An Old World Skink, Chalcides ocellatus, with a Long History of
Transcription
An Old World Skink, Chalcides ocellatus, with a Long History of
ARTICLES 551 Herpetological Review, 2012, 43(4), xxx–xxx. © 2012 by Society for the Study of Amphibians and Reptiles An Old World Skink, Chalcides ocellatus, with a Long History of Anthropogenically Assisted Dispersal, Now Established in Mesa, Arizona, USA The Ocellated Skink, Chalcides ocellatus, is native to northern Africa, the Middle East and the Mediterranean (Pasteur 1981; Schleich et al. 1996). It occurs in a diverse array of habitats including: “…sand and gravel deserts, agricultural lands, gardens, and piles of refuse along the Mediterranean coast…” (Attum et al 2007). Using genetic analyses, Kornilios et al. (2010) argued that this lizard has colonized islands throughout the central and eastern Mediterranean in part due to anthropogenic assistance over the past three thousand years. Caputo et al. (1997) suggested that populations of C. ocellatus in southern Italy and nearby islands (Sicily, Sardinia), as well as its discontinuous range across Greece and various islands of the Aegean Sea, are best explained by a long history of colonization via anthropogenic facilitation. More recently, Kraus (2009) documented that C. ocellatus has been introduced to France and Great Britain, and established in Italy. With respect to the New World, Krysko et al. (2011) documented its presence in Broward and Pasco counties, Florida, USA. They found that a local reptile dealer in Mirimar, Florida, purchased C. ocellatus collected from local areas for resale in the pet trade (Krysko et al. 2011). It appears that C. ocellatus, like a number of squamates (e.g., gekkonids, lacertids, and iguanids), has expanded its range due in part to its ability to thrive in close proximity to humans and their habitations in relatively warm regions on several continents. Here we report on an established, actively reproducing population of C. ocellatus in a suburban area located in the arid Sonoran Desert Biome, near Phoenix, Arizona, USA. Kornilios et al. (2010) argued that, as a relatively generalized omnivore with ovoviviparous reproduction, C. ocellatus is a good candidate for colonization following transportation in soil with plants, or via other means associated with human activities. Attum et al. (2007) suggested that with respect to morphology, C. ocellatus is a generalized skink in comparison to relatives specialized for sandy habitats, and unlike its sand-dwelling relatives, typically escapes to vegetation in response to the approach of predators. Though a number of the recently established populations of C. ocellatus have been documented in relatively mesic environments, with ample vegetation associated with anthropogenically altered habitats (e.g., Caputo et al. 1997; Krysko et al. 2011), they have not been documented in arid regions of the New World. Given its occurrence in relatively arid habitats in the Old World, and propensity to colonize anthropogenically impacted landscapes, the success of C. ocellatus in the southwestern USA is potentially of great interest. One of us (JG) first observed C. ocellatus in a relatively high density housing area of Mesa, Maricopa Co., Arizona, USA (111.852°W, 33.361°N; NAD 1927), in 2007; in 2011, another of the authors (RB), independently discovered individuals (Fig. 1) in the same neighborhood, and began to canvass the area to determine the extent of the distribution. The results we present here are of two kinds: data on individual skinks collected by one of the authors during 2011 and early 2012, and reports on skinks by residents in the neighborhood in response to either door to door interviews or “information wanted flyers” distributed in the fall of 2011. Person to person interview validity during door to door surveys and in follow-up interviews with residents that responded to flyers was established by only recording those observations in which the occupant was familiar with lizards in general, and had lived in the residence for a minimum of one year, or recognized C. ocellatus from a photograph. During interviews, several residents volunteered “oh, those skinks” before they were even provided the photograph of the lizard (no other skinks occur within ~ 50 km of Mesa; Brennan and Holycross 2006). Canvassing of the neighborhood revealed that two different residents were confident they first observed C. ocellatus during 2001 (both within 0.5 km of the 2007 observation of JG). Residents reported C. ocellatus from potted plants, block walls, larger planters, and shrubbery, but also from comparatively barren micro-sites, such as the interiors of garages and storerooms. In sum, 18 different residents spread across an area of ~ 30 ha reported the presence of one or more individuals of one or more size classes over the past decade (Fig. 2). During 2011–2012, we collected a total of 20 individuals within roughly 15 ha of the same general area, which ranged in size from 68 to 118 mm SVL (mean ± SE: 91.0 ± 3.21 mm), with an apparent bimodal size class distribution (most individuals were ~ 85 or 115 mm SVL; total length ~160–230 mm). This mean SVL is at the upper end of that documented for a number of Old World populations of C. ocellatus (mean = 79–94 mm for six samples; see review in Greenbaum et al. 2006). It is important to note that these individuals were collected during a particularly dry fall and winter, prior to the onset of warm temperatures and presumably higher levels of activity. The cumulative distribution of sightings and collected individuals yields an area of occupation of ~ 30 ha. Because two size classes have been observed over more than ten years, including many sub-adults (not represented in the size data above; lizards ~ 50 SVL were often observed, but escaped capture), it is clear that reproduction is occurring locally, and thus a “stage 3” level introduction (Emerton and Howard 2008) has been attained for this species in Arizona: a naturalized population is established, and capable of spreading in the immediate area without JOHN GUNN 857 W. Portobello Ave, Mesa, Arizona 85210, USA ROBERT W. BOWKER Biology Department, Glendale Community College, Glendale, Arizona 85302, USA KEITH O. SULLIVAN School of Mathematical and Natural Sciences, P.O. Box 37100, Arizona State University, Phoenix, Arizona 85069, USA BRIAN K. SULLIVAN* School of Mathematical and Natural Sciences, P.O. Box 37100, Arizona State University, Phoenix, Arizona 85069, USA *Corresponding author; e-mail: [email protected] Herpetological Review 43(4), 2012 552 ARTICLES Fig. 1. Ocellated skink (Chalcides ocellatus) from Mesa, Arizona; SVL = 125 and 95 mm. Our observations highlight the establishment of C. ocellatus in a relatively mesic island of urban habitat surrounded by the xeric Sonoran Desert in Arizona. It is noteworthy that the only widespread lizards inhabiting urban areas of the Sonoran Desert are arboreal or scansorial (Urosaurus ornatus and Hemidactylus turcicus), which may be less susceptible to predation by house cats; C. ocellatus represents the only relatively large, ground-dwelling saurian in this urbanized environment. The notion that biological communities can be negatively impacted by the successful colonization of exotic species is a widely held tenet of conservation biology, though the costs and the benefits of removing exotics is open to debate (see reviews in Davis et al. 2011 and Simberloff 2011). While any introduced species warrants monitoring, understanding the means by which exotic organisms become introduced and established in novel communities, including the timeline during the early stages of establishment, should be afforded careful consideration. Acknowledgments.—We thank George Bradley, Petros Lymberakis, and Panagiotis Kornilios for their assistance and support; definitive identification of specimens from Mesa was provided by P. Kornilios. This work was conducted under IACUC approval (BKS) and with support of the Arizona Game and Fish Department (scientific collecting permits to BKS). We thank the many residents of Mesa that assisted with our observations, allowed access to their yards, and facilitated our research efforts; thanks as well to Tom Jones, Rob Lovich, and an anonymous reviewer for comments on the manuscript. A specimen has been accessioned in UA herpetology collection (UAZ 57401), and BKS # 2046-2049 are awaiting accession in the ASU Vertebrate Collection. Literature Cited Fig. 2. Upper panel shows aerial view of the approximate distribution for Chalcides ocellatus in a residential area of Mesa, Arizona; W Pecos Drive is roughly the center of 30 ha occupied by skinks. Solid circles-specimens collected; open circles-flier/interview responses only (used by permission GoogleEarth©). The lower panels show outlines of the USA and Mesa, Arizona, and a ground level view of W Pecos Drive, from left to right. assistance. Although assessment of size estimates by residents is potentially problematic, at least two residents reported having seen much larger individuals (~ 250 mm TL, the upper end of the size distribution of C. ocellatus; Mateo et al. 1995). Given their popularity in the pet trade, perhaps the simplest explanation for this colonization by C. ocellatus is the result of herpetocultural exchange including accidental or intentional release. If C. ocellatus arrived, as they reportedly did in Naples (Caputo 1997) via ornamental vegetation nursery stock, they may be arriving intermittently, or transported elsewhere via landscape management practices including debris removal from resident yards in the area of establishment. In addition to the landscape management assisted transport scenario described above, as area residents move, C. ocellatus will also have the opportunity to relocate via ornamental vegetation nursery stock, storage boxes, and other items. Chalcides ocellatus is the third saurian to become established in Arizona (Ctenosaura macrolopha and Hemidactylus turcicus; Brennan and Holycross 2006). Attum, O., P. Eason, and G. Cobbs. 2007. Morphology, niche segregation, and escape tactics in a sand dune lizard community. J. Arid Environ. 68:564–573. Brennan, T. C., and A. T. Holycross. 2006. A Field Guide to Amphibians and Reptiles in Arizona. Arizona Game and Fish Department, Phoenix, Arizona. 150 pp. Caputo, V., F. M. Guarino, and F. Baldanza. 1997. A new finding of the skink, Chalcides ocellatus in the ex Royal Garden of Portici (Naples, Italy). Bol. Asoc. Herpetol. Esp. 8:3–4. Davis, M. A., M. K. Chew, R. J. Hobbs, A. E. Lugo, J. J. Ewel, G. J. Vermeij, J. H. Brown, M. L. Rosenzweig, M. R. Gardener, S. P. Carrol, K. Thompson, S. T. A. Pickett, J. C. Stromberg, P. del Tredici, K. N. Suding, J. G. Ehrenfeld, J. P. Grime, J. Mascaro, and J. C. Biggs. 2011. Don’t judge species on their origins. Nature 474:153–154. Emerton, L., and G. Howard. 2008. A Toolkit for the Economic Analysis of Invasive Species. Global Invasive Species Programme, Nairobi, Kenya. 110 pp. Greenbaum, E., A. C. Campbell, and C. J. Raxworthy. 2006. A revision of sub-Saharan Chalcides (Squamata: Scincidae), with redescriptions of two east African species. Herpetologica 62:71–89. Kornilios, P., P. Kyriazi, N. Poulakakis, Y. Kumlutas, C. Ilgaz, M. Mylonas, and P. Lymberakis. 2010. Phylogeography of the ocellated skink Chalcides ocellatus (Squamata, Scincidae), with the use of mtDNA sequences: a hitch-hiker’s guide to the Mediterranean. Mol. Phyl. Evol. 54:445–456. Kraus, F. 2009. Alien Reptiles and Amphibians: a Scientific Compendium and Analysis. Springer, Dordrecht, Netherlands. 563 pp. Krysko, K. L., J. P. Burgess, M. R Rochford, C. R. Gillette, D. Cueva, K. M. Enge, L. A. Somma, J. L. Stabile, D. C. Smith, J. A. Wasilewski, G. N. Kieckhefer III, M. C. Granatrosky, and S. V. Nielsen. 2011. Verified non-indigenous amphibians and reptiles in Florida from 1863 through 2010: outlining the invasion process and identifying invasion pathways and stages. Zootaxa 3028:1–64. Herpetological Review 43(4), 2012 ARTICLES Mateo, J. A., P. Geniez, and J. Bons. 1995. Saurians of the genus Chalcides Laurenti 1768 (Reptilia, Scincidae) in Morocco, I: Review and distribution. Rev. Esp. Herpetol. 9:7–36. Pasteur, G. 1981. A survey of the species groups of the Old World scincid genus Chalcides. J. Herpetol. 15:1–16. 553 Schleich, H. H., W. Kastle, and K. Kablisch. 1996. Amphibians and Reptiles of North Africa: Biology, Systematics, Field Guide. Koeltz Scientific Books, Keonigstein, Germany. 630 pp. Simberloff, D. 2011. Non-natives: 141 scientists object. Nature 475:36. Herpetological Review, 2012, 43(4), xxx–xxx. © 2012 by Society for the Study of Amphibians and Reptiles Northwestern Salamanders (Ambystoma gracile) in Mountain Lakes: Record Oviposition Depths Among Salamanders Oviposition timing, behaviors, and microhabitats of ambystomatid salamanders vary considerably (Egan and Paton 2004; Figiel and Semlitsch 1995; Howard and Wallace 1985; MacCracken 2007). Regardless of species, however, females typically oviposit using sites conducive to embryo development and survival. For example, the results of an experiment by Figiel and Semlitsch (1995) on Ambystoma opacum (Marbled Salamander) oviposition indicated that females actively selected sites that were under grass clumps in wet versus dry treatments, and surmised that environmental conditions such as humidity, moisture, and temperature contributed to their results. Other factors associated with ambystomatid oviposition and embryo survival include water temperature (Anderson 1972; Brown 1976), dissolved oxygen concentration (Petranka et al. 1982; Sacerdote and King 2009), oviposition depth (Dougherty et al. 2005; Egan and Paton 2004), and oviposition attachment structures such as woody vegetation (McCracken 2007; Nussbaum et al. 1983). Resetarits (1996), in creating a model of oviposition site selection for anuran amphibians, hypothesized that oviparous organisms were also capable of modifying oviposition behavior and site selection to accommodate varying habitat conditions and to minimize potential negative effects of environmental stressors. Kats and Sih (1992), investigating the oviposition of Ambystoma barbouri (Streamside Salamander) in pools of a Kentucky stream, found that females preferred pools without predatory Lepomis cyanellus (Green Sunfish), and that the number of egg masses present in a pool historically containing fish increased significantly the year after fish had been extirpated from the pool. Palen et al. (2005) determined that Ambystoma gracile (Northwestern Salamander) and Ambystoma macrodactylum (Longtoed Salamander) eggs were deposited either at increased depth or in full shaded habitats, respectively, as water transperancy to UV-B radiation increased. Ambystoma gracile is a Pacific Northwest (USA and Canada) species that breeds in permanent ponds and lakes from sea level to about 2000 m elevation (Corkran and Thoms 1996; Leonard et al. 1993; Richter 2005). Egg masses are usually affixed to stems of emergent–submergent vegetation or the branches of submerged woody debris. Reported depths for A. gracile egg mass oviposition range from just below the water surface to 2 m deep (Table 1). Here we describe A. gracile oviposition in a montane lake in Mount Rainier National Park (MORA), Washington, USA, which is substantially deeper than previous reports. Methods.––On 23–24 July 2003 and 12 July 2005, we surveyed 4 lakes at MORA for A. gracile egg masses (Table 1). A total of 276 egg masses were observed in the 4 lakes, all attached to branches of submerged fir and hemlock trees (Fig. 1). In 2003, Dick, Harry, and Sunrise Lakes were surveyed during daytime snorkel surveys, and depths from the lake surface to the top of each observed egg mass were measured using a meter tape. In 2005, Upper Palisades Lake (Fig. 2) was surveyed by two SCUBA divers, and egg mass depths were measured using a Suunto Favor Air Lux Dive Computer with depth gauge. During the period 1996–2004, 12 daytime and 2 nighttime shallow littoral snorkel surveys for locating A. gracile egg masses and larvae were also conducted in Upper Palisades Lake. Larvae were observed during these surveys but egg masses were not. Dick, Harry, and Sunrise Lakes have extensive and relatively shallow littoral zones which slope gradually to a flat bottom (maximum depths = 2.5, 4.2, and 7 m, respectively). The littoral zones contain abundant sunken logs and large woody debris, and some emergent–submergent vegetation. In 2003, the 3 lakes were fishless, although Harry and Sunrise Lakes were historically stocked with non-native salmonids (Harry = 3 times between 1926 to 1951; Sunrise = 21 times between 1926 to 1971; MORA, unpubl. stocking records). All fish were removed from Harry Lake using gill nets during the summers of 1996 through 1998, and the absence of fish from Sunrise Lake was determined during the same period by angling, using gill nets, and observation during snorkel surveys. Although Dick Lake was never stocked, gill nets were set in the lake in 1996 to determine the absence of fish and subsequent snorkel surveys were used to further document fish absence. Upper Palisades Lake has minimal littoral habitat primarily on a relatively shallow shelf (variable maximum depth = ~1–3 m) just beyond the mouth of a stream flowing into the lake, and the lake slopes steeply on all sides beyond the shelf to a maximum depth of 15.3 m (Fig. 2). There is no emergent–submergent vegetation in the littoral zone, and accumulations of large woody debris are present predominantly at depths >3m, due, in part, to the steeply sloping perimeter and bowl-shaped bathymetry of the lake (Fig. 2). Gill nets were used to remove Eastern Brook Trout (Salvelinus fontinalis) from Upper Palisades Lake in 1996. Subsequent gill netting efforts and snorkel surveys documented the continued absence of fish from the lake, which was fishless in 2005. The lake had previously been stocked 7 times between 1961 and 1971 (MORA, unpubl. stocking records). The A. gracile adults in Upper Palisades Lake are predominantly neotenes or gilled-adults. Frequency of this life-history stage increases with ROBERT L. HOFFMAN* CHRISTOPHER A. PEARL GARY L. LARSON US Geological Survey, Forest and Rangeland Ecosystem Science Center, 3200 SW Jefferson Way, Corvallis, Oregon 97331, USA BARBARA SAMORA Mount Rainier National Park, 55210-238th Ave East, Ashford, Washington 98304, USA * Corresponding author; e-mail: [email protected] Herpetological Review 43(4), 2012