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Assisted colonisation trials for the western swamp turtle show that juveniles can grow in cooler and wetter climates


Abstract and Figures

Species with restricted ranges and long generation times are vulnerable to climate change due to limited opportunity to disperse or adapt. Australia’s rarest reptile, the western swamp turtle Pseudemydura umbrina , persists naturally in only one seasonal swamp that holds water in the Austral winter and spring. A marked reduction in winter rainfall in recent decades has shortened the swamp hydroperiod, restricting when turtles are able to feed, grow and reproduce. To mitigate possible future loss of reproductive capacity in the native habitat, assisted colonisation was trialled in 2016 using 35 captive-bred juveniles. Here, we report the outcomes of this 6 mo trial, which compared the growth of turtles released approximately 300 km south of the species’ indigenous range with growth of turtles released at an existing northern translocation site. We showed that growth rates comparable to those at warmer northern translocation sites can be achieved in the south, even in an atypically cool spring as occurred in 2016. Microclimates available to P. umbrina at 2 southern sites were suitable for foraging and growth in late spring and early summer, but juvenile growth at one southern site was significantly better than at the other, likely due to higher prey biomass when water temperatures were suitable for foraging. These early results suggest that introduction of P. umbrina to seasonal wetlands near the south coast of Western Australia could be considered in the immediate future, but further trials are recommended to assess growth and survivorship over longer periods.
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Endang Species Res
Vol. 43: 75– 88, 2020 Published September 17
Climate change is one of the most significant
threats to biodiversity this century (Pereira et al.
2010, Dickinson et al. 2014), and is rapidly shifting
the conditions that dictate the structure and function
of ecosystems (Walther et al. 2002, Parmesan & Yohe
2003, Parmesan 2006, Williams et al. 2008). One of
the most recognised impacts is a systematic shift of
the poleward range limit of a variety of taxa (Hughes
2000, Walther et al. 2002), occurring along the same
trajectory as climate change, at an average of 17 and
72 km decade−1 for terrestrial and marine taxa
respectively (Parmesan & Yohe 2003, Pecl et al.
2017). The accelerated rate at which global climatic
shifts are occurring places pressure on range-
restricted species, as geographic isolation reduces
their ability to track climatic changes and relocate to
more suitable areas (Parmesan 2006, Williams et al.
2008, Gibson et al. 2010). Furthermore, species with
long generation times have limited potential for
genetic or evolutionary adaptation in such rapidly
changing environments (Meynecke 2004, Urban et
al. 2014, Urban 2015). Without the capacity to move
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Assisted colonisation trials for the western swamp
turtle show that juveniles can grow in cooler and
wetter climates
Alexandra Bouma1, Gerald Kuchling1,2, Sherry Yi Zhai3, Nicola Mitchell1,*
1School of Biological Science, The University of Western Australia, 35 Stirling Highway, Crawley, WA 6009, Australia
2Department of Biodiversity, Conservation and Attractions, Parks and Wildlife Service, Wanneroo, WA 6065, Australia
3School of Earth and Environment, The University of Western Australia, 35 Stirling Highway, Crawley, WA 6009, Australia
ABSTRACT: Species with restricted ranges and long generation times are vulnerable to climate
change due to limited opportunity to disperse or adapt. Australia’s rarest reptile, the western
swamp turtle Pseudemydura umbrina, persists naturally in only one seasonal swamp that holds
water in the Austral winter and spring. A marked reduction in winter rainfall in recent decades
has shortened the swamp hydroperiod, restricting when turtles are able to feed, grow and repro-
duce. To mitigate possible future loss of reproductive capacity in the native habitat, assisted
colonisation was trialled in 2016 using 35 captive-bred juveniles. Here, we report the outcomes of
this 6 mo trial, which compared the growth of turtles released approximately 300 km south of the
species’ indigenous range with growth of turtles released at an existing northern translocation
site. We showed that growth rates comparable to those at warmer northern translocation sites can
be achieved in the south, even in an atypically cool spring as occurred in 2016. Microclimates
available to P. umbrina at 2 southern sites were suitable for foraging and growth in late spring and
early summer, but juvenile growth at one southern site was significantly better than at the other,
likely due to higher prey biomass when water temperatures were suitable for foraging. These
early results suggest that introduction of P. umbrina to seasonal wetlands near the south coast of
Western Australia could be considered in the immediate future, but further trials are recom-
mended to assess growth and survivorship over longer periods.
KEY WORDS: Assisted colonisation ∙ Translocation ∙ Climate change ∙ Turtle ∙ Wetland ∙ Growth ∙
Hydroperiod ∙ Pseudemydura umbrina
Endang Species Res 43: 75– 88, 2020
or adapt, many species will go extinct as a direct
result of climate change (Thomas et al. 2004).
Worldwide, reptile species are experiencing signifi-
cant declines, with an estimated 25% of species at
risk of extinction (Gibbons et al. 2000, Böhm et al.
2016) predominantly due to habitat loss and degrada-
tion and climate change (Gibbons et al. 2000, Sinervo
et al. 2010). Turtles (order Testudines) are particularly
imperilled relative to other larger vertebrate orders,
with 52% of species threatened (Rhodin et al. 2018).
The threat of climate change is amplified for turtles
and other ectotherms due to their fundamental re-
liance on a particular range of environmental temper-
atures for maintaining physiological performance
(Walther et al. 2002, Böhm et al. 2016). Al though in-
creases in global temperatures may elicit faster
growth rates and earlier sexual maturity (e.g. Mitchell
et al. 2012, Zuo et al. 2012), heat stress induced by
sustained periods at high temperatures interferes
with the regulation of metabolic functions (i.e. growth
and reproduction), resulting in reduced fitness (Sin-
ervo et al. 2010, Kingsolver et al. 2013). Reptile be-
haviours are also influenced by changes to microcli-
mates. While time budgets for basking, resting and
foraging can be adjusted under new microclimates
to improve physiological performance (Böhm et al.
2016), some species may be unable to meet their en-
ergetic requirements in warmer conditions, resulting
in reduced growth and survival (Sinervo et al. 2010,
Buckley et al. 2015). The magnitude of these impacts
is likely to be substantial for freshwater reptiles, as
aquatic environments have narrower temperature
ranges than terrestrial environments, limiting the
availability of thermal refugia under warmer con -
ditions (Pratchett et al. 2011). Further, freshwater
habitats in drying climates may shift from being
per manent to seasonal, rendering some habitats com-
pletely unsuitable for the species that currently utilise
them (Walther et al. 2002, Pratchett et al. 2011).
The Critically Endangered (Burbidge et al. 2010)
western swamp turtle (or tortoise; Pseudemydura um-
brina) is endemic to Western Australia, with only 40
adults surviving in small conservation reserves 30 km
north of Perth (see Fig. 1). Little is known of the spe-
cies’ past distri bu tion, but ecological evidence and
anecdotal infor mation suggests that the indigenous
range encompassed winter-wet swamps on the Swan
Coastal Plain, between Mogumber in the north and
Pinjarra in the south (Burbidge 1967, Burbidge et al.
2010). Habitat loss due to urban and agricultural ex-
pansion has been the primary driver of past population
de clines, but groundwater abstraction and climate
change are major new threats that have contributed
to the demise of the original Twin Swamps population
(Burbidge et al. 2010). Winter rainfall in the south-
west of Western Australia has reduced by approxi-
mately 26% since the 1970s (CSIRO & Bureau of
Meteorology 2018), heavy rainfall events have dimin-
ished (Philip & Yu 2020), groundwater has declined
(McFarlane et al. 2020) and summers have become
hotter (CSIRO & Bureau of Meteorology 2018). All
these processes shorten swamp hydro periods, which
define the activity season of P. u m bri na (Burbidge
1981, King et al. 1998). Historically, swamps held wa-
ter from May− June for 5−7 mo, and hatchlings consis-
tently grew to large sizes before their first aestivation
(Burbidge 1967). However, in recent years of low rain-
fall, hydro periods in P. u m bri na habitats have short-
ened to 3−4 mo (Arnall 2018). Consecutive years of
short hydroperiods limit foraging opportunities, con-
strain the capacity of females to accrue energy for re-
production (Arnall et al. 2019) and prevent hatchlings
growing to a critical size that prevents desiccation
during their first aestivation period (Mitchell et al.
2012, Arnall et al. 2015). Shortening hydroperiods
have also been observed at 2 northern translocation
sites for P. umbrina (Mo gumber and Moore River Na-
ture Reserves) established in the past 2 decades (P.
Muirdon unpubl. data), and projections from ecohy-
drological models indicate that hydroperiods will con-
tinue to decline (Mitchell et al. 2013). Such transloca-
tions to drier and warmer climates may ultimately fail,
highlighting the need for innovative conservation
practices to avoid the species’ extinction.
Assisted colonisation (also assisted migration, man-
aged relocation), is the intentional introduction of a
species of conservation concern to an area outside of
its indigenous range (IUCN/SSC 2013), and has
gained traction as a strategy for mitigating the im -
pacts of climate change on threatened species (Mc -
Lachlan et al. 2007, Seddon et al. 2015). Opponents
of this strategy appropriately highlight the risks of
introducing a species to a new habitat and the uncer-
tain impacts upon recipient ecosystems (Ricciardi &
Simberlo 2009). However, assisted colonisation has
the potential to protect threatened species and build
climate-resilient ecosystems (Seddon 2010, Lunt et
al. 2013), provided it can be done within an adaptive
management framework.
The current habitats of P. umbrina are likely to be
irreversibly altered under future climate change
unless major drought-proofing actions can be imple-
mented. Assisted colonisation has become an option
of strong interest to conservation managers, as P. um -
brina is unlikely to adapt rapidly to a new climatic
regime (generation lengths are at least 15− 20 yr;
Bouma et al.: Assisted colonisation of a freshwater turtle
Mitchell et al. 2012), and because any suitable habi-
tats nearby have been altered or destroyed. Hence,
following a decade of research on methods to iden-
tify optimal translocation sites outside the indi genous
range (Mitchell et al. 2012, 2013, 2016, Dade et al.
2014, Arnall 2018), a decision to trial assisted coloni-
sation was made by the species recovery team.
Wetlands near the south coast of Western Australia
are cooler than P. umbrinas current habitats, but
have longer hydroperiods and are likely to provide
ideal microclimates within 30−50 yr due to climate
change (Mitchell et al. 2013). The objective of the
trial was to assess the current suitability of southern
coastal habitats for supporting populations of P. um -
bri na, with a longer term goal of establishing new
populations should trials be successful. We expected
that P. umbrina released at southern sites would grow
more slowly than turtles released at a northern site,
but predicted that slower growth rates could be oset
by the longer hydroperiods over which individuals
forage and gain mass. Here, we quantified growth
rates of P. umbrina at 3 sites, assessed the thermal
variation in swamp microclimates, and analysed the
factors that influence juvenile growth. Taken together,
our data provide strong indicators as to whether P.
umbrina could persist in southern wetlands whose
current microclimates are near the lower limit of their
currently understood thermo dynamic niche (Mitchell
et al. 2013).
2.1. Translocation sites and study animals
Two wetlands near the south coast of Western Aus-
tralia (hereafter East Augusta and Meerup) were se-
lected as trial sites for assisted colonisation, and an
existing translocation site at Moore River Nature Re -
serve was selected to provide a comparison (Fig. 1).
The southern wetlands were identified by spatial
analysis (Dade et al. 2014) and assessed for thermal
and hydrological suitability via mechanistic species-
distribution modelling (Mitchell et al. 2013, 2016); site
visits by G.K. confirmed their structural similarity to
existing habitats. The trial was endorsed by the West-
ern Swamp Tortoise Recovery Team, and ap proved
by the Western Australian Department of Biodiversity
Conservation and Attractions (Animal Ethics Ap-
proval no. DPW-AEC 2016-19).
A total of 35 juvenile turtles with an average mass
of 130 g were sourced from the captive breeding
colony at Perth Zoo. Individuals were mostly 2−5 yr
old, but one slower growing turtle was 10 yr old.
Pseudemydura umbrina show rapid growth in their
first year and slower rates thereafter (Mitchell et al.
2012, Arnall et al. 2019); hence, we ensured a similar
distribution of age and mass in each of 3 release
groups to minimise any impact of these covariates on
growth after translocation.
Perth Zoo incubates P. umbrina under dierent in -
cubation regimes, so the turtles used in the trial had
dierent incubation histories; namely, constant 24°C,
constant 29°C, 24 ± 2°C and 29 ± 2°C (daily fluctua-
tions). Further, 4 turtles originated from an unde-
tected nest in a breeding pen. We analysed post-
hatching growth rates of juveniles reared in captivity
(which included the 35 turtles selected for the trial
but excluded any growth that occurred after release;
see Text S1 in the Supplement at
articles/suppl/n043p075_supp.pdf) and found that
incubation history aected growth in the first year
(p < 0.001) and over a 3 yr period (p = 0.005). In both
instances, incubation at cooler temperatures resulted
in more rapid growth than incubation at higher tem-
peratures (Fig. S1). Hence, incubation regimes were
evenly represented among the 3 release groups to
Fig. 1. South western Australia, showing the location of nat-
ural populations of Pseudemydura umbrina at Twin Swamps
(the population at Twin Swamps Nature Reserve now con-
sists only of animals reintroduced from captivity) and Ellen
Brook Nature Reserves (EBNR), the established transloca-
tion site at Moore River Nature Reserve (70 km north of
EBNR) and the 2 sites for the assisted colonisation trials at
East Augusta (290 km south of EBNR) and Meerup (330 km
south of EBNR)
Endang Species Res 43: 75– 88, 2020
minimise any impact of incubation history on growth
after translocation.
2.2. Release and monitoring
Prior to release, all turtles were fitted with a 6 g
radio transmitter (Model RI-2B; Holohil Systems) and
an iButton temperature logger (Thermochron DS -
1921G; Maxim Integrated Products). Grayson & Dor-
cas (2004) demonstrated a strong correlation in exter-
nal and cloacal temperatures of the turtle Chrysemys
picta, making external measures of temperature a
good proxy for body temperature. Temperature log-
gers and transmitters were each attached to the rear
of the carapace using marine-grade epoxy resin and
covered with black PlastiDip to waterproof and min-
imise visibility from aerial predators (see King et al.
1998). The mass of the transmitter, iButton, epoxy
and PlastiDip was approximately 10 g, which was
5.4% of the mass of the largest individual in the trial
(185 g at release) and 10.1% of the smallest individ-
ual (99.2 g at release). We programmed iButtons to
log every 30 min, which increases detection of bask-
ing events that are often shorter than 60 min (King et
al. 1998).
Turtles were released at the 3 sites in August 2016:
11 individuals were released at Moore River (10 Au -
gust), and 12 released each at Meerup and East
Augusta (11 August). Each site was visited 1 wk after
release to relocate turtles using a VHF receiver (Sika;
Biotrack) and a directional and stick antenna (Yagi;
Titley Electronics); thereafter, turtles were relocated
fortnightly for the duration of the hydroperiod, and
approximately monthly once turtles moved overland
or began aestivation. As a condition of translocation
approvals, all individuals that could be recaptured
from the southern sites were returned to Perth Zoo at
the termination of the trial. Although the trial was
approved for 12 mo, the recovery team elected to end
the trial after approximately 6 mo due to 3 factors:
(1) many turtles were losing transmitters as a result of
normal scute shedding after growth, (2) reattach-
ment of transmitters during aestivation was unadvis-
able due to possible disturbance of aestivation be -
haviours and (3) some turtles at East Augusta moved
onto private property to find aestivation sites.
2.3. Turtle microclimates and growth
To evaluate the microclimates available to turtles
at each site, temperature loggers (model DS1921G;
Thermochron iButton) were haphazardly deployed
in unshaded (and hence more open) areas of the
swamp at each translocation site. The loggers re -
corded temperatures in shallow water (~2 cm below
surface), deep water (bottom of swamp) and 5 cm
above the water in a typical location where juveniles
might bask. Logging stations (Fig. S2) were estab-
lished in triplicate at each site, and if necessary were
relocated by up to 10 m near the end of the hydro -
period to deeper water, which allowed us to continue
to compare 3 microclimates. At each site, ambient
temperature was measured 1.5 m above ground level
in a shaded location. Temperature loggers were pro-
grammed to record every 30 min for basking, shallow
and deep water microclimates, and hourly for ambi-
ent temperatures, at the same times as the tempera-
tures recorded on a turtle’s carapace. Hydroperiod
lengths could not be measured, as trials commenced
when standing water was already present. However,
the dates when standing water had evaporated at
each site were noted, and were used to infer dier-
ences in hydroperiod length.
Growth of turtles throughout the trial was quanti-
fied through measurements of body mass (Pesola
spring balance, ±0.3%), carapace length, carapace
width, carapace height and plastron length (digital
callipers, ±0.01 mm). Where possible (i.e. if a turtle
could be relocated), growth data were collected fort-
nightly for the duration of the hydroperiod at each
release site (until 17 November 2016 at Moore River
and until 20 December 2016 at Meerup and East
Augusta). All data were collected during daylight
hours (07:00−18:30 h), and eort was made to meas-
ure turtles at similar times of day across all 3 sites.
Turtles were not measured or otherwise disturbed
during aestivation in case they left aestivation bur-
rows, increasing predation risk.
2.4. Statistical analysis
All statistical analyses were conducted in R v.3.3.1
(R Core Team 2017), and data were checked for nor-
mality and outliers to ensure that they met the
assumptions of parametric testing. Any instances
where these assumptions were not met are noted in
the results.
Mass was used to assess growth rate, as it is a bet-
ter indicator of growth over short time scales relative
to morphometric measures. Appropriate adjustments
were made to each mass measurement in accordance
with the equipment an individual carried at the time
(i.e. iButton, transmitter and epoxy adhesive). The
Bouma et al.: Assisted colonisation of a freshwater turtle
specific growth rate (SGR) of each individual was
then calculated using the following formula:
where ln is the natural log, m(f ) is the final mass, m(i)
is the initial mass and time is the number of days
between initial and final measurements (Mitchell et
al. 2012). Individuals had dierent growth periods
according to when they left the swamp to search for
aestivation sites, and the dates that transmitters were
shed also influenced the timeframe over which
growth could be compared. Consequently, the SGR
over the longest time interval was calculated for all
individuals. For 24 individuals, the time interval was
from release to either the beginning of overland
movement or the end of the hydroperiod, and for
4 individuals SGRs were calculated over slightly
shorter time periods due to loss of transmitters. Tur-
tles with fewer than 6 wk of growth data were
excluded from the analysis of SGR described below.
A linear regression model was used to determine if
the SGRs of translocated turtles diered across the
release sites. The model included site as the predic-
tor variable and 5 covariates to test if any dierences
in growth rate were related to individual fixed
eects. Covariates were age (in years), incubation
regime (5 categories as described in Text S1 and Fig.
S1), mass at release (measured at Perth Zoo on 21 or
22 July 2016), the SGR of each individual in its first
year of life at Perth Zoo and a temperature correction
factor (a constant temperature equivalent [CTE]) that
integrated data on each turtle’s body temperature
during the growth period after its release. The CTE
was calculated from the hourly shallow water tem-
peratures (a proxy for turtle body temperature)
measured at each site, trimmed to align with the
dates over which the corresponding SGR was calcu-
lated. Temperature records were then converted into
rates (based on the thermal reaction norm of resting
metabolic rate of adult P. umbrina; Arnall et al. 2015),
and integrated as described in Georges et al. (2005)
to calculate the CTE. There was no significant inter-
action or collinearity between covariates included in
the model. We then conducted a backward elimina-
tion regression, removing the covariates with the
largest p-values one at a time until all terms in the
model were significant (p < 0.05). Model comparisons
were based on second-order corrected AICc for small
sample sizes.
A 1-way ANOVA with pairwise Tukey post hoc
comparisons was then used to determine at which
sites P. umbrina exhibited significantly dierent
SGR. Unequal variances were assumed due to small
sample sizes, and all data were checked for normal-
ity through visual inspection of Q−Q plots, distribu-
tion of residuals and histograms. Histograms showed
small deviance from normality due to some outliers
in the Meerup data, but this was considered accept-
able as data were unlikely to be normally distributed
due to the small sample size.
To assess dierences in available microclimates
across the translocation sites, average daily maximum
and minimum temperatures were calculated for the
duration of the hydroperiod. Some iButtons attached
to logging stations at Moore River did not record from
23 September to 10 November 2016, in which case we
reconstructed microclimates from the linear relation-
ship between ambient temperatures and each of the
microclimate temperatures (basking, shallow water,
deep water) for periods where all data types were
available. In some instances, data on ambient temper-
atures were missing, so we sourced ambient tempera-
ture data from a weather station maintained by the
Western Australian Department of Agriculture (Lan -
celin East) located 35 km northwest of the site. All re-
constructed data were used for visualisation purposes
only. When iButton-derived data were available across
the 3 sites (41 d between 12 Au gust and 22 Septem-
ber 2016), we compared microclimates using 1-way
ANOVA of daily minimum and maximum tempera-
tures. Additionally, micro climates were measured at
the southern trial sites for a further 83 d (28 Sep tem -
ber to 20 December 2016, demarcated by the end of
the hydroperiod), in which case dierences between
the minimum and maximum temperature values at
each site were assessed using 2-way t-tests.
We attempted to deduce the microclimates that tur-
tles utilised at the southern sites by determining
which microclimate temperatures aligned best with
averaged turtle carapace temperatures throughout
daylight hours (06:00−19:00 h; sensu Pittman & Dor-
cas 2009). We identified dates where most turtle data
were available and then arbitrarily selected 1 d each
month from August to November 2016 for plotting.
No statistical analysis was attempted, in recognition
that comparisons of carapace temperature based on
single dates could have been confounded by dier-
ences in solar radiation at each site.
2.5. Climate trend analysis
Growth in reptiles is influenced by annual variation
in weather, particularly during the activity season
ln ln
() ()
mf mi 100
Endang Species Res 43: 75– 88, 2020
(Adolph & Porter 1996), so we conducted an a poste-
riori climate trend analysis to determine if the
weather during the 2016 trial was typical. We con-
ducted separate analyses for annualised data, and for
data from July−December, which corresponds with
the activity period of P. umbrina. In both cases, data
on mean maximum air temperature, mean minimum
air temperature and rainfall were obtained from
weather stations located within 50 km of each site
that had long-term data sets (at least 10 yr of temper-
ature data or 30 yr of rainfall data). In addition to raw
values, anomalies from the 1961−1990 climate aver-
age were calculated and then normalised. In brief,
the 30 yr average of 1961−1990 is the current inter-
national standard for the recent climate (CSIRO &
Bureau of Meteorology 2018); hence, for any one
year, the anomaly is the rainfall dierence from the
1961−1990 mean rainfall, and the normalised anom-
aly is the dierence between the yearly anomaly and
the mean of all anomalies from 1961−1990. For both
air temperature and rainfall, statistical trends were
examined in R using the ‘autoregressive integrated
moving average’ (ARIMA) model of the ‘forecast’
package (Hyndman & Khandakar 2008). For rainfall,
‘cumulative deviations from the mean’ (CDFM) were
calculated to represent long-term rainfall trends
(Emelyanova et al. 2013).
Of the 35 Pseudemydura umbrina released in the
assisted colonisation trial, we were able to assess
growth until near the hydroperiod end for 24 individ-
uals, and so could evaluate a key criteria for translo-
cation success — whether an animal was able to gain
mass. However, radio transmitters and iButtons fre-
quently detached from turtles throughout the trial,
sometimes due to normal shedding of scutes, but also
due to poor attachment due to a faulty batch of epoxy
adhesive. For example, within the first week of re -
lease, 9 P. umbrina at East Augusta were returned to
Perth to have transmitters and iButtons re-attached
by G. K. with an improved adhesive. Ultimately,
16 turtles were transported to Perth for this 2 d proce-
dure before being returned to their release sites
within 3−4 d. These complications meant that not all
turtles in each release group were relocated during
each site visit, resulting in inconsistent sample sizes
for growth measurements. Similarly, as iButtons
were periodically shed and re-attached throughout
the trial, continuous records of carapace temperature
were not available for all turtles.
Hydroperiod lengths diered between northern
and southern translocation sites, with swamps in the
release areas at Meerup and East Augusta holding
water 6−8 wk longer than at Moore River. At Moore
River, swamps had dried completely by 11 November
2016, while at East Augusta water remained until
20 December 2016 in a trench dug to provide a re -
fuge, but this had evaporated by 4 January 2017. At
Meerup, shallow pools were present on 20 De cember
2016, but by 3 January 2017 the only standing water
was at least 500 m from the release swamp. In the
southern sites, all turtles had left swamps and com-
menced overland movements and aestivation behav-
iours by 20 December 2016.
Analysis of long-term climate data (Text S2)
showed that the winter−spring months at Moore
River and Meerup were wetter in 2016 than average,
while the winter−spring period at East Augusta was
drier and cooler than average (Tables S1 & S2,
Figs. S3− S5). Radio tracking revealed that all turtles
were moving overland or beginning to aestivate at
Moore River by 10 November, while at Meerup and
East Augusta these behaviours were first observed
on 20 December. Turtles were able to find suitable
aestivation sites in the assisted colonisation sites in
the south by using depressions under the skirts of
grass trees Xanthorrhoea sp. or shallow burrows at
the base of fallen logs. One Meerup turtle died in
February 2017. In this instance there were no visible
signs of predation but the animal was in poor body
condition. No other turtles were known to have died
during the trial.
Despite many turtles shedding radio transmitters,
most were relocated by chance near the end of the
hydroperiod at the southern trial sites. Once the deci-
sion to end the trial was made in January 2017 (see
Section 2.2), 10 individuals that had been released at
East Augusta were returned to Perth Zoo on 18 Jan-
uary 2017, and 2 turtles released at Meerup were
returned between 8 February and 8 March 2017.
Turtles released at Moore River were not collected,
as this is an established translocation site. In total, 2
and 9 turtles whose radio transmitters had been shed
remained at East Augusta and Meerup respectively
at the end of the trial; one of the Meerup individuals
was relocated in January 2019 by N. M.
3.1. Turtle growth rates
The average mass of juvenile P. umbrina through-
out the first month of the trial was similar at each
translocation site, but thereafter the average mass of
Bouma et al.: Assisted colonisation of a freshwater turtle
juveniles at Moore River increased until the hydro -
period ended in mid-November (Fig. 2a). In contrast,
juveniles at the 2 southern sites lost an average of
10 g over the first 2 mo of the trial. After this initial
loss, growth rates at East Augusta were comparable
to those at Moore River until the end of the hydro -
period in late December (Fig. 2a). The mass of juve-
niles at Meerup fluctuated throughout monitoring,
with little change in average mass over the trial
period (Fig. 2a). Comparison of linear regression
models showed that translocation site was the only
factor that aected the SGR of juvenile P. umbrina
(F2,25 = 9.46, p = 0.0008), as none of the 5 covariates
included in the model were significant, and models
that in clu ded covariates had lower support than the
model that included only site (Table S3). Post hoc
comparisons showed significant dierences between
SGRs at Meerup and East Augusta (p = 0.001), and at
Meerup and Moore River (p = 0.004), but no sig -
nificant dif ference between Moore River and East
Au gusta (p = 0.6) (Fig. 2b).
3.2. Microclimates of translocation sites
There were clear dierences in the aquatic micro-
climates available to P. umbrina at each translocation
site — most notably, all microclimates at Moore River
were warmer than those at Meerup and East Au -
gusta in the first 6 wk of the trial (August and Sep-
tember; Table 1, Fig. 3). Across all sites, daily maxi-
mum basking and shallow water temperatures were
within the activity range for P. umbrina (14−30°C) for
the duration of the trial, but deep water temperatures
at all sites were below 14°C until approximately mid-
October (Table 1, Fig. 3) and were significantly dif-
ferent between sites (F2,123 = 4.03, p = 0.02), with tem-
peratures at Moore River being higher than those at
East Augusta (p = 0.018). Daily maximum shallow
water temperatures across the 3 translocation sites
were also significantly dierent (F2, 123 = 98.03, p <
0.001; August−September data), with each site being
significantly dierent from the other (p < 0.001).
Shallow water environments at Moore River had a
smaller range of generally warmer temperatures than
the southern sites (Fig. 3d f). From late September
until December, when only the southern sites could
be compared, Meerup had significantly war mer shal-
low water temperatures than East Augusta (t210 =
7.05, p < 0.001), with more pronounced dierences
from September to December (Table 1, Fig. 3e,f).
There were no significant dierences in the mini-
mum (t138 = 0.7, p = 0.48) or maximum (t138 = 1.69, p =
0.09) deep water temperatures at the southern sites
over the same time period.
Basking microclimate temperatures followed simi-
lar patterns to those of the aquatic microclimates:
daily maximum basking temperatures across all sites
between 12 August and 22 September 2016 were sig-
nificantly dierent (F2,123 = 21.51, p < 0.001), with
temperatures at Moore River being higher than those
at Meerup (p < 0.001) and East Augusta (p < 0.001).
Daily minimum basking temperatures during this
same period were also significantly dierent (F2, 123 =
5.86, p = 0.003), with temperatures at Moore River
being higher than those at East Augusta (p = 0.002).
Fig. 2. (a) Average (±1 SE) mass of Pseudemydura umbrina
released at 3 translocation sites during the 2016 hydroperi-
ods, and (b) box and whisker plots of specific growth rates at
each release site. Lower and upper box boundaries: 25th and
75th percentiles respectively; thicker line inside the box: me -
dian; lower and upper error bars: 10th and 90th percen tiles
respectively; open circles: jittered raw data. Significant dif-
ferences are indicated by dierent letters (ANOVA, Tukey’s
post hoc test, α= 0.05)
Endang Species Res 43: 75– 88, 2020
Temperature (°C)
Moore River East Augusta Meerup
Min. Mean Max. Min. Mean Max. Min. Mean Max.
Basking microclimates
August 1.5 12.9 28.5 1.8 12.0 23.7 0.5 11.5 22.8
September 1.7 13.2 28.3 3.5 12.4 24.2 2.2 12.0 24.5
October 5.0 14.1 27.3 4.3 14.3 29.7
November 6.8 17.1 34.8 4.8 17.1 33.7
December 7.0 18.1 32.0 4.3 17.4 38.2
Shallow water microclimates
August 9 14.3 23.5 8.7 12.1 14.7 8.5 13.2 19.2
September 10.5 15 22.8 9.7 12.7 18.3 9.7 14.3 22.2
October 10.3 15.2 21.0 10.5 17.6 27.2
November 12.5 17.3 29.0 13.7 20.9 31.2
December 11.5 17.5 43.0 11.1 20.6 37.3
Deep water microclimates
August 9.3 12.5 21.2 9.2 12.2 13.8 9.2 12.1 14.0
September 10.7 13.0 14.5 10.5 12.7 18.3 10.2 13.0 15.5
October 10.7 15.0 19.2 10.7 16.0 20.2
November 13.8 18.7 29.0 14.0 19.7 27.7
December 11.8 19.6 33.2 12.3 20.1 33.7
Table 1. Indicative daily minimum, maximum and mean temperatures of basking, shallow water and deep water microcli-
mates at the 3 translocation sites during the hydroperiod. Values are the averages from 3 logging stations established at each
site. Data availability varied slightly in some months as follows: ‘August’ was 11−31 August at Moore River, and 12−31 August
at Meerup and East Augusta; ‘September’ was 1−22 September at Moore River, 1−23 and 28−30 September at Meerup and
1−23 and 29−30 September at East Augusta; ‘November’ was 1−10 and 22−30 November at Meerup, with the full monthly data
set available for East Augusta. (−) not available due to missing data
Fig. 3. Mean daily maximum temperatures (lighter lines) and mean daily minimum temperatures (darker lines) for (a−c) bask-
ing, (d−f) shallow water and (g−i) deep water microclimates at (a,d,g) Moore River Nature Reserve, (b,e,h) East Augusta and
(c,f,i) Meerup over the duration of the hydroperiods. Data at Moore River end on 10 November when the swamps dried.
Dashed lines: reconstructed data; gaps: missing data; grey shading: temperature range (14−30°C) at which Pseudemydura
umbrina are active (Lucas et al. 1963, Burbidge 1967). Daily maximum and minimum values were averaged for 3 envi-
ronmental stations located within the swamps at each site
Bouma et al.: Assisted colonisation of a freshwater turtle
From September to December, daily
maximum basking temperatures at
Meer up were significantly higher
(t138 = 2.43, p = 0.01) than those at East
Augusta, but minimum basking tem-
peratures were significantly lower at
Meerup (t138 = −4.56, p < 0.001),
reflecting the narrower range of bask-
ing temperatures at East Augusta
(Fig. 3b,c).
3.3. Comparison of carapace
temperatures across
translocation sites
During August and September at
both southern sites, both aquatic mi -
croclimates were below or just within
the critical thermal range considered
suitable for P. umbrina activity (14−
30°C; Lucas et al. 1963, Arnall et al.
2015), and turtle carapace tempera-
tures closely tracked these microcli-
mates and only rea ched temperatures
suited to activity near the end of the
day (Fig. 4a−d). By late October, both
shallow and deep water microclimates
were between 14− 30°C during day-
light hours, and carapace tempera-
tures recorded for Meerup turtles
were similar to those of the shallow
water microclimates, which were war -
mer than basking sites towards the
end of the day (Fig. 4f). In contrast, on
the same day at East Augusta, shallow
water microclimates were colder than
at Meerup, and juveniles operated at
temperatures closer to those of the
basking microclimate (Fig. 4e).
At the beginning of November (ap -
proximately 6 wk before southern
swamps dried), all microhabitats at the
southern sites were at suitable tem -
peratures for activity in P. umbri na.
Turtles at both sites exhibited a range
of carapace temperatures throughout
the day, most of which were substan-
tially warmer than those captured by the micro -
climate temperature loggers (Fig. 4g,h). In general,
turtles tracked water temperatures closely until ap-
proximately 10:00 h, after which time carapace tem-
peratures both in creased and fluctuated, suggesting
basking and foraging behaviours. Notably, P. um bri -
na were frequently observed basking in warm, shal-
low water during October and November at East Au-
gusta, but basking behaviour was never observed at
Fig. 4. Mean (±1 SE) carapace temperatures of juvenile Pseudemydura umbrina
(n = no. of ind.) and mean temperatures of basking, shallow water, deep water
and ambient microclimates between 06:00 and 19:00 h on 4 arbitrary dates at
East Augusta and Meerup when the most turtle data were available: (a,b) 18
August, (c,d) 18 September, (e,f) 28 October and (g,h) 8 November 2016. These
days were mostly sunny, with daily global solar exposure close to a typical
value, given in square brackets, for the month — East Augusta: (a) 13.3 [11.3], (c)
11.2 [15.2], (e) 20.5 [19.6], (g) 22.4 [24.9]; Meerup: (b) 10.6 [10.6], (d) 13.0 [13.6],
(f) 20.6 [18.7], (h) 20.3 [24.4]; all data from, Cape Leeuwin and
Northclie weather stations respectively. Areas between the deep and shal-
low water microclimates are filled to emphasise the contrasting range of water
temperatures measured at the 2 southern sites. Grey shading as in Fig. 3
Endang Species Res 43: 75– 88, 2020
This study reports a world first trial of assisted
colonisation of a vertebrate species in response to the
threat of climate change. Our fundamental objective
was to determine if assisted colonisation to wetlands
more than 300 km south of the indigenous range of
Pseudemydura umbrina is a viable option for cap-
tive-bred juveniles. The capacity for turtles to gain
mass during their winter−spring activity period was
considered to be a good indicator of the ability of
P. umbrina to persist in a novel habitat. At one of the
assisted colonisation trial sites (East Augusta), juve-
niles achieved equivalent growth rates to those re -
leased at the established northern translocation site
at Moore River. As growth at Moore River re flected
the growth expected in the indigenous range, this re -
sult suggests that seasonal wetlands in the East Au -
gusta area could be suitable for assisted colonisation
of P. umbrina in the immediate future. However, as
juveniles failed to gain mass at Meerup, despite ex -
periencing similar hydroperiods as at East Augusta,
there are clearly site-specific factors that contributed
to these contrasting results.
One factor (based on earlier work of Mitchell et al.
2012) that we considered likely to influence juvenile
growth rate was water and basking temperature.
While microclimates were significantly dierent
across translocation sites, each turtle’s estimated
temperature during their growth period (the CTE)
was not a significant covariate explaining their SGR,
nor did we detect significant dierences in carapace
temperatures of P. umbrina at the southern sites.
Examination of the carapace temperatures relative to
microclimate temperatures suggested that turtles at
Meerup and East Augusta selected shallow water
and basking microclimates in October and Novem-
ber. Aquatic basking is common in P. umbrina (King
et al. 1998) and allows turtles to forage in cooler envi-
ronments (Crawford et al. 1983). At East Augusta, the
similarity in the carapace temperatures of P. umbrina
and shallow water microclimates coincided with a
period of higher growth from September to late No -
vember (e.g. Fig. 4c,f,g). Juveniles at this site were
frequently found moving through warm, shallow
water, which suggested they selected microclimates
that met their thermal requirements while simultane-
ously providing opportunities for foraging.
A link between shallow water occupancy and
physiological performance is supported by data from
King et al. (1998), who showed that P. umbrina indi-
viduals that spent more time in warm water gained
mass faster than those that spent more time in cold
water. The temperature range for activity of P. umb-
rina is 14−30°C, and performance is optimal between
22 and 28°C (King et al. 1998); hence, low water tem-
peratures were the likely reason that P. umbrina
translocated to southern sites did not gain mass until
mid-September. The behavioural response of P. u m -
bri na to colder temperatures (<10−12°C) is to con-
serve energy by resting at the bottom of the swamp
(Lucas et al. 1963). This behaviour was observed at
both southern sites during daylight hours at Meerup
and East Augusta, where carapace temperatures
close ly tracked deep water temperatures (Fig. 4).
This passive behaviour likely resulted in preserva-
tion of energy, but also lack of growth as turtles were
not able to forage.
Cold water temperatures that constrained activity
were likely to be the key factor that prevented growth
of translocated turtles at the beginning of the trial, but
the lack of spring growth at Meerup, de spite suitably
warm microclimates, suggests that food resour ces
were limiting at this site. Swamp turtles require abun-
dant sources of aquatic invertebrates and tadpoles to
feed on during their activity period (Burbidge et al.
2010), and a concurrent study of food resources at
each translocation site (Schmölz 2018) showed that al-
though biomass in the Meerup wetland was generally
comparable to that at Moore River Nature Re serve,
towards the end of the hydro period it did not increase,
in contrast to the biomass at East Augusta. At East Au-
gusta, the biomass of tadpoles increased threefold be-
tween early and late spring. So while the total bio -
mass at Meerup was slightly higher in early spring
than in East Augusta, it did not in crease in late spring
when the thermal environment was more suitable for
foraging (Schmölz 2018). This suggests a phenological
mismatch in prey abundance and suitable foraging
microclimates at Meerup, which is problematic given
that the relationship between temperature and forag-
ing rates in reptiles is highly synergistic (Avery 1978,
Grant 1990, Zug et al. 2001). In a previous study of
captive-reared juvenile P. umbrina, food intake was
the primary driver of rapid growth, while water
tempe rature mediated higher rates of food intake
(Mitchell et al. 2012). Hence, wetland biomass and
the phenology of prey items should be important cri-
teria when selecting sites for future assisted colonisa-
tions of P. umbrina; otherwise their reduced activity at
lower temperatures cannot be oset by high food
While P. umbrina were capable of gaining mass in
the southern wetlands, even during months where
water temperatures were below the accepted thresh-
old for activity, growth of P. umbrina is clearly faster
Bouma et al.: Assisted colonisation of a freshwater turtle
at higher temperatures (King et al. 1998, Mitchell et
al. 2012). However, many ectotherms have higher
fitness near the lower bounds of their thermal opti-
mums (Bickford et al. 2010). This is likely to be true
for P. umbrina, as their activity decreases more rap-
idly at higher temperatures than it does at lower ones
(Lucas et al. 1963). Lucas et al. (1963) hypo thesised
that P. umbrina increase their body tem peratures in
cooler environments through re du ced but continued
activity, whereas sustained activity near upper ther-
mal limits is likely to destabilise the metabolic pro-
cesses necessary for survival. Furthermore, ecto-
therms from colder environments often reach larger
body sizes at maturity (Angilletta et al. 2004), which
may be beneficial for P. umbrina, as female body size
is correlated with fecundity (Ar nall 2018). These con-
siderations mean that assist ed colonisation to a suit-
able southern site could occur sooner rather than
later, as any fitness cost of occupying cooler habitats
may not necessarily be less than the impacts of con-
sistently short hydroperiods in the species’ indige-
nous range.
It will be necessary to consider landscape-scale site
characteristics, not only swamp areas, when selecting
areas for assisted colonisation for example, the
thermal suitability of terrestrial nests at candidate as-
sisted colonisation sites has already been evaluated
for P. umbrina (Mitchell et al. 2016). Importantly, the
long-term suitability of any southern site will be con-
tingent upon juvenile turtles being able to survive
their annual period of terrestrial aestivation. The
early end to our trial meant that aestivation behav-
iours such as arousal following low pressure systems
or rainfall could not be compared across sites. En-
couragingly, captive-reared juveniles found suitable
aestivation sites at both southern sites, but as the East
Augusta swamp was largely bounded by private prop -
erty, it led to several individuals moving onto private
land to aestivate. Appropriate land tenure (ideally
conservation estate) is viewed by species experts as a
key criteria in translocation site selection for P. umb-
rina (Dade et al. 2014), so the trial swamp at East Au-
gusta is unlikely to be the best option for establishing
a permanent assisted colonisation site. Fortunately,
the nearby Scott River National Park may oer a suit-
able alternative to the East Augusta trial site, as it has
similar vegetation and swamp characteristics, pro-
vides a much larger area and has little connectivity to
farmland or private properties.
Although this study revealed clear dierences in
the apparent suitability of the trial assisted colonisa-
tion sites, several limitations need to be acknowl-
edged. The first is small sample sizes, which were
further diminished when radio transmitters and tem-
perature loggers periodically detached from turtles
throughout the trial. This reduced the power of statis-
tical analyses, and limited the confidence in interpre -
ting the behavioural responses of P. umbrina to the
thermal microclimates available at each site. Second -
ly, data on carapace temperatures at Meerup came
from only 1 or 2 individuals. Thirdly, the lack of mi cro -
climate data from Moore River meant we were un -
able to establish whether P. umbrina consistently
utilised warmer microclimates in northern versus
southern sites, and whether this could explain the
marked increase in growth from September on -
wards. Finally, the south-west of Western Australia
experienced below average temperatures through-
out winter and spring in 2016 (see Figs S3 & S4),
which meant that the trial was conducted in an atyp-
ically cool period. As such, the results presented here
are preliminary, but provide a solid basis to support
further field trials in southern wetlands.
4.1. Recommendations for future trials
This study has provided important empirical data
to guide the selection of a site for assisted colonisa-
tion of P. umbrina. Earlier modelling and spatial
mapping studies that were focused on assisted colo -
ni sation of P. umbrina produced variable assess-
ments on the suitability of each of the southern sites.
For example, Dade et al. (2014) ranked the Meerup
site (named Doggerup Creek) as 8 out of 12 possible
sites, with food availability, site size and vegetation
composition noted to be likely limiting factors. Addi-
tionally, Mitchell et al. (2016) found that under future
climate change, the Meerup site had the lowest suit-
ability for supporting embryonic development due to
cool soil temperatures. This has important impli -
cations when considering permanent introduction
rather than a trial, as the suitability of the swamp
area for supporting juvenile growth is of little rele-
vance if P. umbrina are unable to successfully hatch.
East Augusta was previously identified as a site
where food availability was ideal, but site size and
land tenure were presented as key factors that re -
duced its suitability (Dade 2013). Notably, these pre-
dictions were borne out by the results of this trial.
When combined with the findings presented here, it
is clear that the assisted colonisation strategy for
P. umbrina will need multi-faceted evaluation to
ensure the best possible site is selected.
This study does not provide conclusive recommen-
dations for future assisted colonisation sites, but
Endang Species Res 43: 75– 88, 2020
shows that assisted colonisation could form part of
the conservation toolbox for P. umbrina provided that
the release site oers suitable aquatic and terrestrial
microclimates and abundant food. However, the
prospects of long-term survival of P. umbrina within
southern coastal habitats are less clear. Understand-
ing the biological constraints that aect P. umbrina in
new habitats (e.g. time to maturity, fecundity, hatch-
ling survival, movement patterns and population
growth rates) will be imperative for evaluating if a
translocation site will ultimately support a self-
sus taining population. Further, the impact of P. u m -
bri na on the recipient ecosystem needs to be quanti-
fied and monitored. We recommend that future trials
initially aim to be conducted over 12−18 mo to evalu-
ate survival, growth, microclimate use and behaviour
over the winter−spring activity period, throughout
aestivation and once turtles emerge from aestivation
at the beginning of the following hydroperiod. These
data should then inform a well-resourced assisted
colonisation attempt that is subject to regular moni-
toring to assess biological responses that will be ex -
pressed over long time periods — likely decades. Pur-
suing these recommendations should occur without
delay, as assisted colonisations may be the best op -
tion for maintaining self-sustaining wild populations
of P. umbrina as the regional climate rapidly transi-
tions to a drier, hotter state.
4.2. Conclusions
As global climates shift too rapidly for many spe-
cies to evolve and adapt in situ, it becomes increas-
ingly necessary to explore proactive methods of spe-
cies conservation. This will likely entail moving away
from traditional conservation ideologies of maintain-
ing or returning ecosystems to a historical reference
state (Hobbs et al. 2009, Thomas 2011). Assisted colo -
nisation is an inherently risky form of translocation
(Ricciardi & Simberlo 2009), but in order to promote
its eectiveness for conserving threatened species,
trials preceded by detailed planning and research, as
occurred here, are critical. This will allow assisted
colonisation to move beyond conjecture around its
collateral impacts to a fully explored strategy for con-
ferring species with resilience to an unprecedented
rate of climate change.
Acknowledgements. Funding was provided by the Australian
Government’s National Environmental Science Programme
through the Threatened Species Recovery Hub, the Depart-
ment of Biodiversity, Conservation and Attractions (Swan
Coastal District), the National Climate Change Adaptation
Research Facility’s National Adaptation Network for Natural
Ecosystems and the School of Biological Sciences at the Uni-
versity of Western Australia. We thank Don Bradshaw, Clive
Digney, Craig Olejnik, Bradley Barton, Ian Wilson and Kim
Williams for logistical support, Clive Digney for providing ac-
commodation at East Augusta and Stewart Macdonald,
Nicholas Rodriguez, Marcus Lee, Katja Schmöelz and Jian
Wang for their assistance with fieldwork. Data on early
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Editorial responsibility: Michael Mahony,
Callaghan, New South Wales, Australia
Submitted: April 4, 2020; Accepted: July 1, 2020
Proofs received from author(s): September 4, 2020
... It is evident that that there are long-term increases in temperature and decreases in rainfall in the south west of Western Australia as well as in the translocation sites (Bouma et al., 2020). The annual mean temperature in the south west of Western Australia has increased by 0.1-0.3 ...
... In the present study, as a first step to evaluate the feasibility of the management technique of assisted colonization of P. umbrina to two selected wetlands, food availability was investigated through the temporary translocation of captive-bred juveniles and the assessment of the biomass and diversity of potential prey. Habitat and temperature selection and growth of the turtles were evaluated in a parallel study (Bouma et al., 2020). The potential food resources and prey selection by P. umbrina were assessed at the above three sites (Moore River, Meerup and East Augusta). ...
... The average invertebrate biomass was lower in the two southern areas of Meerup and East Augusta than in Moore River (Table 1). Chironomidae 3 3 3 3 3 3 3 4 4 4 3 4 3 3 3 3 3 3 Culicidae 3 2 2 1 1 1 Muscidae 1 1 invertebrates in Moore River Nature Reserve compared with the southern sites might be attributed to warmer shallow water conditions (Bouma et al., 2020) and the relatively wet winter and spring in 2016: in 2016 Moore River received 743.4 mm, the highest annual rainfall since 1999 although the July to December rainfall was slightly below average (Bureau of Meteorology Perth, 2017). Crayfish, some of which can be predators of P. umbrina (Bradsell et al., 2002), were also found in Meerup and East Augusta. ...
• The natural habitat of the western swamp turtle (Pseudemydura umbrina Siebenrock, 1901) – the ephemeral, winter wet swamps north of Perth, Australia – is in danger owing to climate change and habitat fragmentation. The decline in rainfall in this area over the last five decades is predicted to continue, shortening the annual activity period for the turtles and potentially shifting their optimal climate zone to the south. • Assisted colonization to wetlands in the cooler far south west of the state is one management response. As a contribution to such a measure, the diversity and abundance of food resources and consumption by turtles were evaluated at two potential and one existing colonization site. • Thirty‐five captive‐bred juvenile P. umbrina were temporarily released into three sites: Moore River Nature Reserve north of Perth (into which the species had already been successfully translocated) and Meerup and East Augusta in the cooler far south of Western Australia. • Food resources were assessed using sweep nets to sample invertebrates on two occasions at each wetland. Separate samples were collected for biomass determination and for assessing invertebrate diversity. Feeding by turtles was assessed by stomach flushing. • Neither biomass nor biodiversity differed significantly between the southern sites and the reference site north of Perth. Stomach contents varied greatly, from 0 to 62 animals per turtle. The main prey items were beetles, ostracods, isopods and tadpoles. • Each candidate wetland provided adequate food resources, indicating that assisted colonization to the cooler south coast of Western Australia has the potential to become a reasonable conservation tool to ensure the long‐term survival of P. umbrina.
... To combat emerging threats, increasingly more extensive ecosystem manipulations are suggested, including assisted colonisation (Brodie et al., 2021), the translocation of individuals outside of their established range as a response to threats such as climate change (IUCN/SSC, 2013). These sorts of translocations, moving organisms outside of both their current and indigenous ranges are inherently extrapolative, as managers are knowingly creating unprecedented conditions and ecological interactions (Rendall et al., 2018;Bouma et al., 2020). ...
... We urge caution in the application of extrapolative translocation strategies, particularly with regard to assisted colonisation and rewilding projects that seek to create novel ecosystem conditions (Corlett, 2016). In these cases, where there is so much inherent uncertainty, we suggest that decisions should always be informed by what data are available, and that even the most experimental translocations should be based on evidencebased hypotheses regarding the potential success and risks of the translocation (Armstrong and Seddon, 2008;Bouma et al., 2020). This is due to the cautionary tales from the field of invasive species management, in which many species that have been introduced outside of their native range, whether accidentally or intentionally, are a major driver of ecosystem degradation and biodiversity decline, costing conservation management vast resources to reduce and reverse the resulting damage (Brook et al., 2008;O'Donnell et al., 2017). ...
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In response to anthropogenic threats, conservation translocations are increasingly used to combat species' population and range declines. However, moving animals outside of their current distribution can mean introducing them to novel conditions, even in the case of reintroductions to formerly inhabited areas due to ecosystem changes following extirpation. This exposure to novel conditions introduces uncertainty that can undermine decision making for species conservation. Here we propose two strategies, which we define as conservative and extrapolative, for approaching and managing novelty and the resulting uncertainty in conservation translocations. Conservative strategies are characterised by the avoidance and removal of novel conditions as much as possible, whereas extrapolative strategies are more experimental, allowing exposure to novel conditions and monitoring outcomes to increase understanding of a species' ecology. As each strategy carries specific risks and opportunities, they will be applicable in different scenarios. Extrapolative strategies suit species in recovery which can afford some experimental management, or species facing novel and emerging threats which require less traditional translocations, such as assisted colonisations. We provide examples, applying our framework to two endemic New Zealand species with long histories of translocation management: tuatara (Sphenodon punctatus), a reptile and takahē (Porphyrio hochstetteri), a flightless bird.
... These may include improving demography (e.g. to address a declining population size, Forbes et al., 2016); improving genetic diversity (such as by identifying inbred populations, e.g. Poirier et al., 2019); restoring faunal assemblages/ecological processes across a species' former range (Mittelman et al., 2020); or ensuring the long-term survival of a species through assisted colonisation (Bouma et al., 2020). Genetic data can help inform conservation translocations and other population management actions by providing data on i) the current situation, ii) which populations may require supplementation/augmentation, and iii) which populations may be the best source locations for augmenting/establishing new populations to ensure the long-term adaptive potential of the species is maintained, i.e. the more genetic diversity the greater the adaptive potential (Frankham et al., 2017a). ...
The value of genetic management is increasingly recognised in natural resource management particularly in relation to threatened species conservation and translocations. Technical advancements in methodologies available to conservation managers for genetic management present a challenge for long-running programs that monitor genetic diversity over time. Given that microsatellite and single nucleotide polymorphism (SNP) data are not interchangeable, conservation managers are faced with two options: continue using older techniques for consistency (limits genetic knowledge); or discard previous data and move to more precise modern genetic markers (wastes resources and prevents temporal monitoring). To achieve a balance, we should consider whether conservation recommendations made are broadly similar between interpretations of different marker sets, even if estimates are not directly comparable. Here we generated 13,194 SNPs for the woylie (Bettongia penicillata), an Australian marsupial, to provide conservation recommendations across their current range (N=13 indigenous, reintroduced and haven populations) and provide guidance to conservation managers on how these recommendations align with those previously made using 12 microsatellite markers. Observed heterozygosity was significantly less than expected heterozygosity reflecting the historical bottleneck for the species. Only 4 of the 13 populations showed evidence of inbreeding, and effective population sizes ranged from 9.9 to 268.9. Trends in observed heterozygosity were broadly similar between microsatellite and SNP marker sets. Herein we provide advice for conservation managers undertaking translocations on using genetic data, highlight the benefits of moving to newer SNP based approaches for monitoring conservation actions over time, and show that historical management actions are supported by new technologies.
... Combining the different aspects of a species rarity (its low abundance; the distinctiveness of its traits; its isolated position in the phylogeny), for the scope of this paper, we will thus consider two intuitive conditions that a measure of effective FP-originality should respect. Consider an assemblage composed of N species with relative abundances Australia (Bouma et al., 2020), morphologically unique among extent Chelidae. The originality of this species may be due to strict trait conservatism along its evolution as fossil data indicates little morphological change for this species since the early Miocene (Zhang et al., 2017). ...
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Rarity reflects the low abundance of a species while distinctiveness reflects its quality of being easy to recognize because it has unique functional characteristics and/or an isolated phylogenetic position. As such, the assemblage-level rarity of a species' functional and phylogenetic characteristics (that we name 'effective originality') results from both the rarity and the distinctiveness of this species. The functional and phylogenetic diversity of an assemblage then results from a compromise between the abundances and the effective originalities of the species it contains. Although the distinctiveness of a species itself depends on the abundance of the other species in the assemblage, distinctiveness indices that are available in the ecological literature scarcely consider abundance data. We develop a unifying framework that demonstrates the direct connections between measures of diversity, rarity, distinctiveness and effective originality. While developing our framework, we discovered a family of distinctiveness indices that permit a full control of the influence one wants to give to the strict uniqueness of a species (=its smallest functional or phylogenetic distance to another species in the assemblage). Illustrating our framework with bat phylogenetic diversity along a disturbance gradient in Mexico, we show how each component of rarity, distinctiveness and originality can be controlled to obtain efficient indicators for conservation. Overall our framework is aimed to improve conservation actions directed towards highly diverse areas and/or towards species whose loss would considerably decrease biodiversity by offering flexible quantitative tools where the influence of abundant versus rare, and ordinary versus original, species is understood and controlled.
... Second, the change in conditions may require some species to move to an area with more suitable habitat or environmental conditions. However, the ability of animals to move to more suitable areas is severely threatened by habitat fragmentation in some places, or the resources they rely on to be available (for example, frugivores can only move to areas with sufficient mature fruiting trees to feed on), as well as their own mobility (Bouma, Kuchling, Zhai, & Mitchell, 2020;Monzón, Moyer-Horner, & Palamar, 2011;Razgour et al., 2018). ...
While considerable evidence exists that extreme climate events such as high temperatures and drought are becoming more common, there is growing recognition that we have limited empirical evidence on how wild animals are able to behaviorally and physiologically adjust to these potentially rapid changes. Despite considerable lab-based research on thermal physiological processes in animals, there is relatively little field-based research on how thermal stress affects physiology and behavior in wild animals. Directly relating physiological state to behavioral change is an important step in understanding the ability of species to adapt to changing climatic conditions and is therefore an important research gap to address during both the current and predicted future rapid changes in climate. Given that the ability of animals to adjust to changing conditions can directly impact their fitness, understanding the behavioral and demographic responses of animal populations to current climate events may be an essential way to determine future population viability. By synthesizing the long-term behavioral research on the pied babbler (Turdoides bicolor), conducted over the last 18 years, we determine the potential impact of climate change through an examination of behavioral responses to social and environmental factors. By combining our detailed behavioral, demographic and physiological research, we use the pied babbler as a model species to highlight the incredible value of (a) long-term behavioral research and (b) studying populations under natural conditions, to help understand the potential impacts of climate change on wild animals.
With novel ecosystems becoming the norm, it is increasingly necessary to re‐evaluate what is meant by “restoration”. An important aspect of this concept is what we define to be native and, by extension, alien. In order to better prioritize restoration projects, we have here devised a classification system of ten, graduated terms that describe intermediate states of nativeness which can be applied to different organisms based on their histories, origins and impacts. This article is protected by copyright. All rights reserved.
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A warming and drying climate in the South West of Australia since about 1975, and especially from 2000, has reduced flooding and lessened salinisation risks, but also has reduced fresh water supplies. As well as continuous trends, there have been abrupt changes in hydrological processes as groundwater levels have receded from valleys. In some cleared inland wheatbelt areas, saline groundwaters are still rising where the watertable is deep, clearing has been recent and/or the reduction in rainfall has been limited. Over time, groundwater level changes will better reflect the drying climate. The reduction in rainfall and higher potential evaporation rates has dried catchments overall, and greatly reduced runoff and major flooding, even in catchments where salinity is still expanding across valley floors. Major flooding after rare storms may occur, but now is more likely in summer than winter. It is now driven by infiltration-excess rather than saturation-excess runoff processes, depending on landscape position, and rainfall amount and duration. Episodic events, such as occurred in 2017, may increase salinity and flooding for a period despite the overall decreasing trend in such risks. In the largely cleared Zone of Rejuvenated Drainage and vegetated Darling Range, groundwater levels in cleared areas are close to reaching a new equilibrium, with the drier climate reducing salinisation risks. In the largely forested Darling Range, groundwater levels are falling below stream beds thereby substantially reducing runoff into dams in the western part of the zone where groundwaters are fresh. As a result, Perth (population two million) has transitioned from being almost entirely dependent on such runoff for its drinking water, to not having any usable runoff in some years. In the Perth Basin, groundwater levels are falling within sedimentary strata as the predominantly perennial vegetation uses a high proportion of incoming rainfall. The less intense and more intermittent rainfall is also increasing canopy interception and unsaturated-zone water losses. Cleared areas with high watertables are least affected because a reduction in recharge may be offset by less rejected runoff, lower drain flows and evaporation from vegetation tapping into groundwater. This buffering will continue until groundwater levels fall beneath drain inverts and plant rooting depths. The impact of the drying climate on groundwater levels has been masked to date by increasing recharge due to clearing and urbanisation. Streams connected to strata in the Perth and Collie basins usually gain fresher water from unconfined aquifers. With falling groundwater levels drainages are transitioning from gaining-to losing-streams, with reducing surface water flows and increasing risk of aquifer salinisation where the cross-cutting streams are saline. Climate projections indicate a continuing drying trend is likely with increased temperatures and possibly a greater proportion of annual rainfall, and therefore flood risks, in summer. Water yields in dams and aquifers will continue to decline if these projections are correct. However, risks associated with too much water (salinisation, flooding, soil waterlogging) will probably continue to abate unless the amount and/or intensity of rainfall increases in the future.
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Significant decreases in rainfall in South West of Western Australia (SWWA) over recent decades are of concern for water supply and agricultural production in the region. Total rainfall can be decomposed into light, medium and heavy rainfall, and the land responds differently to these rainfall classes. Little, however, is known about changes in different rainfall classes in SWWA. The objective of this study is to quantify contributions from these rainfall classes to the decrease and interannual variations in rainfall, and to relate the decreases to station characteristics, i.e. latitude, elevation and the mean annual rainfall, and to the large scale circulation pattern known as the Southern Annular Mode (SAM). Long‐term data for 30 stations were used, and daily rainfall was divided into three classes in such a way that they contributed equally (one‐third of the total) for each station. Trend and correlation analysis was applied to these classes. The decrease in heavy rainfall was mainly responsible for the decrease in total rainfall, followed by the medium and light rainfall. The rate of decrease in heavy rainfall was 68% higher than, while that in light rainfall was about half, of the expected trend. Heavy rainfall exhibited a significant decreasing trend in winter and autumn but mildly increasing trend in summer. The number of heavy rain days also showed a significant decreasing trend. The rate of decrease relative to the mean was similar for both heavy rainfall and number of heavy rain days. Stations with a higher rainfall were more likely to experience a decrease in rainfall than those in the drier inland areas. Stations where rainfall was strongly correlated with SAM were mostly concentrated along the west coast of SWWA. The SAM index explained 9% of the variation in heavy rainfall and 11% in total rainfall for the region. This article is protected by copyright. All rights reserved.
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We present a review and analysis of the conservation status and International Union for Conservation of Nature (IUCN) threat categories of all 360 currently recognized species of extant and recently extinct turtles and tortoises (Order Testudines). Our analysis is based on the 2018 IUCN Red List status of 251 listed species, augmented by provisional Red List assessments by the IUCN Tortoise and Freshwater Turtle Specialist Group (TFTSG) of 109 currently unlisted species of tortoises and freshwater turtles, as well as re-assessments of several outdated IUCN Red List assessments. Of all recognized species of turtles and tortoises, this combined analysis indicates that 20.0% are Critically Endangered (CR), 35.3% are Critically Endangered or Endangered (CRþEN), and 51.9% are Threatened (CRþENþVulnerable). Adjusting for the potential threat levels of Data Deficient (DD) species indicates that 56.3% of all data-sufficient species are Threatened. We calculated percentages of imperiled species and modified Average Threat Levels (ATL; ranging from Least Concern = 1 to Extinct = 8) for various taxonomic and geographic groupings. Proportionally more species in the subfamily Geoemydinae (Asian members of the family Geoemydidae) are imperiled (74.2% CRþEN, 79.0% Threatened, 3.89 ATL) compared to other taxonomic groupings, but the families Podocnemididae, Testudinidae, and Trionychidae and the superfamily Chelonioidea (marine turtles of the families Cheloniidae and Dermochelyidae) also have high percentages of imperiled species and ATLs (42.9–50.0% CRþEN, 73.8–100.0% Threatened, 3.44–4.06 ATL). The subfamily Rhinoclemmydinae (Neotropical turtles of the family Geoemydidae) and the families Kinosternidae and Pelomedusidae have the lowest percentages of imperiled species and ATLs (0%–7.4% CRþEN, 7.4%–13.3% Threatened, 1.65–1.87 ATL). Turtles from Asia have the highest percentages of imperiled species (75.0% CRþEN, 83.0% Threatened, 3.98 ATL), significantly higher than predicted based on the regional species richness, due to much higher levels of exploitation in that geographic region. The family Testudinidae has the highest ATL (4.06) of all Testudines due to the extinction of several species of giant tortoises from Indian and Pacific Ocean islands since 1500 CE. The family Testudinidae also has an ATL higher than all other larger polytypic families (higher than 5 species) of Reptilia or Amphibia. The order Testudines is, on average, more imperiled than all other larger orders (� 20 species) of Reptilia, Amphibia, Mammalia, or Aves, but has percentages of CRþEN and Threatened species and an ATL (2.96) similar to those of Primates and Caudata (salamanders).
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Distributions of Earth’s species are changing at accelerating rates, increasingly driven by human-mediated climate change. Such changes are already altering the composition of ecological communities, but beyond conservation of natural systems, how and why does this matter? We review evidence that climate-driven species redistribution at regional to global scales affects ecosystem functioning, human well-being, and the dynamics of climate change itself. Production of natural resources required for food security, patterns of disease transmission, and processes of carbon sequestration are all altered by changes in species distribution. Consideration of these effects of biodiversity redistribution is critical yet lacking in most mitigation and adaptation strategies, including the United Nation’s Sustainable Development Goals.
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In south-western Australia (SWA) groundwater levels have been declining under the changing climate associated with a decline of rainfall. Possible future groundwater yields in SWA have been estimated under a range of climate change scenarios using a number of numerical groundwater models. For the Northern Perth Basin (NPB) in SWA, where no groundwater models were available, a relatively simple statistical method CDFM (Cumulative Deviation from Mean) has been applied using HARTT (Hydrograph Analysis and Rainfall Time Trends), an automated derivation of the CDFM. This study has evaluated the potential of the CDFM to project groundwater levels under various future climate scenarios in the NPB. Firstly, HARTT projections were validated by comparing with the modelled hydrographs in areas where numerical groundwater models were available. It was evident that HARTT may overestimate future declines or rises in groundwater levels depending on the time a new climate regime is imposed on the model. Secondly, HARTT was applied to suitable bores in the NPB under future climate scenarios. HARTT projected a slight decline under a drier future climate than under the historical future climate and a moderate or slight rise in groundwater levels under a wetter future climate. If historical climatic conditions continue until 2030, groundwater levels are expected to slightly rise in the NPB.
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Assisted colonisation, the translocation of organisms with release in areas outside their indigenous range in response to threats such as climate change, was presented in the scientific literature only a few years ago as a new tool for species conservation. The idea of planned introductions for conservation is a controversial issue, prompting vigorous and sometimes ill-informed debate in the scientific literature. The broad consensus was that this represented a bold new direction that had merit but carried great risk. Unacknowledged by most commentators, assisted colonisation, by other names, was already taking place, and in Australasia was even a long-accepted part of the conservation management tool kit. In 2013 the IUCN recognised assisted colonisation as a legitimate, if inherently risky, conservation translocation, and set out a comprehensive set of guidelines for its application. We review the history of assisted colonisation, with a focus on Australasian projects moving species in response to threats within the indigenous range. We review the current status of assisted colonisation in Australasia and present two case studies to illustrate the application of new approaches for assisted colonisation planning: western swamp turtle (Australia), and hihi (New Zealand stitchbird). We conclude by considering future directions in the specific application of translocations for climate change mitigation in the region.
The embryos of many egg-laying species develop under the environmental conditions selected by one or both parents, and these conditions may cease to be optimal under a changed climate. Assisted colonization is an emerging option to relocate species that are threatened by unfavourable changes in the local climate, but the incubation requirements of embryos are rarely considered in conservation translocations despite suggestions that relocation of early life stages could be more effective than relocating older animals. Here we review examples and outcomes of relocations of reptile eggs, and the decision tools currently available for guiding translocation decisions from an embryonic perspective. We then demonstrate a mechanistic approach, using the modelling framework NicheMapR, for assessing the optimal translocation range for the Western Swamp Turtle (Pseudemydura umbrina), a Critically Endangered reptile with an extremely restricted natural distribution. We determine thermal reaction norms and critical thermal limits for embryonic development based on laboratory and field data, and model soil temperatures at typical nest depths, simulate embryonic development at these depths, and map the probability of survival of P. umbrina embryos within the major bioregions of south-western Australia. The same model forced by future climates for 2050–70 demonstrates a southerly shift in the regions where embryos would be viable. However, if P. umbrina is to be translocated in the near future to regions 300–400 km south of its natural range, females will need to nest in relatively unshaded sites to achieve temperatures that are high enough to promote hatchling success.
The fourth edition of the textbook Herpetology covers the basic biology of amphibians and reptiles, with updates in nearly every conceptual area. Not only does it serve as a solid foundation for modern herpetology courses, but it is also relevant to courses in ecology, behavior, evolution, systematics, and morphology. Examples taken from amphibians and reptiles throughout the world make this book a useful herpetology textbook in several countries. Naturalists, amateur herpetologists, herpetoculturists, zoo professionals, and many others will find this book readable and full of relevant natural history and distributional information. Amphibians and reptiles have assumed a central role in research because of the diversity of ecological, physiological, morphological, behavioral, and evolutionary patterns they exhibit. This fully revised edition brings the latest research to the reader, ranging over topics in evolution, reproduction, behavior and more, allowing students and professionals to keep current with a quickly moving field.
Current predictions of extinction risks from climate change vary widely depending on the specific assumptions and geographic and taxonomic focus of each study. I synthesized published studies in order to estimate a global mean extinction rate and determine which factors contribute the greatest uncertainty to climate change-induced extinction risks. Results suggest that extinction risks will accelerate with future global temperatures, threatening up to one in six species under current policies. Extinction risks were highest in South America, Australia, and New Zealand, and risks did not vary by taxonomic group. Realistic assumptions about extinction debt and dispersal capacity substantially increased extinction risks. We urgently need to adopt strategies that limit further climate change if we are to avoid an acceleration of global extinctions. Copyright © 2015, American Association for the Advancement of Science.