Abstract and Figures

Mitigation-driven translocations represent an increasingly common management solution to reduce animal mortality and habitat loss caused by human development. Although they currently outnumber other translocation types, there is a lack of scientific approaches to evaluate the outcome of this management tool. We designed an experimental translocation with two groups of translocated males and two of control males of a small (6-14 g) lizard (totaling 120 individuals). Our results suggest that translocated individuals covered longer distances (53 vs. 18 m) from their respective release points in one month (on average), although this distance diminished over time. Displacing longer distances was associated with a body condition impoverishment and an increase in parasitization by ectoparasites. To the best of our knowledge, this is the first study that finds a positive relationship between covering longer distances and an increase in the number of mites. This was also explained by the initial mite load that lizards had, suggesting that controlling the infestation by mites is energetically demanding for lizards, being traded by locomotor activity. At least for those individuals in poorer body condition, we recommend the implementation of soft release (gradually accustoming individuals to their new environment by previously releasing them into controlled conditions) and deparasitization before accomplishing a mitigation-driven translocation.
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Amphibia-Reptilia (2021) DOI:10.1163/15685381-bja10040 brill.com/amre
Associated costs of mitigation-driven translocation in small lizards
Rafael Barrientos1,,∗∗,∗∗∗, Rodrigo Megía-Palma2,3,∗∗∗,∗∗∗∗
Abstract. Mitigation-driven translocations represent an increasingly common management solution to reduce animal
mortality and habitat loss caused by human development. Although they currently outnumber other translocation types,
there is a lack of scientific approaches to evaluate the outcome of this management tool. We designed an experimental
translocation with two groups of translocated males and two of control males of a small (6-14 g) lizard (totaling 120
individuals). Our results suggest that translocated individuals covered longer distances (53 vs. 18 m) from their respective
release points in one month (on average), although this distance diminished over time. Displacing longer distances was
associated with a body condition impoverishment and an increase in parasitization by ectoparasites. To the best of our
knowledge, this is the first study that finds a positive relationship between covering longer distances and an increase in
the number of mites. This was also explained by the initial mite load that lizards had, suggesting that controlling the
infestation by mites is energetically demanding for lizards, being traded by locomotor activity. At least for those individuals
in poorer body condition, we recommend the implementation of soft release (gradually accustoming individuals to their new
environment by previously releasing them into controlled conditions) and deparasitization before accomplishing a mitigation-
driven translocation.
Keywords: corrective measures, environmental impact, habitat loss, homing behaviour, human development, Psammodromus
algirus, road ecology, translocation.
Introduction
Human activities like overexploitation, agricul-
tural development, urban expansion or infras-
tructure building currently threaten the survival
of three quarters of the 82 000 species assessed
by the International Union for Conservation
of Nature (Maxwell et al., 2016). The human
footprint will continue growing in the com-
ing decades, as global infrastructure network is
expected to continue its expansion in the com-
ing years (Laurance et al., 2014; Meijer et al.,
2018). Infrastructures can impact wildlife in
1 - Road Ecology Lab, Department of Biodiversity, Ecol-
ogy and Evolution, Faculty of Biology, Complutense
University of Madrid, Madrid, Spain
2 - School of Pharmacy, Department of Biomedicine and
Biotechnology, Universitdad de Alcalá (UAH), Parasi-
tology Area, A.P. 20 Campus Universitario, Alcalá de
Henares, E-28805, Madrid, Spain
3 - Functional Biodiversity (FBIO), CIBIO – Centro de
Investigação em Biodiversidade e Recursos Genéticos,
Universidade do Porto, Vairão, Portugal
Corresponding author; e-mail: rbarrientos@ucm.es
∗∗ORCID: https://orcid.org/0000-0002-1677-3214
∗∗∗Both authors contributed equally to this work
∗∗∗∗ORCID: https://orcid.org/0000-0003-1038-0468
many ways, like increasing accessibility to nat-
ural areas, triggering urban development, and
causing direct mortality or barrier effects (For-
man et al., 2003; van der Ree, Smith and Grilo,
2015).
Mitigation-driven translocations (i.e., mov-
ing animals away from the path of development
projects; also called short-distance transloca-
tions) attempt to reduce animal mortality and
to compensate habitat loss caused by human
activities as individuals are moved to new,
undisturbed areas (Germano et al., 2015). They
can involve species of any conservation sta-
tus (Germano et al., 2015). These projects
have traditionally responded to management
needs, and currently outnumber and receive
more funding than purely conservation-driven
translocations (Germano et al., 2015). How-
ever, the success of mitigation-driven translo-
cations is rarely monitored (but see Reinert
and Rupert, 1999; Sullivan, Kwiatkowski and
Chutt, 2004; Brown, Bishop and Brooks, 2009),
which implies that their benefits for conserva-
tion remain unclear to date (Germano et al.,
©Koninklijke Brill NV, Leiden, 2021. DOI:10.1163/15685381-bja10040
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2R. Barrientos, R. Megía-Palma
2015). Experimental approaches allow practi-
tioners to evaluate different aspects of translo-
cations in a scientifically rigorous manner (Tet-
zlaff, Sperry and DeGregorio, 2019), but only
a small set of carefully-designed studies have
allowed progress in evidence-based conserva-
tion (Germano and Bishop, 2009; Germano
et al., 2015; Taylor et al., 2017; Tetzlaff et
al., 2019). More studies focused on gaining
the knowledge needed to improve the success
of future translocations are needed to achieve
true evidence-based conservation (Tuberville et
al., 2005; Taylor et al., 2017). These studies
should incorporate experimental designs includ-
ing the use of controls, apriorihypothesis test-
ing or exploring advantages and disadvantages
of potential alternatives (e.g., Tuberville et al.,
2005; Taylor et al., 2017). One of the main dif-
ficulties that practitioners face before carrying
out a translocation, which is common to all taxa,
is precisely the lack of baseline information
on the parameters that determine establishment
success (Berger-Tal, Blumstein and Swaisgoo,
2020).
We assessed the impact of translocation on
males of a common Mediterranean lizard com-
pared to controls. We expected that transloca-
tion drives males to search for a new territory
in their novel habitat, while control individuals
remain in the same place where they were cap-
tured (and released). Consequently, we expect
that (i) translocated individuals move farther
distances from the release point than non-
translocated ones (Reinert and Rupert, 1999;
Sullivan et al., 2004; Tuberville et al., 2005;
Brown et al., 2009). This active search for
an empty territory will entail costs: (ii) a
short-term impoverishment of body condition
(Matthews, 2003); and, (iii) an increase in par-
asitization intensity by mites either by encoun-
tering more infested lizards during their search,
or by increasing their exposure to the mites that
are present on the ground and vegetation, and/or
by reduction of available energy resources to
fight parasite infestations because of increased
movement (Wu et al., 2019; Wieczorek et al.,
2020).
Material and methods
Study species and study area
Psammodromus algirus (Linnaeus, 1758) is a medium-sized
(snout-vent length, SVL, 60-80 mm; 6-14 g), short-lived (5
years) lizard, widespread in shrub and woodland Mediter-
ranean habitats from the Iberian Peninsula (Salvador, 2015).
It is considered an active forager with a territorial behav-
ior that tends to increase with age in males (Belliure et al.,
1996; Martín and López, 1999). Our study was located at
‘El Pardo’ (Spain; 40°31N, 03°47W; 650 m elevation),
a typical shrub-woodland Mediterranean area, where our
study species reaches high densities (up to 178 individ-
uals/ha, Salvador, 2015). During the breeding season of
2018 we sampled lizards in two separate areas >200 m
from each other, which is above the homing distance of
medium-sized lacertids (see Strijbosch, van Rooy and Voe-
senek, 1983). We focused on males to remove the likely
confounding effects of sex in the use of the space, which
is known to differ between males and females in lacertids
(e.g., Lewis and Saliva, 1987; Wieczorek et al., 2020). In
total, we sampled 120 adult males, 60 per area, that were
divided in 4 groups of 30 males. Two of these groups,
one per area, were translocated and reciprocally released
into the opposite area (i.e., ‘treatment’), and the remain-
ing two groups (also one per area), were released in their
original location (i.e., ‘control’). One of these areas was
adjacent (0-150 m) to a road (9,050 vehicles per day). We
captured (including recaptures) lizards during 18 sampling
days, between 24th of April and 27th of June. We extended
the recapture effort in 5 more sampling days until 6th of
July.
Sampling protocol
Lizards were collected by using a rod with a noose that
tightens around the neck of the lizards, a technique widely
used to catch lizards unharmed (e.g., Álvarez-Ruiz et al.,
2018). Males were carried to the lab in individual cotton
bags to collect additional data under controlled conditions.
Lizards were weighed with a digital balance to the nearest
centigram. The SVL of the lizards was measured with a ruler
to the nearest millimetre as a value of body size. The lizards
were toe-clipped and assigned an individual code. Being
fully aware that this is an invasive tagging, it is the one that,
in small lizards, produces less stress in the medium and long
term as evidenced by the methodological work of Langkilde
and Shine (2006). These authors concluded that the levels
of stress produced by toe-clipping in lizards would not be
different from those suffered by lizards in the wild due to
predation attempts (Langkilde and Shine, 2006). Because
P. algirus is a non-arboreal species, this marking does not
imply a reduction in its habitual behaviour, and it agrees
with the ethical premises of animal experimentation (Perry
et al., 2011), when necessary to carry out scientific studies
(Buchanan et al., 2012).
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Translocations costs for lizards 3
Distance moved
We measured the ‘distance moved’ as the Euclidean dis-
tance between the point where the individual was released
and the point where it was recaptured by using geo-
graphic information system. Recaptures in the first 14
days after the release were not included in our analy-
ses.
Body condition
We calculated a ‘body condition’ index as the residu-
als of the regression between log10-transformed values of
both body mass and body size (e.g., Dunlap and Mathies,
1993). We included the length of the tail in the regres-
sion because 61% of the lizards in our sample had regen-
erated tails and this fact can bias the relation between
body size and mass. Positive values of the body condition
index correspond to lizards being fatter than the sample
mean, and negative values are thinner lizards than aver-
age.
Quantification of mite parasitization
We counted ‘mites’ (ectoparasites) in the field immediately
after the lizards were captured (and recaptured) with a
magnifying (×10) glass (Álvarez-Ruiz et al., 2018). We
searched for parasites at the base of the tail because it is
the place where they concentrate the most (Álvarez-Ruiz et
al., 2018).
Statistical analyses
We compared the differences in elapsed days between cap-
ture and recapture between control and translocated individ-
uals with a two-way ANOVA where the interaction between
treatment and area was also considered. Distance moved
by the lizards was right skewed (most were small to me-
dium values) and best fitted a Gaussian model after its
log10-transformation. The rest of response variables did
fit well to Gaussian models without any transformation.
The parametric assumptions of normality, homoscedastic-
ity, skewness, and kurtosis were checked on the residual
errors of all the models. We carried out three analyses:
(i) ‘Distance moved’ (between the point where the indi-
vidual was released and the point where it was recap-
tured). We included as continuous explanatory predictors
‘body size’, ‘body condition’ and intensity of parasitiza-
tion by ‘mites’ at capture, ‘date’ of capture, and ‘elapsed
days’ between capture and recapture. As categorical pre-
dictors we included the treatment (control vs. translocated),
the area and their interaction; (ii) ‘Change in body con-
dition’ (the value at recapture minus the value at cap-
ture, corrected by tail size). We included as continuous
explanatory predictors ‘body size’, ‘initial body condition’
and intensity of parasitization by ‘mites’ at capture, ‘date’
of capture, ‘elapsed days’ between capture and recapture,
and ‘distance moved’ (log10 transformed). We included
the same categorical predictors and their interaction as
above; (iii) ‘Change in parasitization by mites’ (the value
at recapture minus the value at capture). We included as
continuous explanatory predictors ‘body size’, ‘body con-
dition’ and intensity of parasitization by ‘mites’ at cap-
ture, ‘date’ of capture, ‘elapsed days’ between capture and
recapture, and ‘distance moved’. We included the same
categorical predictors and their interaction as above. We
checked the multicollinearity of all the models by means
of the variance inflation factor (VIF), and also confirmed
the normality and the homoscedasticity of the model resid-
uals.
We applied a multimodel inference approach using the
R-package ‘MuMIn’ (Barton, 2013). For this, we consid-
ered sufficiently informative all the models with AICc
4 (Burnham and Anderson, 2004). We used model
averaging to obtain a final model and calculate the rela-
tive importance of each predictor. Only the models that
included the effect (i.e., conditional average) were con-
sidered to calculate the significance (α<0.05) of the
predictors and their z-standardized ß coefficient ±stan-
dard error. The resulting final models were cross-validated
using a k-fold split of 3 in the R-package ‘DAAG’
(Maindonald, Braun and Braun, 2015). Finally, we cal-
culated the percentage of the variance explained by each
significant predictor by means of their sum of squares.
Mean values ±their standard errors are presented here-
after.
Results
Distance moved
We recaptured 40 lizards (20 controls, 20
translocated). The elapsed days between capture
and recapture were 29.30 ±1.38, not differing
between treatment groups (F1, 36 =0.02, P=
0.87) or areas (F1, 36 =0.26, P=0.61), thus
confirming that sampling effort and likelihood
of recapture were similar between sampling
areas. Lizards moved between 3 and 325 meters
(mean ±SE =35.41 ±8.46 m). The multi-
model inference approach produced 16 likely
models for the distance moved (supplementary
table S1). The most important predictors were
the treatment (importance =0.96, ß =−0.15 ±
0.05; z =2.70, P=0.007), and the number
of elapsed days between capture and recapture
(importance =0.89, ß =0.02 ±6*103;z=
2.39, P=0.017). Thus, translocated lizards
moved longer distances shortly after release
(fig. 1a). Our results suggested a similar effect
of the experiment between areas (importance =
0.09, ß =−0.043 ±0.054; z =0.76, P=0.44)
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4R. Barrientos, R. Megía-Palma
(supplementary fig. S1). The cross-validation of
the final model reaffirmed the significant predic-
tors that had been suggested by the multimodel
inference approach (table 1).
Figure 1. Plots according to model averaging and cross-
validation (see table 1) showing the significant effect of the
translocation experiment on (a) the distance moved (F1, 37
=8.53, P=0.006) and (b) the change in body condition
(F1, 36 =4.16, P=0.048) of the males of Psammodromus
algirus. Box shows mean ±SE and whisker confidence
intervals (95%).
Change in body condition
Lizards tended to lose weight during the breed-
ing season as the mean value of change in
body condition (residual value) was negative
(0.00008 ±0.004). In terms of body mass
(grams), lizards lose in average 0.09 ±0.10
grams (mean 0.92% of the initial weight). The
multimodel inference approach produced 13
likely models (supplementary table S2) and sug-
gested that the translocation had a significant
effect on the change in body condition of the
lizards (importance =0.77, ß =7.25*103±
3.39*103;z=2.07, P=0.038). Thus, control
lizards improved their body condition (0.009 ±
0.005), whereas translocated ones impoverished
it (0.009 ±0.004) (fig. 1b). Indeed, the max-
imum weight lost by a lizard was 1.82 grams
(19.7% of its initial weight) in an individual
translocated close to the road. As well as in the
previous variable, the effect of the treatment was
independent of the area (importance =0.03,
ß=−1.87*103±3.15*103;z=0.57, P=
0.57) (supplementary fig. S1). Important predic-
tors for the change in body condition were the
number of elapsed days between capture and
recapture (importance =0.96, ß =1.12*103±
4.08*104;z=2.67, P=0.008), and the dis-
tance covered by the individuals (importance =
0.69, ß =−1.37*104±6.87*105;z=1.94,
P=0.053). The farther a lizard travelled,
Tab le 1. Cross-validation (k-fold =3) of the final model obtained by multimodel inference for log10-distance moved, change
in mite intensity, and change in body condition. Significant predictors are shown in bold (α=0.05). Sum of squares (SS) are
also shown.
Distance moved df F-value P-value SS % variance
Treatment 1 8.53 0.006 0.96 16.5
Elapsed days 1 5.94 0.019 0.67 11.5
Residuals 37 4.18 71.9
Change in body condition
Treatment 1 4.16 0.048 0.001 7.4
Elapsed days 1 8.05 0.007 0.003 14.2
Distance moved 1 8.23 0.007 0.003 14.6
Residuals 36 0.128 63.8
Change in parasitization by mites
Distance moved 1 7.54 0.009 1695 9.8
Mites_initial 1 32.38 <0.001 7281 42.1
Residuals 37 8318 48.1
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Translocations costs for lizards 5
Figure 2. Regression plots showing the relationship
between the distance moved by the lizards and the change
in (a) body condition, and (b) intensity of mite infestation
between capture and recapture.
the worse its body condition became (fig. 2a),
but the body condition improved over time.
The cross-validation of a model including these
three variables confirmed their significance as
predictors for the change in body condition
(table 1).
Change in parasitization by mites
The prevalence of haematophagus mites in
males of P. algirus from El Pardo was 95%
(114/120) at capture. The initial number of
mites was 19.94 ±1.34 per infested lizard. The
change in mite load ranged from 31 to 59
between captures. In general lizards tended to
increase their mite load since the mean change
was positive (10.12 ±3.33). The model averag-
ing approach produced 12 likely models (sup-
plementary table S3). The initial intensity of
mites was the best predictor for the change in
mite intensity (importance =1.00, ß =−1.10 ±
0.24; z =4.37, P=0.001), followed by the dis-
tance travelled (importance =0.95, ß =18.9 ±
7.01; z =2.60, P=0.009). Cross-validation of
a final model that included these two predictors
showed that lizards increased their mite inten-
sity when they moved longer distances (Fig-
ure 2b), but this increase was lower if they had
a higher number of mites at the beginning of the
treatment.
Discussion
We found increased movements in translocated
individuals, likely related to exploratory move-
ments in the search for a new territory. Our
results are consistent with telemetry-based stud-
ies of mitigation-driven translocations (e.g.,
Reinert and Rupert, 1999; Sullivan et al., 2004;
Tuberville et al., 2005; Brown et al., 2009).
This higher motor activity may imply costs
for translocated lizards, since they reduced
their body condition compared to controls. Fur-
thermore, we demonstrated for the first time
that mitigation-driven translocations increase
the intensity of parasitization by ectoparasites
(mites, in our case). The idea that the ectopar-
asite load might increase as a cost associated
with increased mobility has been frequently
suggested (e.g., Salvador et al., 1996; Wu
et al., 2019), and only recently demonstrated
with ticks (Wieczorek et al., 2020). How-
ever, whether ectoparasite load increases in the
lizards as a function of encounter rate between
lizards and ectoparasites provoked by the trav-
els of the host within their home range, or
if contrarily, ectoparasites can replicate within
the host as a direct trade-off between immune
and motor functions remains obscure. The first
seems likely for the case of hard ticks (i.e.,
fam. Ixodidae), which usually are heteroxe-
nous parasites that require infesting different
host taxa to complete their reproductive cycle
(Eisen et al., 2004). However, haematophagous
mites that infest P. algirus in El Pardo (Megía-
Palma, unpubl. data), are homoxenous, com-
pleting their whole reproductive cycle on the
lizards (Reichenow, 1920). Thus, the second
scenario of a mite load increase as a function
of energetic trade-offs in the host is more likely.
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6R. Barrientos, R. Megía-Palma
Translocated animals may face a more stress-
ful environment than controls (reviewed in Teix-
eira et al., 2007). In vertebrates, the activation
of the hypothalamic-pituitary axis in response
to stress increases both the mobilization of fat
reserves and the activity of the individual as a
survival response (Cote et al., 2006). Neverthe-
less, if food is not accessed because translocated
individuals still do not know the resource dis-
tribution in their new habitat or the individual
is facing a long-term stress, the allocation of
body fats to motor activity may be traded by the
energy allocated to immune defense (French et
al., 2007). In this sense, our data support that
the initial mite load was an important predictor
of mite load increase at recapture. This suggests
that mites may not increase in the lizards as the
encounter rate between lizards and new mites
increases, but instead as a function of the repli-
cation rate of mites on the lizards’ body. In sup-
port of this hypothesis, our preliminary experi-
ments of mites reared in captivity demonstrate
that new cohorts of mites hatch within only 3-4
days after the mother mites complete a blood-
meal (Megía-Palma, pers. obs.). This can multi-
ply mite loads on the lizards in only few days,
supporting our hypothesis and making biolog-
ical sense of the statistical results achieved in
this study. The important aspect of these obser-
vations is that the results of our translocation
experiment suggest that containing mite infes-
tation is energetically demanding for P. algirus
as their body condition decreases with the dis-
tance travelled, while mite load increases. Thus,
energy invested in exploration seems to be
traded by immune defense against mites. Our
results would, thus, suggest that translocated
lizards should be disinfested, as ectoparasite
infestation may entail costs for hosts as they
transmit hematic parasites and produce wounds
in the skin surface, which can also be associated
with mass loss (Smith et al., 2017; Megía-Palma
et al., 2020). Other effects of severe ectopara-
sitic infestations in small to mid-sized lizards
include alteration of the host’s thermoregulatory
behaviour (Megía-Palma et al., 2020), although
the latter was not tested in our study
The lack of differences in the average number
of days between capture and recapture both for
treatments and areas is consistent with the idea
that it was equally difficult to find and recap-
ture control or translocated males, and that there
were no differences between areas. It is possi-
ble that translocation effects are stronger due to
reduced survival, but we have no data in this
sense. However, given the symmetry in both
the time invested in re-sampling effort between
areas, and recapture ratio between treatment
groups, a differential survivorship due to the
soft translocation treatment is unlikely in the
short time. Whereas we found a negative influ-
ence of the number of elapsed days between
captures on distance covered, the former vari-
able was positively related to the change in
body condition. This is in line with the idea
that translocated lizards increased their motor
activity shortly after release, decreasing it after-
wards, when they found a new territory to set-
tle (Reinert and Rupert, 1999; Tuberville et
al., 2005). Consequently, whereas mass loss
is found in the short-term (Matthews, 2003),
when translocated individuals find a new terri-
tory, they manage to increase their body mass in
similar rates to control individuals (Reinert and
Rupert, 1999; Brown et al., 2009). Although we
are aware that we have not tested the survivor-
ship of lizards after soft translocation, based
on the results achieved, we recommend that
individuals with below-average body condition
should not be directly released in mitigation-
driven translocations, especially in short-lived
species, in which short-term body condition
impoverishment may have greater impact. Our
data are consistent with previous studies show-
ing that male lizards, in average, loss weight
during the reproductive season at low to mod-
erate rates (Abell, 2000). Alternatively, we sug-
gest that the implementation of soft releases
(which allow the animals a period to acclimate
to their new environment), at least for those
individuals in poorer body condition, could
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Translocations costs for lizards 7
minimize the costs of this management prac-
tice (e.g., Tuberville et al., 2005; Germano and
Bishop, 2009). This pre-release management is
designed so that animals in worse conditions
can gain body mass.
In summary, although translocation protocols
should be tailored to the target species and
their habitats, being based on a thorough under-
standing of the species’ biology and behaviour,
including a long-term post-translocation moni-
toring (Tuberville et al., 2005; Germano et al.,
2015), our study provides evidence that simu-
lated mitigation-driven translocations result in
increased exploratory behavior, decreased body
condition, and increased parasite loads in a
common lizard. If these issues are not taken
into account, the success of mitigation-driven
translocations may be compromised.
Acknowledgements. S. Reguera, C. Ponce, I. Pozo, M. Fer-
nández, Z. Rohrer, C. Luque and P. Quiles helped with the
field work. Z. Rohrer reviewed the language of the final ver-
sion. Two anonymous reviewers improved a first draft. Han-
dling protocols, as well as the general ethics of our research
were approved by the ethic committee of University Com-
plutense de Madrid (Ref. 5005), and by Comunidad de
Madrid, Consejería de Medio Ambiente, Ordenación del
Territorio y Sostenibilidad (Ref. 10/165944.9/18, PROEX
271/19) in accordance with current Spanish laws. RB
enjoyed a postdoctoral grant from Comunidad de Madrid
(2018T1/AMB10374), and RMP a postdoctoral contract by
ICETA – Instituto de Ciências, Tecnologias e Agroambiente
da Universidade do Porto and Fundação da Ciência e Tec-
nologia.
Supplementary material. Supplementary material is avail-
able online at:
https://doi.org/10.6084/m9.figshare.14332955
References
Abell, A.J. (2000): Costs of reproduction in male lizards,
Sceloporus virgatus.Oikos88: 630-640.
Álvarez-Ruiz, L., Megía-Palma, R., Reguera, S., Ruiz, S.,
Zamora-Camacho, F.J., Figuerola, J., Moreno-Rueda, G.
(2018): Opposed elevational variation in prevalence and
intensity of endoparasites and their vectors in a lizard.
Curr. Zool. 64: 197-204.
Barton, K. (2018): MuMIn: Multi-Model Inference.
R package version 1.40.4. https://CRAN.R-project.org/
package=MuMIn.
Belliure, J., Carrascal, L.M., Diaz, J.A. (1996): Covariation
of thermal biology and foraging mode in two Mediter-
ranean lacertid lizards. Ecology 77: 1163-1173.
Berger-Tal, O., Blumstein, D.T., Swaisgood, R.R. (2020):
Conservation translocations: a review of common dif-
ficulties and promising directions. Anim. Conserv. 23:
121-131.
Brown, J.R., Bishop, C.A., Brooks, R.J. (2009): Effective-
ness of short-distance translocation and its effects on
western rattlesnakes. J. Wildlife Manage. 73: 419-425.
Buchanan, K. (2012): Guidelines for the treatment of ani-
mals in behavioural research and teaching. Anim. Behav.
83: 301-309.
Burnham, K.P., Anderson, D.R. (2004): Multimodel infer-
ence, understanding AIC and BIC in model selection.
Sociol. Methods. Res. 33: 261-304.
Cote, J., Clobert, J., Meylan, S., Fitze, P.S. (2006): Exper-
imental enhancement of corticosterone levels positively
affects subsequent male survival. Horm. Behav. 49: 320-
327.
Dunlap, K.D., Mathies, T. (1993): Effects of nymphal ticks
and their interaction with malaria on the physiology of
male fence lizards. Copeia 1993: 1045-1048.
Eisen, L., Eisen, R.J., Lane, R.S. (2004): The roles of birds,
lizards, and rodents as hosts for the western black-legged
tick Ixodes pacificus.J.VectorEcol.29: 295-308.
Forman, R.T.T., Sperling, D., Bissonette, J.A., Clevenger,
A.P., Cutshall, C.D., Dale, V.H., Fahrig, L., France,
R., Goldman, C.R., Heanue, K., Jones, J.A., Swanson,
F.J., Turrentine, T., Winter, T.C. (2003): Road Ecology:
Science and Solutions. Island Press, Covelo and London.
French, S.S., McLemore, R., Vernon, B., Johnston, G.I.,
Moore, M.C. (2007): Corticosterone modulation of
reproductive and immune systems trade-offs in female
tree lizards: long-term corticosterone manipulations via
injectable gelling material. J. Exp. Biol. 210: 2859-2865.
Germano, J.M., Bishop, P.J. (2009): Suitability of amphib-
ians and reptiles for translocation. Conserv. Biol. 23:
7-15.
Germano, J.M., Field, K.J., Griffiths, R.A., Culow, S., Fos-
ter, J., Harding, G., Swaisgood, R.R. (2015): Mitigation-
driven translocations: are we moving wildlife in the right
direction? Front. Ecol. Environ. 13: 100-105.
Langkilde, T., Shine, R. (2006): How much stress do
researchers inflict on their study animals? A case study
using a scincid lizard, Eulamprus heatwolei. J. Exp.
Biol. 209: 1035-1043.
Laurance, W.F., Clements, R.G., Sloan, S., O’Connell, C.S.,
Mueller, N.D., Goosem, M., Venter, O., Edwards, D.P.,
Phalan, B., Balmford, A., van Der Ree, R., Burgues
Arrea, I. (2014): A global strategy for road building.
Nature 513: 229-232.
Lewis, A.R., Saliva, J.E. (1987): Effects of sex and size on
home range, dominance, and activity budgets in Ameiva
exsul (Lacertilia: Teiidae). Herpetologica 43: 374-383.
Maindonald, J.H., Braun, W.J., Braun, M.W.J. (2015): Pack-
age ‘DAAG’. Data Analysis and Graphics Data and
Functions.
Martín, J., López, P. (1999): Nuptial coloration and mate
guarding affect escape decisions of male lizards Psam-
modromus algirus. Ethology 105: 439-447.
Downloaded from Brill.com04/07/2021 11:20:59AM
via free access
8R. Barrientos, R. Megía-Palma
Matthews, K.R. (2003): Response of mountain yellow-
legged frogs, Rana muscosa, to short distance translo-
cation. J. Herpetol. 37: 621-626.
Maxwell, S.L., Fuller, R.A., Brooks, T.M., Watson, J.E.M.
(2016): The ravages of guns, nets and bulldozers. Nature
536: 143-145.
Megía-Palma, R., Paranjpe, D., Blaimont, P., Cooper, R.,
Sinervo, B. (2020): To cool or not to cool? Intestinal coc-
cidians disrupt the behavioural hypothermia of lizards in
response to tick infestation. Ticks Tick-borne Dis. 11:
101275.
Meijer, J.R., Huijbregts, M.A.J., Schotten, K.C.G.J., Schip-
per, A.M. (2018): Global patterns of current and future
road infrastructure. Environ. Res. Lett. 13: 604006.
Perry, G., Wallace, M.C., Perry, D., Curzer, H., Muhlberger,
P. (2011): Toe clipping of amphibians and reptiles: sci-
ence, ethics, and the law. J. Herpetol. 45: 547-555.
Reichenow, E.(1920): Los Hemococcidios de los lacértidos:
estudio del desarrollo de karyolysus: observaciones pre-
vias y 1a parte: estudio y desarrollo de Karyolysus.
Imprenta y Librería de Nicolás Moya.
Reinert, H.K., Rupert, R.R. (1999): Impact of translocation
on behavior and survival of timber rattlesnake, Crotalus
horridus. J. Herpetol. 33: 45-61.
Salvador, A., Veiga, J.P., Martín, J., López, P., Abelenda,
M., Puerta, M. (1996): The cost of producing a sexual
signal: testosterone increases the susceptibility of male
lizards to ectoparasitic infestation. Behav. Ecol. 7: 145-
150.
Salvador, A. (2015): Lagartija Colilarga – Psammodro-
mus algirus in Enciclopedia Virtual de los Vertebra-
dos Españoles. Salvador A., Marco A., Eds. Museo
Nacional de Ciencias Naturales, Madrid. Available from
http://www.vertebradosibericos.org/ (Accessed 9th Oc-
tober 2020).
Smith, G.D., Neuman-Lee, L.A., Webb, A.C., Angilletta,
M.J., DeNardo, D.F., French, S.S. (2017): Metabolic
responses to different immune challenges and varying
resource availability in the side-blotched lizard (Uta
stansburiana). J. Comp. Physiol. B 187: 1173-1182.
Strijbosch, H., van Rooy, P.T.J., Voesenek, L.A.C.J.
(1983): Homing behaviour of Lacerta agilis and Lac-
erta vivipara (Sauria, Lacertidae). Amphibia-Reptilia 4:
43-47.
Sullivan, B.K., Kwiatkowski, M.A., Chutt, G.W. (2004):
Translocation of urban Gila Monsters: a problematic
conservation tool. Biol. Conserv. 117: 235-242.
Taylor, G., Canessa, S., Clarke, R.H., Ingwersen, D., Arm-
strong, D.P., Seddon, P.J., Ewen, J.G. (2017): Is rein-
troduction biology an effective applied science? Trends
Ecol. Evol. 32: 873-880.
Teixeira, C.P., De Azevedo, C.S., Mendl, M., Cipreste, C.F.,
Young, R.J. (2007): Revisiting translocation and rein-
troduction programmes: the importance of considering
stress. Anim. Behav. 73: 1-13.
Tetzlaff, S.J., Sperry, J.H., DeGregorio, B.A. (2019): Effects
of antipredator training, environmental enrichment, and
soft release on wildlife translocations: a review and
meta-analysis. Biol. Conserv. 236: 324-331.
Tuberville, T.D., Clark, E.E., Buhlmann, K.A., Gibbons,
J.W. (2005): Translocation as a conservation tool: site
fidelity and movement of repatriated gopher tortoises
(Gopherus polyphemus). Anim. Conserv. 8: 349-358.
van der Ree, R., Smith, D.J., Grilo, C., Eds (2015): Hand-
book of Road Ecology. John Wiley and Sons, Chichester.
Wieczorek, M., Rektor, R., Najbar, B., Morelli, F. (2020):
Tick parasitism is associated with home range area in the
sand lizard, Lacerta agilis. Amphibia-Reptilia 1: 1-10.
Wu, Q., Richard, M., Rutschmann, A., Miles, D.B., Clobert,
J. (2019): Environmental variation mediates the preva-
lence and co-occurrence of parasites in the common
lizard, Zootoca vivipara. BMC Ecology 19: 44.
Submitted: May 1, 2020. Final revision received:
December 2, 2020. Accepted: December 2, 2020.
Associate Editor: Sylvain Dubey.
Downloaded from Brill.com04/07/2021 11:20:59AM
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... extreme heat waves, Dupoué et al., 2018). We hypothesize that the increased activity associated with the release of glucocorticoids may also favor exposure of lizards to questing ectoparasites (Wieczorek et al., 2020;Barrientos and Megía-Palma, 2021;Smolinský et al., 2021). Thus, both glucocorticoids and parasites can be interpreted as biomarkers of increased activity associated with environmental stress in lizards (Oppliger et al., 1998;Josserand et al., 2017;Kechnebbou et al., 2019;Tylan et al., 2020). ...
... This is a typical road-effect zone, with increased human pressure (high numbers of walkers, cyclers, pickers) with a lower cover of ground level vegetation, gramineous plants, and bushes (Supplementary Materials), transforming it into a low quality habitat for our study species (Carrascal et al., 1989). The second area, placed on the surrounding hills, was 7.9 ha and ranged between 350 and 550 m from the road (Barrientos and Megía-Palma, 2021). This left a 200-m band between both sampling plots. ...
... The size of the smallest of our sampling plots exceeded by approximately 75 times the maximum home range size described for the species, which is 0.09 ha (Díaz, 1993). Moreover, in a previous translocation capture-recapture experiment in the same population, control lizards (not translocated) travelled on average 18 m linear distance in a period of four weeks (Barrientos and Megía-Palma, 2021). Therefore, there was a high likelihood that only a few lizards, if any, moved between sampling plots and thus, ectoparasites and fecal glucocorticoid metabolites do reflect conditions of the plot where lizards were actually captured. ...
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Wildlife translocations can have conservation value but results have been mixed regarding animal behavior and survival post-release. Practitioners have adopted antipredator training, environmental enrichment, and soft release as pre-release conditioning tactics to encourage adaptive behavior and improve post-release survival, but their utility has not been broadly quantified. We performed a formal literature review and conducted meta-analysis on 108 effects from 41 studies experimentally testing how these tactics affected survival, movement, or site fidelity compared to unconditioned animals. We further investigated how each conditioning tactic, animal source (wild-to-wild translocated or captive-released), age, and taxonomic group (birds, fish, mammals, and reptiles) influenced outcomes. Relative to unconditioned animals, conditioned individuals were 1.5 times more likely to survive, had reduced movement, and were three times more likely to show site fidelity. Each of the three conditioning tactics resulted in improved survival. Juveniles released from captivity derived the greatest survival benefit from conditioning. Across taxa, conditioning most benefitted survival of fish. Conditioning also had positive effects on survival of mammals and reptiles, albeit with less certainty than for fish. Estimates comparing survival of conditioned to unconditioned birds were much more variable, suggesting avian translocation programs using conditioning generally need improvement. Soft release consistently reduced movement and increased site fidelity; this was an especially viable technique for adult wild-to-wild translocated animals. We provide quantitative evidence that behavioral conditioning can aid wildlife translocations, and we encourage continued experiments to further elucidate how refined tactics could advance conservation efforts using translocation as a management tool.
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Reintroduction biology is a field of scientific research that aims to inform translocations of endangered species. We review two decades of published literature to evaluate whether reintroduction science is evolving in its decision-support role, as called for by advocates of evidence-based conservation. Reintroduction research increasingly addresses a priori hypotheses, but remains largely focused on short-term population establishment. Similarly, studies that directly assist decisions by explicitly comparing alternative management actions remain a minority. A small set of case studies demonstrate full integration of research in the reintroduction decision process. We encourage the use of tools that embed research in decision-making, particularly the explicit consideration of multiple management alternatives because this is the crux of any management decisions.
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Ameiva exsul, a widely foraging non-territorial lizard, was studied in Mayaguez, Puerto Rico. Average home range area for males significantly exceeded that for females, but males were larger than females. With the effect of body size removed statistically, there was no intersexual difference in home range area even though males engaged in significantly more non-foraging walking than females. The dominance hierarchy was size-based and independent of sex. Proportion of time spent basking was the same for 3 size classes. Digging and feeding were significantly correlated in large lizards and independent in small lizards. -from Authors