pathogens to native species as well as competition for basking sites, nesting sites, and other resources (Holland 1994; Cadi and Joly 2003, 2004; Lambert et al. 2013; Polo-Cavia et al. 2014; Meyer et al. 2015; Keenan and Tellez 2016). Pet stores that sell Red-eared Sliders, available at one store in Jefferson County at the time of this writing for $19.95, frequently house additional turtle species in the same tank, a practice that promotes parasite and disease transmission among the turtles.

Although most sites occupied by Red-eared Sliders in Colorado were urban or suburban, several localities also supported sympatric Chrysemys picta and Chelydra serpentina. Because of the similarity in basking habits, Painted Turtles are more likely to be negatively affected by behavioral interactions with the larger Red-eared Sliders than are Snapping Turtles. In some circumstances, Red-eared Sliders can occupy basking sites for seven hours or more (Selman and Qualls 2009), possibly precluding use of favorable sites by native turtles (Cadi and Joly 2003; Spinks et al. 2003; Cadi and Joly 2004; Drost et al. 2011).

Even as ownership of “specialty pets” including birds, fish, and reptiles has decreased in the United States, ownership of turtles has increased (American Veterinary Medical Association 2012). With changes of circumstances or interest, owners of pet turtles may elect to discard animals through release rather than finding new homes for them. Pet stores sometimes distribute ed-ucational material such as the PARC Don’t Turn It Loose brochure (http://www.parcplace.org/images/stories/pdfs/DontTurn.pdf). We observed signage posted at several of the sites occupied by Red-eared Sliders that specifically prohibits the release of ani-mals. These educational measures clearly are inadequate, given the growing presence of this invasive species in Colorado.

It is unknown whether summer soil temperatures are too low at present for successful reproduction of Red-eared Sliders in Colorado. Laboratory studies indicate that embryos of Chrysemys picta have higher survival rates than T. s. elegans when incubated at 23°C (Les et al. 2009). Winter soil temperatures may also limit overwinter survival in hatchling Red-eared Sliders (Packard et al. 1997). However, reproduction has been documented in introduced populations in northern sites such as Ontario, Canada, and Michigan (USGS 2016). To the extent that prevailing soil temperatures in Colorado may limit successful incubation of Red-eared Slider eggs and overwinter survival of hatchlings, warming associated with climate change may enhance the potential for reproductive success in feral populations of T. s. elegans if it does not already take place.

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Sliders (T. s. scripta and T. s. elegans) have a reported lifespan in nature of 30 or more years (Parker 1996; Thomas et al. 1997), and in captivity of more than 37 years (Snider and Bowler 1992). When one or more turtles are released into a habitat where they can survive long-term, an enduring population can be established and maintained even in the absence of reproduction.

Especially in urban areas, Red-eared Sliders can be more visible to people than native turtles. Kraus (2009) writes: “… alien species,…because of their frequent abundance, will often be unthinkingly accepted by most people as ‘normal,’ implicitly interpreted to mean ‘native.’” People often are unaware of the potential for alien species to negatively affect native species through competition and spread of parasites and pathogens. Consequently, programs to eliminate Red-eared Sliders from occupied localities may be met with resistance from the public (Kraus 2009).

Given the opportunistic nature of our observations, additional impoundments in Colorado may be occupied by Red-eared Sliders. Lack of regulation by state agencies, the growing popularity of turtles as pets, and lack of effective education for pet owners combine to ensure that Red-eared Sliders will continue to be introduced and to be a part of Colorado’s herpetofauna, especially in urban and suburban areas.

Acknowledgments.—T. Taggart and B. Hubbs provided informa-tion about T. s. elegans in Kansas, while K. Geluso answered ques-tions about this species in Nebraska. We thank E. Braker at the Uni-versity of Colorado Museum of Natural History for curating many of the photographic vouchers. A. Treble gave us permission to include sightings from the aquatic database for Colorado Parks and Wildlife. Because T. s. elegans is an unregulated species in Colorado and we did little or no handling of the turtles, we did not operate under a scientific collection permit.

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Herpetological Review, 2017, 48(4), 739–743.© 2017 by Society for the Study of Amphibians and Reptiles

New Records of Dero (Allodero) lutzi, an Oligochaete Parasite of the Urinary Tract of South American Anurans

There are currently six oligochaete species assigned to the subgenus Allodero (Clitellata: Naididae), which are found in the urinary tract (Wolffian ducts) and eyes of anurans (Gelder

1980; Pinder et al. 1998; Andrews et al. 2015). The nature of this association has been controversial in the literature. Some consider this to be a case of parasitism (Michaelson 1926a, 1926b; Lutz 1927), while others believe it is case of commensalism (Harman 1971; Pinder et al. 1998). These oligochaetes can use frogs as means of transport and as hosts (Lopez et al. 1999; Rodrigues and Maldonado Junior 1982; Righi 1984). Their life cycle was studied for the first time by Lutz (1927), who discovered a free-living stage, but the transition from parasitism to free living stage remained unknown (Andrews et al. 2015). More recently, Andrews et al. (2015) studied the life cycle of Dero (Allodero) hylae and claimed that these worms are parasites and can cause physical changes in the host. Studies have suggested that oligochaetes infect amphibians in the larval stage, but the transmission mode is still unknown (Harman and Lawler 1975).

Reports of this endoparasite species in South American frogs are scarce and limited to southeastern Brazilian in the Atlantic Forest (Michaelson 1926a; Rodrigues and Maldonado Junior 1982; Prado et al. 2003; Oda et al. 2015) and two records in the Amazonia Forest in Venezuela (Michaelson 1926a; Rodrigues and Maldonado Junior 1982). Tree frogs of the Hylidae (e.g., Dendropsophus spp. and Scinax spp.) seem to be the main hosts for this oligochaete (Michaelson 1926a; Rodrigues and Maldonado Junior 1982; Prado et al. 2003; Oda et al. 2015), although there is one record for Bufonidae (Rhinella ornata) (Rodrigues and Maldonado Junior 1982).

In this paper we report new occurrences of the oligochaete Dero (Allodero) lutzi infecting amphibians from three geographic regions and distinctive ecosystems in Brazil and therefore update the distributional map with new and published data for South America. We surveyed amphibians from three different regions in Brazil: 1) Midwest-Pantanal Wetland, in Corumbá municipality,

DRAUSIO HONORIO MORAIS*Universidade Federal Rural da Amazônia (UFRA), PA 275, Km 13, Zona Rural, CEP: 68.515-000, Parauapebas, Pará, BrazilALINE AGUIARUNESP – Univ. Estadual Paulista, Campus de Botucatu, Instituto de Biociências, Departamento de Parasitologia. Av. Bento Lopes, s/n, Rubião Júnior, Caixa Postal 510, CEP 18618-970, Botucatu, São Paulo, BrazilKARLA MAGALHÃES CAMPIÃODepartamento de Zoologia, Universidade Federal do Paraná, Curitiba, BrazilLUIZ EDUARDO ROLAND TAVARESDepartamento de Biologia, Universidade Federal de Mato Grosso do Sul, BrazilWALTÉCIO DE OLIVEIRA ALMEIDAUniversidade Regional do Cariri, Centro de Ciências Biológicas e da Saúde, Departamento de Química Biológica, Campus do Pimenta, Crato, CE, BrazilROBSON WALDEMAR ÁVILAUniversidade Regional do Cariri, Centro de Ciências Biológicas e da Saúde, Departamento de Química Biológica, Campus do Pimenta, Crato, CE, BrazilREINALDO JOSÉ DA SILVAUNESP – Univ. Estadual Paulista, Campus de Botucatu, Instituto de Biociências, Departamento de Parasitologia, Av. Bento Lopes, s/n, Rubião Júnior, Caixa Postal 510, CEP 18618-970, Botucatu, São Paulo, Brazil

* Corresponding author: [email protected]