Status of the Airlie Island Ctenotus, Ctenotus angusticeps (Lacertilia: Scincidae), with notes on distribution, habitat and genetic variation

2013·6.2 MB·

by  M O’Connell

STATUS OF THE AIRLIE ISLAND CTENOTUS,
CTENOTUS ANQUSTICEPS (LACERTILIA: SCINCIDAE),
WITH NOTES ON DISTRIBUTION, HABITAT
AND GENETIC VARIATION
By B. MARYAN1, R. SOMAWEERA1, R. LLOYD1,
M. BUNCE2 and M. O’CONNELL1
biologic Environmental Survey, 50B Angove Street,
North Perth WA 6006
2 Ancient DNA Laboratory, Murdoch University,
Perth WA 6150
ABSTRACT
The scincid lizard, Ctenotus angusticeps was previously only
known from a single island (Airlie Island) and two disjunct
mainland localities in Western Australia. As a result of its
restricted distribution and little documentation, it has for
some time been listed under both state and federal
legislation. Recent surveys have revealed additional
populations along the northwestern coast, which appear to
be highly restricted to specific habitats, primarily salt marsh
communities adjacent to mangroves where lizards shelter
down crab holes. Genetic analysis of mitochondrial DNA
shows very little variation between populations, suggesting
a single widespread population or recent radiation. In light
of this additional information the conservation status of C.
angusticeps is evaluated.
INTRODUCTION their species descriptions repre¬
senting the only source of
The scincid genus Ctenotus is
available information.
Australia’s most diverse with
currently 103 described species Ctenotus angusticeps was first
(Wilson and Swan 2013) dis¬ described by Storr (1988) from a
playing frequent sympatry and series collected during a
morphological similarity. As a biological survey on Airlie Island,
result, numerous studies on 35km NNE of Onslow on the
habitat separation and ecological northwestern coast of Western
interactions have been carried Australia (Figure 1). Presumably
out (e.g. Read 1998; James 1991; due to its restricted distribution
Sadlier 1987; Pianka 1986). How¬ on a small island (0.28km2) and
ever, for many species, published the comments made by Browne-
ecological data is minimal with Cooper and Maryan (1990)
103
Figure 1. Updated distribution map for Ctenotus angusticeps showing a very
discontinuous range along the northwestern coast of Western Australia due to
an association with a very specific habitat. Abbreviations: Ck: Cape Keraudren,
Ps: Port Smith, Th: Thangoo, Cc: Crab Creek, Wc: Willie Creek.
regarding habitat disturbances at logical comparisons between
the island, this species was listed known populations. Currently,
as ‘Threatened’ in Western C. angusticeps has both a state and
Australia [under the Wildlife federal listing as Schedule 1
Conservation Act Specially Pro¬ under the Wildlife Conservation
tected Fauna Notice in 1990]. Act 1950 and Vulnerable under
Since this listing, C. angusticeps the Environment Protection and
has been found on the mainland Biodiversity Act 1999. Two other
at two very disjunct coastal restricted range Ctenotus species
localities, one on Thangoo C. lancelini and C. zastictus have
Station, at the southern end of the same listings.
Roebuck Bay in the Kimberley Due to its perceived vulnerable
region (Sadlier 1993) and the status, one of the stipulated
other at Port Hedland in the research priorities for C.
Pilbara region (Turpin and Ford angusticeps is to undertake survey
2011). Both mainland accounts work to locate additional
provide information on ecology populations in the intervening
and habitat and make morpho¬ areas and determine the dis-
104
tribution of C. angusticeps along conducted daytime searches for
the northwestern coast of West¬ C. angusticeps from 2-10 May 2012.
ern Australia (Threatened Species This involved two teams of three
Scientific Committee 2008). people investigating areas of
Considering the distance be¬ potential suitable habitat as
tween the two mainland described by Sadlier (1993) and
localities and the lack of survey Turpin and Ford (2011), and the
effort in its documented habitat immediate surrounding habitats
thus far by experienced field between Onslow and Broome.
zoologists, it seemed highly likely Potential habitat was initially
that additional populations examined using vegetation maps,
would be located. Due to recent aerial imagery and Google Earth
finding of C. angusticeps at Port imagery, and permission was
Hedland (Turpin and Ford 2011), sought from landowners to
an area undergoing rapid port conduct any surveys on private
and/or infrastructure develop¬ land.
ment by mining companies, a
Searching methods involved
reconnaissance survey was con¬
slowly walking through areas
ducted in December 2011 to considered suitable and visually
determine its local distribution,
observing active lizards until a
relative abundance and habitat
positive identification was made.
preference. This was followed by
Once confirmed, attempts to
a broader-scale survey in May
capture some individuals were
2012, covering much larger areas
made by hand or by using a
to the north and south of Port circular metal ring to entrap a
Hedland to search for additional
lizard within low vegetation.
populations. Here we report on
Due to the extensive survey area
results of a targeted survey from to be assessed and time restraints,
Onslow to Broome in May 2012,
the use of more permanent trap¬
presenting new location records,
ping techniques was not feasible.
molecular examination of
Photographic records were taken
known populations and further
of the habitats where C.
notes on habitat preferences and
angusticeps were found along
other observations. We also pro¬
with images of individual lizards
vide a suggestion of a common
from most localities. Tissue
name change and a discussion
samples (tail-tips) were taken
relating to its current con¬
from ten C. angusticeps captured,
servation status.
and representative voucher
specimens were also collected
and lodged with the Western
METHODS
Australian Museum (Tissues
Experienced field zoologists R634-43; Specimens R172522,
familiar with the identification R172876-78). Each lizard cap¬
of Ctenotus spp. and with con¬ tured was then weighed,
siderable survey experience measured and released at capture
105
site. The retention of tissue and quences were edited and aligned
specimens was done in accord¬ with Sequencher v. 4.10 (Gene
ance with Regulation 17 licence Codes, Ann Arbor, Ml) and
to take fauna for scientific Geneious v5.5.6. Pairwise se¬
purposes (Number SF008623) quence divergence was calcu¬
issued by the Department of lated using MEGA 5. JModel test
Environment and Conservation, (Posada 2008) favoured an
Western Australia. GTR+G model for the ND2
mtDNA data and accordingly
We analysed 580 base pairs of
MrBayes (Huelsenbeck and
mitochondrial DNA for the ND2
Ronquist 2001) was used to
gene from thirteen individuals,
the rate of change in this generate a maximum a postori
mitochondrial locus has been tree (2.2 million iterations with
10% burnin) where parameters
estimated to be c. 1.3—1.4% Myr in
were surveyed (through ESS
other skink species (Macey et al.
values) to ensure appropriate
1997; Greaves et al. 2008). DNA
was extracted using DNeasy mixing. A sequence of Ctenotus
tissue extraction kits (Qiagen) robustus, the closest Ctenotus for
and the primers ND2 L4437 which ND2 has been sequenced,
was downloaded from GenBank
(Macey et al. 1997) and ND2rl02
(AY662548) and incorporated
(Sadlier et al. 2004) were used.
into the alignment as an
Standard PCR thermocycling
outgroup.
protocols were used and ampli-
cons were purified using either
ExoSap-lT (USB Corporation, OH,
NEW LOCATION RECORDS
USA) or QiaQuick PCR clean up
(Qiagen). Purified templates were In the Port Hedland area, C.
sequenced in both directions by angusticeps was recorded at
Macrogen (Seoul, Korea). Se¬ multiple localities, including
Table 1. Summary of new location records for C. angusticeps recorded in May 2012.
LOCATION DATE
Pretty Pool, Port Hedland 02/05/2012
Wedgefield, Port Hedland 02/05/2012
Redbank, Port Hedland 03/05/2012
Finucane Island, Port Hedland 03/05/2012
Boodarie Station, 12 and 16km W Port Hedland 03/05/2012
Lulu Creek, 7km E Karratha 06/05/2012
Beebingarra Creek, 15km E Port Hedland 03/05/2012
Cape Keraudren, 9km N Pardoo Roadhouse 04/05/2012
Port Smith, 25km NE Bidyadanga Community 07/05/2012
Thangoo Station, 28km SSE Broome 08/05/2012
Crab Creek, 16km ESE Broome 08/05/2012
Willie Creek, 25km N Broome 08/05/2012
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Redbank (Turpin and Ford 2011), angusticeps sampled from sites
Finucane Island, Pretty Pool and throughout their known range
Wedgefield. The species was also (Figure 2) up to 850 km apart was
recorded immediately west of small; the thirteen sequences
Port Hedland on Boodarie were 99.3% identical across the
Station and east at Beebingarra 580 nucleotide positions. The
Creek. We also recorded C. pairwise distance (using multiple
angusticeps from near Karratha, models) in the ND2 gene was
Cape Keraudren, Port Smith, uniformly low ~ 0.6%. While the
Thangoo Station (Sadlier 1993) Airlie Island population share a
and both Crab and Willie Creeks haplotype (based on a single
in the Broome area (Table 1, transversion), the clade is
Figure 1). embedded within the mainland
diversity. The ND2 gene region
used here has been investigated
SEQUENCE DIVERGENCE
in other skink species where
Intraspecific variation in the clades within the same species
ND2 gene fragment for C. were much greater than observed

C. angusticepsAirlie Island R103931

C. angusticepsAirlie Island R104349
0.98

H C. angusticepsAirlie Island R97423

C. angusticeps7km E Karratha AWFS-R12-035
0.99

C. angusticeps7km E Karratha AWFS-R12-034
0.98

- C. angusticepsRedbank TR252

r C. angusticepsRedbank R170418
I 0.64

L C. angusticepsRedbank TR253
- 0.99

L C. angusticepsBoodarie Station AWFS-R12-033
1.00

C. angusticepsCrab Creek RBB-R172522

- C. angusticepsPort Smith AWFS-R12-031
1.00

C. angusticepsThangoo Station AWFS-R12-032

- C. angusticepsCape Keraudren AWFS-R12-030

— C. robustusAY662548
0.01
Figure 2. Maximum a postori tree of Ctenotus ND2 sequence. The tree was
constructed in MrBayes (Huelsenbeck and Ronquist 2001) using thirteen C.
angusticeps sequences (580 bp) along with C. robustus (AY662548) as the
nominated outgroup. Posterior probabilities are shown on the nodes.
107
here (Greaves et al 2008). Taken sometimes forming large vege¬
together the data suggest the tation communities (Van
sampled populations are con- Vreeswyk et al. 2004). Although
specific. While the mtDNA ND2 the habitats on Airlie Island and
genetic distance is very shallow it the mainland are markedly
is acknowledged that to more different, the primarily coastal
accurately map the extent of distribution of C. angusticeps may
gene flow between populations suggest that the ‘salt marsh
that polymorphic markers (such communities’ are the ancestral
as STR’s) may need to be habitat of this species, with
evaluated. ND2 sequences have arguably the island population
been deposited on GenBank with secondarily adapting to the
accession numbers (KF537351- habitat now present on the
KF537363). island. This fragmented distri¬
bution is mirrored in other
fauna such as the legless lizard
HABITAT AND ENVIRONMENT
Delma borea and the murid
Ctenotus angusticeps has been rodent Pseudomys nanus, which
previously recorded as occurring also have relictual populations
in most habitat types on Airlie on islands off the Pilbara coast
Island, such as tussock grasslands (Maryan et al 2007).
and Acacia coriacea shrubland Our observations confirm that C.
with coastal Spinifex (Browne- angusticeps is very habitat specific,
Cooper and Maryan 1990), occupying areas broadly de¬
however this differs markedly to scribed as the landward fringe of
the vegetation occupied on the salt marsh communities, vege¬
mainland at Roebuck Bay tated with samphire and marine
(Sadlier 1993). Turpin and Ford couch grass immediately
(2011) provided a detailed de¬ adjacent to mangroves or some
scription of the habitat where C. distance away, though still
angusticeps was recorded at Port within close association. The
Hedland that is consistent with dominant vegetation being the
the ‘samphire shrubland along a succulent samphires Tecticornia
mangrove margin’ described by halocnemoides subsp. tenuis and
Sadlier (1993). Our survey effort Suaeda arbusculoides on clayey
was concentrated in these ‘salt soils with a mixed herb and
marsh communities’ on the grass cover of Muellerolimon
landward fringe of mangroves, salicorniaceum and Sporobolus
which are numerous and patchy virginicus on sandy soils (Beard
along the northwestern coast 1990). Ctenotus angusticeps was
Figure 3. The habitat at some of the locations where C. angusticeps were recorded ¿
showing the subtle differences in structure of samphire and marine couch grass
on a sandy clay substrate with numerous crab holes. All locations become
inundated during very high tides, (A) Karratha, (B) Cape Keraudren, (C) Crab
Creek.
108
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observed at some localities Derby, where ample mangroves
within the mangrove-lined creek and tidal creeks margin the King
edges but displayed a marked Sound. However from our
preference for the low open observations, the extreme land¬
shrubland area that is subject to ward fringes of salt marsh
tidal influences with numerous communities were devoid of crab
crab holes on a heavy, greyish holes and appeared unsuitable
sandy clay substrate. At some for this species. We did however;
locations where low sandy rises observe the abundant species C.
persisted with dense vegetation, inornatus in these areas.
especially marine couch grass, C.
The salt marsh communities
angusticeps was more numerous. inhabited by C. angusticeps are
These areas either formed a raised associated with the more ex¬
‘island’ surrounded by bare,
tensive mangrove communities,
sparsely vegetated mud flats or a
which are typically coastal plants
narrow strip (< 10m) growing subject to periodic tidal inun¬
through the samphire. Overall,
dation and exhibit a number of
the general structure of the
anatomical adaptations and
samphire did vary subtly from physiological characteristics
very low, dense clumps inter¬
which enable them to flourish
spersed with marine couch grass
under these conditions
to very flat, prostrate clumps or
(Semeniuk et al. 1978). Not only is
medium-high shrubs surrounded
this saline environment harsh,
by bare ground (Figures 3A-C).
subjected to extreme heat, wind,
Despite the apparent suitability glare and tidal influences, it is
of the habitat, C. angusticeps was also dynamic by virtue of the
not observed in the marginal, ever encroaching movement and
sandier Trzodza-dominated vege¬ recruitment of mangroves into
tation, where other species such new adjacent areas that are
as C. saxatilis and C. pantherinus dependant on water levels and
were prevalent. The occasional C. the effects of erosion. The
saxatilis was observed in the same mangroves are interconnected
habitat as C. angusticeps, particu¬ with the landward salt marsh
larly in the Port Hedland area, communities by trapping sedi¬
though in fewer numbers. An ment and creating areas of sand
apparent barrier may be the deposition for samphire and
Eighty Mile Beach area (Figure 1), other species to grow. Therefore,
where no C. angusticeps were it is feasible to assume that the
detected, despite the presence of environment for C. angusticeps
flat coastal plains of clayey sand would expand and contract over
with some samphire and marine relatively short periods of time
couch grass; however there were connecting and isolating lizard
no substantial mangroves with populations on a regular basis
associated crab holes. We also did and correspondingly, if C.
not record any C. angusticeps at angusticeps were reliant on crab
110
holes (see notes below) for To test whether lizards would
shelter, then the creation of utilise the crab holes even in the
these holes would fluctuate absence of perceived threat of
seasonally and possibly change being captured by us, we used a
from year to year. non-toxic fluorescent powder
(Radiant Colour Series Tl,
DayGlo Colour Corporation,
USAGE OF CRAB HOLES Ohio) to track their movements.
At all locations where C. Two adult C. angusticeps at
Redbank near Port Hedland
angusticeps was detected, crab
caught early in the day were
holes of varying sizes were
dipped in the ‘powder’ and
present and as reported by
released shortly afterwards
Turpin and Ford (2011), these
(methodology adopted from
were often used by skinks to
Stark and Fox 2000; Bernd and
take shelter, evading our at¬
Henle 2004). The next morning
tempts to capture them. Initially,
we tracked their movements
when adult lizards were observed
from the previous day to separate
they took shelter at the base of
crab holes where lizards sheltered
low vegetation, followed by
overnight, showing that the
retreating down a hidden hole
lizards are using crab holes by
among the samphire and marine
choice.
couch grass. By contrast, juvenile
lizards usually relied on the In highly exposed and harsh
protective cover of the vege¬ environments, burrows and
tation to avoid capture, often holes created by other animals
taking refuge amongst the dense would provide effective pro¬
tussocks of marine couch grass. tection to lizards (Davidson et al.
They would do this with some 2008). Many other species of
ease and after being pursued, Ctenotus shelter down holes,
later being located deep within mainly excavated by insects, or
the tussock. In addition, both by themselves (Taylor 1984)
adults and juveniles were some¬ especially in areas where the
times observed to retreat up into abundance of cover in the form
samphire vegetation, sometimes of rocks, logs, leaflitter, various
up to 30cm above the ground. hummock grasslands and deep
Thus, this species seems to be earth cracks is less (B. Maryan and
opportunistic in selecting retreat R. Lloyd pers. obs.). Similarly,
sites upon pursuing, and the there is minimal effective shelter
tendency and ability of lizards to where the C. angusticeps live apart
utilise a range of refuge types, from the crab holes and limited
both above and below ground dense vegetation, thus the
level, may be of great advantage former could be an essential
in a relatively open environment criterion in their habitat selec¬
where vulnerability to predation tion. In areas where there was
could be high. artificial shelter (e.g. pieces of
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driftwood), some skinks took and Ebrahim 2010; Berti et al.
shelter beneath these, but they 2008), frogs and other lizards
eventually disappeared down a elsewhere (Ng and Sivasothi
crab hole. 1999).
Another interesting observation The apparent high frequency of
made regarding the use of crab crab hole usage by lizards in the
holes was at Port Smith, where a salt marsh communities lead us
lizard was observed entering a to believe that these were an
low, prostrate samphire on an essential requirement for this
incoming tide that soon became species. This is reinforced further
submerged without the lizard by not observing any C.
being re-sighted. After the tide angusticeps in areas without crab
receded, we continued our holes. Mangrove crabs could be
searches on the recently inun¬ considered as ‘ecosystem en¬
dated ground that was very gineers’, a group of animals that
damp underfoot and sighted physically create, maintain and
several active C. angusticeps. We modify their environment (Jones
assumed at the time, that the et al. 1994). Hence the spatial
lizards were down crab holes, distribution and abundance of
possibly utilising air pockets to species that utilise these holes
sustain their residence, however could vary with the distribution
this requires further investi¬ of the particular species of crabs.
gation. The use of crab holes by The crab species inhabiting the
reptiles in areas subjected to northwestern coastline of
periodic inundation has been Western Australia are diverse
documented previously for with many specific to mangroves
other species of Australian and associated salt marsh com¬
reptiles occurring in tidal/ munities (Jones and Morgan
mangrove communities (e.g. 1994). The most likely species
Fordonia leucobalia, Myron digging the holes, where we
richardsonii: Gow 1989; Cox 1991; observed C. angusticeps are the
Karns et a12005; Murphy 2007; R. Fiddler Uca spp. and Bubbler
Somaweera pers. obs.). In Crabs Scopimera spp. Further
southwestern Western Australia, studies are required to investi¬
the skink Lissolepis luctuosa and gate whether the distribution of
snake Elapognathus minor, species C. angusticeps is correlated to
that do inhabit seasonally distribution of any particular
inundated wetlands, have been type of crab as shown for some
found in completely submerged other species (e.g. Subramanian
freshwater crayfish holes (B. 1984; Berti et al 2008).
Maryan pers. obs.). Burrows of
other crustaceans in mangrove
ACTIVITY
communities are also used by an
array of invertebrates (Ng and Ctenotus species are typically
Kang 1988), fish (Al-Behbehani diurnal, but some display
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