An Old World Skink, Chalcides ocellatus, with a Long History of

ARTICLES
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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
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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