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.
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,
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,
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.,
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
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-
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-
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-
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-
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
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-
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Submitted: May 1, 2020. Final revision received:
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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. ...
Differences between air and ground temperatures are expected to narrow with the advance of the season in temperate regions (aka seasonal restriction in the availability of thermal microhabitats), which may activate behavioral and physiological responses of ectotherm species adapted to temperate climates. However, according to cost-benefit models of ectotherm thermoregulation, we hypothesize that these responses may also carry some costs. We quantified seasonal shifts in thermoregulatory precision, concentration of fecal glucocorticoid metabolites, and load of ectoparasites in a Mediterranean lizard, Psammodromus algirus. We also tested whether the proximity to a road, a putative source of chronic stress, can facilitate the glucocorticoid-mediated response of lizards to heat stress. As expected, differences between body and environmental temperatures narrowed during the reproductive season and lizards responded by increasing their thermoregulatory precision and the secretion of glucocorticoids, as indicated by metabolites in feces. Interestingly, lizards tended to have higher glucocorticoid concentration when captured far from the road. This might reflect either a putative impairment of the glucocorticoid-mediated response of the lizards to heat stress close to the road or the plastic capability of P. algirus to acclimate to sources of moderate chronic stress. In the latter direction, the increase of both glucocorticoid metabolites and thermoregulatory precision supported that this Mediterranean species responds to environmental thermal restrictions with adaptive behavioral and physiological mechanisms. However, this was also associated with an increase in its susceptibility to ectoparasites, which represents an added cost to the current cost-benefit models of ectotherm thermoregulation.
... Mites of the genus Ophionyssus (Acari: Macronyssidae) were counted using a magnifying glass (× 10) in the field immediately after capture. This was done by checking the base of the tail, the interscale spaces in the belly of the lizards, as well as the tympani, and the mite pockets (Salvador et al. 1999;Barrientos and Megía-Palma 2021;Megía-Palma et al. 2022). In addition, we collected blood samples from the tail using sterile needles (Megía-Palma et al. 2016a). ...
... We analysed if body length, body condition, and SCD are important traits that can explain the distance travelled by the lizards between captures. We controlled this analysis by adding the translocation treatment, the plot, and the number of elapsed days between captures (see Barrientos and Megía-Palma et al. 2021). ...
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Ontogeny is expected to be a determinant factor affecting production of colour patches in lizards, while immune challenges or sudden weight loss may impair the maintenance of pigment-based coloration within a breeding season. We translocated males of the lizard Psammodromus algirus between two sampling plots that differed in distance to a road, vegetation structure, and predator abundance. We analysed variation in spectral reflectance of their colour patches the same and the following year. The change in the reflectance of the lizard colour patches within the first breeding season was explained by the interaction between plot and treatment, but not body condition. The maintenance of the breeding coloration was impaired only in those males translocated close to the road, probably reflecting that it is a poor-quality habitat for P. algirus . The following year, lizards that produced a more elaborate coloration were those that increased their body condition and controlled some parasitic infections, although suffered an increase of others. This study shows that colour patch production is plastic in P. algirus . Lizards increasing parasites or losing weight reduced pigmentation, although habitat quality can cushion these negative effects on pigmentation. However, not all parasites constrain the investment in coloration. In fact, some increased in those lizards that allocated more pigments to colour patches. In conclusion, longitudinal studies following experimental manipulation can contribute to understand pigment allocation rules in lizards. Significance statement Pigments involved in colour patches of animals are limiting resources that can be reallocated off the skin to other functions. However, longitudinal evidence of this phenomenon is scarce in reptiles. We designed a manipulative mark-recapture experiment to investigate effects of habitat and parasitic infections on colour patch maintenance (within-year variation) and production (between-year variation) in male free-ranging lizards that were reciprocally translocated between two patches of habitat that differed in quality. During the first year, lizards translocated to the habitat with more predators and worse vegetation impoverished their coloration, while lizards translocated to the more favourable habitat maintained it despite all translocated lizards loose body condition. The next year we detected different effects on the coloration of three different parasites investigated, suggesting that coloration can reflect the virulence of the infections.
... Accordingly, expect higher prevalence would be expected in P. muralis, which is contrary to the presented findings. Moreover, differences in parasite intensity are governed by different factors, among them by the susceptibility and potential to fight of the parasites (immune competence) of the host (Oppliger et al., 1998) and immune competency to fight off infections requires energy allocation (Barrientos and Megía-Palma, 2021). It is known that the two species differ in their metabolic potential activity (Ţagar et al., 2015c), which is an estimation of enzymatic capacity for metabolism (G. ...
... These results were similar to some other findings in lizards (e.g. Álvarez-Ruiz et al., 2018, Arakelyan et al., 2019 and could be due to behavioral differences between sexes, with males exhibiting riskier behavior, thus encountering more parasite vectors and infected conspecifics (Zuk & McKean, 1996;Barrientos and Megía-Palma, 2021). Besides that, male lacertids have larger home ranges, which will make them more exposed to parasite vectors (Wieczorek et al., 2020. ...
In parasite-host interactions host species may differ in their ability to fight parasitic infections, while other ecological interactions, including competition, may differentially alter their physiological state, making them even more susceptible to parasites. In this study, we analyze the haemogregarine blood parasites infecting two competing lizard species, Iberolacerta horvathi and Podarcis muralis, and explore host—parasite relationships under different host competition scenarios. Both species were infected with haemogregarine parasites belonging to the genus Karyolysus. Using the 18S rRNA gene, six new Karyolysus haplotypes were identified clustering with other Central and Eastern European samples, and widely shared between both lizard hosts. Haemogregarine infections were detected at all sampled sites with over 50% of individuals parasitized. Overall, I. horvathi was more frequently and also more intensely parasitized than P. muralis, with higher infection rates observed in syntopy. Males of both species tended to be more frequently infected and showed a higher infection intensity than conspecific females. The results suggest that parasitisation by haemogregarines may be relevant in the dynamics of the competitive relationship between these lizard species. More studies, including immunological response analysis, and the identification of the vectors are needed to better understand host-parasite relationships and competition.
... Increased parasitism of male lizards as compared to females has been documented previously in other lizard species (Salvador et al., 1996;Václav, Prokop and Fekiač, 2007;Wu et al., 2019), including those of the genus Podarcis (Biaggini, Berti and Corti, 2009). Among male lizards, the effects of elevated levels of testosterone, increased activity levels, and control of larger home ranges may interact to produce the differential parasite infestation often observed between sexes (Salvador et al., 1996;Wieczorek et al., 2020;Barrientos et al., 2021). Additionally, intensity of infection by parasites may fluctuate seasonally for certain sexes (Amo, López, and Martín, 2005;Cox and John-Alder, 2007;Lumbad, Vredevoe, and Taylor, 2011;Tomassone et al., 2017). ...
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Intraspecific colour morphs usually differ in more traits than just colour. These traits can manifest as differences in morph physiology, behaviour, and ecology. Ecological differences among colour morphs, such as the degree of parasitism, can influence the evolution, maintenance, and loss of morphs from populations. High ectoparasite load can directly and deleteriously impact host fitness, and thus could influence colour morph persistence in populations if certain morphs are more frequently exposed to parasites or are more susceptible to parasitism. The Aegean wall lizard, Podarcis erhardii , is a colour polymorphic island lizard that is parasitized externally by ticks and mites. These ectoparasites can affect aspects of host lizard behaviour and physiology – including thermoregulation and body mass – and therefore are an important factor influencing the ecology and fitness of P. erhardii . We find that among sympatric colour morphs, ectoparasite loads differ; namely, monochromatic orange morphs have the highest numbers of ectoparasites, and in general, morphs with orange alleles (orange, orange-white, and orange-yellow) are more heavily parasitized by ticks and mites than the other morphs. Our results indicate that morphs with orange alleles tend to occupy microhabitats with significantly more vegetation cover and thus may increase their exposure to ticks and mites. Ecological differences between morphs could be an important factor contributing to demonstrated patterns of orange morph rarity and loss in P. erhardii populations.
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We present the first study that compares phenological variation in parasite load and inflammatory response in a lizard with asynchronous male and female gonadal cycles. Other studies have used many species with seasonal and synchronous reproductive cycles, in which it is difficult to decouple the effects of internal and external factors that can affect parasite abundance in each sex. Species with asynchronous reproductive cycles provide the opportunity to study the effects of seasonality and reproductive condition separately, but few studies have documented variation in parasite abundance in these species. We made an extensive comparison of parasite load and inflammatory response of the lizard Sceloporus torquatus, a species with asynchronous reproductive cycles, throughout its active period. We hypothesized that the parasite load would be higher in the period of maximum gonadal activity for each sex, negatively related to body condition and inflammatory response. Our results partially support the hypothesis; males had more parasites in summer than in spring and autumn, while females had more parasites in spring and summer than in autumn; however, we do not find a relationship between parasite load, body condition and inflammatory response. Our results indicated that host-parasite interactions are complex and depend upon both environmental and internal factors. Therefore, longer-term studies may provide a more comprehensive picture of host-parasite dynamics in populations of wild lizards.
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Ectotherms are vulnerable to environmental changes and their parasites are biological indicators of their health. Thus, parasite load in ectotherms is expected to show a marked phenology consistent with seasonal changes in the environment. The present study investigates temporal host-parasite dynamics in a lizard community in the Eastern Iberian Peninsula during an entire annual activity period. The host species investigated were Acanthodactylus erythrurus, Psammodromus algirus, and Psammodromus edwardsianus, three lizard species coexisting in a mixed habitat of forests and dunes, providing a range of body sizes, ecological requirements and life history traits. Habitat and climate were considered as potential environmental predictors of parasite abundance, while size, body condition, and sex were considered as intrinsic predictors. Linear models based on robust estimates were fitted to analyse parasite abundance and prevalence. Ectoparasitic haematophagous mites and blood parasites from two genera of haemococcidians were found: Lankesterella spp. and Schellackia spp. The former genus was almost exclusively infecting A. erythrurus, while Schellackia spp. infected the three host species. Habitat type was the only predictor that explained the abundance of all parasites, being mostly higher in the forest than in the dunes except for mites in P. algirus. Besides habitat, different predictors significantly explained different parasites, suggesting that particularities in each host-parasite relationship should be accounted even when parasites infect close-related hosts under the same environmental pressures. Our results support the concept that parasites of lizards can be biomarkers of environmental perturbation, but direction of relationships need to be carefully interpreted for each host-parasite assemblage.
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Background: Hosts and their parasites are under reciprocal selection, leading to coevolution. However, parasites depend not only on a host, but also on the host's environment. In addition, a single host species is rarely infested by a single species of parasite and often supports multiple species (i.e., multi-infestation). Although the arms race between a parasite and its host has been well studied, few data are available on how environmental conditions may influence the process leading to multiple infestations. In this study, we examine whether: (1) environmental factors including altitude, temperature, vegetation cover, human disturbance, and grazing by livestock affect the prevalence of two types of ectoparasites, mites and ticks, on their host (the common lizard, Zootoca vivipara) and (2) competition is evident between mites and ticks. Results: We found the probability of mite infestation increased with altitude and vegetation cover, but decreased with human disturbance and presence of livestock. In contrast, the probability of tick infestation was inversely associated with the same factors. Individuals with low body condition and males had higher mite loads. However, this pattern was not evident for tick loads. The results from a structural equation model revealed that mites and ticks indirectly and negatively affected each other's infestation probability through an interaction involving the environmental context. We detected a direct negative association between mites and ticks only when considering estimates of parasite load. This suggests that both mites and ticks could attach to the same host, but once they start to accumulate, only one of them takes advantage. Conclusion: The environment of hosts has a strong effect on infestation probabilities and parasite loads of mites and ticks. Autecological differences between mites and ticks, as indicated by their opposing patterns along environmental gradients, may explain the pattern of weak contemporary interspecific competition. Our findings emphasize the importance of including environmental factors and the natural history of each parasite species in studies of host-parasite coevolution.
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It is generally accepted that parasites exert negative effects on their hosts and that natural selection favors specific host responses that mitigate this impact. It is also known that some components of the host immune system often co-evolve with parasite antigens resulting in a host-parasite arms race. In addition to immunological components of the anti-parasitic response, host behavioral responses are also important in this arms race and natural selection may favor avoidance strategies that preclude contact with parasites, or shifts in the host’s thermoregulatory strategy to combat active infections (e.g., behavioral fever). Ticks are widespread parasites with direct and indirect costs on their vertebrate hosts. Their saliva provokes hemolysis in the blood of their hosts and can transmit a plethora of tick-borne pathogens. We enquired whether tick infestation by Ixodes pacificus can provoke a thermoregulatory response in Sceloporus occidentalis. For this, we compared the thermoregulatory behavior of tick-infested lizards against tick-infested lizards co-infected with two different species of coccidians (Lankesterella occidentalis and Acroeimeria sceloporis). After this, lizards were kept in individual terraria with a basking spot and fed ad libitum. We found that tick-infested lizards sought cooler temperatures in proportion to their tick load, and this response was independent of the co-infection status by L. occidentalis. This was consistent in April and June (when tick loads were significantly lower) and suggests a conservative strategy to save energy which might have been selected to overcome tick infestations during phenological peaks of this parasite. However, this behavior was not observed in lizards co-infected with A. sceloporis, suggesting that co-infection with this intestinal parasite prompt lizards to be active. Cost of tick infestation was confirmed because housed lizards lost weight at a constant ratio to initial tick load, independently of other infections. The broader implications of these findings are discussed in the context of climate change.
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Translocations are a common conservation and management strategy, but despite their popularity, translocations are a high‐cost endeavor with a history of failures. It is therefore imperative to maximize their success by learning from our collective experience. The Global Re‐introduction Perspectives Series is a collection of conservation translocation case studies, generated by the IUCN’s Conservation Translocation Specialist Group, and presented in a structured format with an emphasis on practical information. All 293 animal translocation case studies to date include a section in which the authors list the difficulties they have faced during the translocation project, with over 1200 difficulties described so far. We reviewed all difficulties reported in the series to get insights into the common perceived difficulties faced by wildlife managers during animal translocations. The most reported‐upon problems had to do with animal behavior, followed by monitoring difficulties, lack of funding, quality of release habitat, lack of baseline knowledge and lack of public support. We scrutinized each of these difficulties to highlight future research directions that are most likely to improve translocation success, and put a special emphasis on difficulties stemming from animal behavior, and on solutions that may alleviate these problems and improve conservation translocation success world‐wide. Conservation translocations are still a high‐cost endeavor with a history of failures. We reviewed over 1200 perceived difficulties reported by managers as part of the Global Re‐introduction Perspectives Series, published by the IUCN’s Conservation Translocation Specialist Group. We found that the most reported upon difficulties had to do with various aspects of animal behavior, followed by monitoring difficulties, lack of funding, quality of release habitat, lack of baseline knowledge and lack of public support. Learning from past difficulties and obstacles will ensure that every new translocation project will have a better chance of succeeding than the ones preceding it. In the picture: a burrowing bettong Bettongia lesueur, a notoriously difficult species to translocate, with a history of many failed attempts. The picture was taken by Dr. Hannah Bannister.
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Georeferenced information on road infrastructure is essential for spatial planning, socio-economic assessments and environmental impact analyses. Yet current global road maps are typically outdated or characterized by spatial bias in coverage. In the Global Roads Inventory Project we gathered, harmonized and integrated nearly 60 geospatial datasets on road infrastructure into a global roads dataset. The resulting dataset covers 222 countries and includes over 21 million km of roads, which is two to three times the total length in the currently best available country-based global roads datasets. We then related total road length per country to country area, population density, GDP and OECD membership, resulting in a regression model with adjusted R 2 of 0.90, and found that that the highest road densities are associated with densely populated and wealthier countries. Applying our regression model to future population densities and GDP estimates from the Shared Socioeconomic Pathway (SSP) scenarios, we obtained a tentative estimate of 3.0–4.7 million km additional road length for the year 2050. Large increases in road length were projected for developing nations in some of the world's last remaining wilderness areas, such as the Amazon, the Congo basin and New Guinea. This highlights the need for accurate spatial road datasets to underpin strategic spatial planning in order to reduce the impacts of roads in remaining pristine ecosystems.
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Studying the causes of parasite geographic distribution is relevant to understand ecological and evolutionary processes that affect host populations as well as for species conservation. Temperature is one of the most important environmental variables affecting parasite distribution, as raising temperatures positively affect development, reproduction, and rate of transmission of both endo- and ectoparasites. In this context, it is generally accepted that, in mountains, parasite abundance decreases with elevation. However, empirical evidence on this topic is limited. In the present study, we analysed the elevational variation of haemoparasites and ectoparasites of a lizard, Psammodromus algirus, along a 2200-m elevational gradient in Sierra Nevada (SE Spain). As predicted, ectoparasite (mites, ticks, mosquitoes, and sandflies) abundance decreased with elevation. However, haemoparasite prevalence and intensity in the lizard augmented with altitude, showing a pattern contrary to their vectors (mites). We suggest that tolerance to haemoparasites may increase with elevation as a consequence of lizards at high altitudes taking advantage of increased body condition and food availability, and reduced oxidative stress. Moreover, lizards could have been selected for higher resistance against haemoparasites at lowlands (where higher rates of replication are expected), thus reducing haemoparasite prevalence and load. Our findings imply that, in a scenario of climate warming, populations of lizards at high elevation may face increased abundance of ectoparasites, with accompanied strong negative effects.
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The energetic cost of immunity depends on many factors, including the type of challenge, the timing of the response, and the state of the animal. We measured changes in the standard metabolic rates of side-blotched lizards (Uta stansburiana Baird and Girard, 1852) in response to different immune challenges and nutritional states. In the first experiment, lizards were randomly assigned to one of four treatments: lipopolysaccharide (LPS) injection (to stimulate the response to a pathogen), cutaneous biopsy (as a proxy to a superficial wound), both injection and biopsy, or neither (control). Four and five days later, we measured the standard metabolic rates of the lizards. In response to healing a cutaneous wound, lizards reduced metabolic rate and lost body mass. Healing rate was also inversely related to weight loss, but LPS had no effect on body mass or metabolic rate. In the second experiment, a new set of lizards were randomly assigned to a high-food or low-food diet and administered a cutaneous biopsy. As in the first experiment, we observed a reduction in metabolic rate after wounding; moreover, this decrease was positively correlated with the rate of healing. We observed higher rates of metabolism in lizards that ate more food, but food consumption was unrelated to the decrease in metabolic rate following the biopsy. These experiments demonstrate the dynamic nature of the immune response in response to immune challenge and the state of the organism.
The sand lizard (Lacerta agilis) is a common species in Europe that inhabits a wide range of habitats, including anthropogenic environments. It is a frequent carrier of common ticks (Ixodes ricinus), which poses a severe threat to the lizards' health. We determined the living space used by lizards in a rapidly changing environment and ascertained the number of parasitic ticks found throughout the reptile's active season. We conducted telemetry research on a dynamically developing housing estate located on the outskirts of the city of Zielona Góra (western Poland) in 2016-2017. We obtained data from 16 adult lizards, from which we collected 2529 ticks. Using generalized linear models (GLMs), we determined the relationships among the number of transmitted parasites, size of occupied areas (minimum convex polygon, MCP), the weight of lizards, and sex of lizards. Results indicated that the number of ticks was negatively correlated with lizard body mass, but positively correlated with home range. Sex was not significantly associated with the number of ticks. Additionally, the parasite load was lower during the lizard's non-breeding season than during the breeding season and was lower for males than for females during the non-breeding season. Males have larger home ranges than females.
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.
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.
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