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A B S T R A C T
Article history:
important tool for the population management of endangered species. Whilst experimen-
tal field manipulations are important in determining optimal rehabilitation and transloca-
20 December 2005
tion strategies, they are rarely implemented in practice. We used an experimental approach
to examine the effects of translocation on post-release survival and behaviour, and the
impact of introductions on the recipient wild population, using the European hedgehog
(Erinaceus europaeus), the most common mammal admitted to British wildlife hospitals.
Keywords:
The post-release survival and behaviour of five groups were compared: three different
Rehabilitation
translocation treatments, one wild population at the release sites and one control wild pop-
Translocation
ulation away from the release sites. Individuals that were held in captivity prior to translo-
Post-release survival
cation had a better survival rate on release than individuals that were translocated with a
Hedgehogs
minimum time spent in captivity. We suggest that temporary captivity improves chances of
Stress
survival by allowing the build up of fat reserves and reducing manipulation stress suffered
on release. No evidence was found for intra-specific competition between introduced individuals and the recipient wild hedgehog population.
2006 Elsevier Ltd. All rights reserved.
1.
Introduction
Wildlife rehabilitation, the managed process whereby a displaced, sick, injured or orphaned wild animal regains the
health and skills it requires to function normally and live
self-sufficiently (International Wildlife Rehabilitation Council, 2005), is an internationally large and growing practice. It
involves both organisations that treat and release wildlife
casualties per se and those that specialise in the treatment
of particular taxa of conservation interest (e.g., Rijksen,
1974; Underhill et al., 1999). In Britain, 30,00040,000 casualties are taken into wildlife hospitals each year (L. Stocker, pers
comm.). Improving rehabilitation protocols, therefore, has the
* Corresponding author: Tel.: +44 0117 928 7593; fax: +44 0117 925 7374.
E-mail addresses: susie.molony@bristol.ac.uk (S.E. Molony), claire.dowding@bristol.ac.uk (C.V. Dowding), p.j.baker@bristol.ac.uk (P.J.
Baker), i.cuthill@bristol.ac.uk (I.C. Cuthill), s.harris@bristol.ac.uk (S. Harris).
0006-3207/$ - see front matter 2006 Elsevier Ltd. All rights reserved.
doi:10.1016/j.biocon.2006.01.015
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2.
531
Methods
Twenty suburban gardens in Bristol, UK were selected as release sites in March 2004 following assessment criteria used
by the Royal Society for the Prevention of Cruelty to Animals
(RSPCA) and The Wildlife Hospital Trust, Buckinghamshire,
UK: information was collected on proximity of nearest road
and level of usage, level of badger activity in the area, level
of hedgehog activity in the area, freedom of movement of
hedgehogs from the release site, risks posed by pesticides/
insecticides and physical features such as ponds, garden netting, etc. and whether the householder would be willing to
provide food and water at the release site. Suburban gardens
were utilized as many rehabilitators release hedgehogs in
these areas (Morris et al., 1993; Key, 1997; Morris, 1997, 1998;
Reeve, 1998). Animals were released in each garden and provisioned with food for the first week, following the release
procedures of the RSPCA and The Wildlife Hospital Trust.
The five treatment groups were: (1) rehabilitated (rehab-translocated); (2) directly translocated (direct-translocated); (3)
translocated after a period in captivity (captive-translocated);
(4) free-living wild at the release sites (recipient wild); and (5)
free-living wild hedgehogs (control wild). The treatment
groups consisted of: (1) 20 adult hedgehogs that had spent
>1 month at The Wildlife Hospital Trust; (2) 20 adults obtained
from the Uist Islands, Outer Hebrides, Scotland as part of a removal operation, and which had spent <6 days in captivity; (3)
23 adults obtained from the Uist Islands, but which had spent
>1 month in captivity; (4) 20 free-living wild hedgehogs captured and re-released at capture site <50 m from each of the
release gardens during MayAugust 2004 inclusive, and (5)
26 free-living wild hedgehogs captured and re-released at
capture site in suburban gardens located >3 km away from
the nearest release site to ensure independence (typical home
range size of hedgehogs is <40 ha (Reeve, 1994; Doncaster
et al., 2001), which is equivalent to a circular area of diameter
c. 0.36 km). All wild hedgehogs were captured by hand under
licence from English Nature, UK.
Due to the large sample sizes, hedgehogs were released in
four batches, each at a different time and in a different area
of Bristol (Table 1). Each hedgehog was fitted with a radiotransmitter glued to the dorsal spines (Biotrack, Dorset, UK:
7 g). This method of tagging does not inhibit free movement
(Schoenfeld and Yom-Tov, 1985; Reeve, 1994). Coloured heatshrink tubing glued to the spines was used to individually
mark animals. All individuals weighed >500 g, and were
matched for sex and mass (50 g) between treatment groups
at the batch level.
All hedgehogs were located every 23 days during daylight
hours for eight weeks to monitor their survival, after which
the transmitters were removed; where possible, details of
nest locations and nest construction were also recorded. A
sub-sample within each batch was selected using random
numbers from a list and radio-tracked; across batches, 11
individuals in each treatment group were followed. Tracking
took place during weeks one, four and seven after release.
Animals were tracked on foot continuously from 21.00 to
03.00 BST using a hand-held three-element Yagi antenna
and CE12 receiver (Custom Electronics of Urbana Inc, USA).
Location positions (fixes) were recorded every 5 min. At each
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Table 1 Details of each treatment group (R-trans, rehab-translocated; D-trans, direct-translocated; C-trans,
captive-translocated; R-wild, recipient wild; C-wild, control wild), sample size, release location and date of release/start
of monitoring
Group 1 (R-trans)
Batch
1
2
3
4
Total
Male/female
Group 2 (D-trans)
Batch
Total
Male/female
Batch
Total
Male/female
Batch
Total
Male/female
Release area
A
B
C
D
Release date
3 May 2004
17 May 2004
3 June 2004
15 June 2004
Release area
A
B
C
D
Release date
31 May 2004
15 June 2004
13 July 2004
3 August 2004
Start of monitoring
3 May 2004
17 May 2004
3 June 2004
15 June 2004
20
10/10
Batch
1
2
3
4
Total
Male/female
3 May 2004
17 May 2004
3 June 2004
15 June 2004
23
14/9
1
2
3
4
Group 5 (C-wild)
A
B
C
D
Release date
20
10/10
1
2
3
4
Group 4 (R-wild)
6
6
6
2
Release area
20
10/10
1
2
3
4
Group 3 (C-trans)
Start of monitoring
3 May 2004
17 May 2004
3 June 2004
15 June 2004
26
11/15
Release areas A, B, C and D are four areas in Bristol and location E is the control area in Bristol.
fix the animal was ascribed to a 25 25 m grid cell and classified as active or inactive based on fluctuations in the strength
of signal received. Whilst the influence of the observer on animal movements was not tested, it is reasonable to assume
that observers had no influence, and measures were taken
to ensure that animal movements were not affected by the
proximity of the observer, e.g., >20 m was maintained between observer and hedgehog at all times.
Approximately every 10 days (5 days) each hedgehog was
recaptured. At capture, individuals were weighed to quantify
changes in body mass during the study period. Individuals
were also examined for ticks and mites, and for signs of injury or trauma.
3.
Statistical methods
At the outset of the study, we had not incorporated individuals from the captive-translocated group. Rehab-translocated
and direct-translocated hedgehogs were released between
May and August 2004 in four batches, and monitoring of the
recipient wild and control wild hedgehogs started in conjunction with these batch releases.
However, initial results indicated that animals in the directtranslocated group had a markedly low survival rate. As a result,
the captive-translocated group was incorporated into the study
to determine whether retaining animals in captivity increased
survival rates. Consequently, animals in the captive-translo-
B I O L O G I C A L C O N S E RVAT I O N
4.2.
Mass loss
4.3.
Nocturnal ranging behaviour and patterns of habitat
utilisation
Recipient wild and control wild hedgehogs had significantly larger mean nightly ranges than rehab-translocated,
R-wild (a)
R-trans (b)
D-trans (c)
C-trans (ab)
C-wild (b)
1.0
0.9
Probability of survival
cated group were not all released at the same time as animals in
the other groups, although they were released at the same sites.
Since each batch of hedgehogs was released at a different site
and at a different time, any significant effect of batch on survival rates could have been attributable to a spatial and/or a
temporal element. Therefore, we initially examined the effect
of batch on the mean survival time (days after release) for
each group using a general linear model (GLM). This analysis
indicated that the timing and spatial location of releases did
not affect patterns of survival (see Section 4) and, as such, it
was valid to incorporate data from the captive-translocated
group and exclude batch from all subsequent analyses.
Survival probabilities were compared using the non-parametric KaplanMeier product limit estimator (Kaplan and Meier, 1958); survival rates (% SE) are given in brackets.
Differences in the maximum percentage mass loss over the
8-week period (arcsine square root transformed) between
treatment groups were quantified using analysis of variance
(ANOVA); mean mass loss (g SE) is given in brackets. The linear distance from the release site to the last known location at
the end of the monitoring period was calculated for each
hedgehog and compared using ANOVA, with sex as a between-subjects factor. The last known location was not always the furthest point that an individual had travelled
from the release site, but it serves as an approximate measure
of determining whether particular treatment groups moved
further from release sites.
Four movement parameters were calculated for those individuals that were radio-tracked: (1) nightly range area (95% kernel range estimate using the Animal Movement extension
(Hooge et al., 1999) for ArcView GIS 3.2 (Environmental Research
Institute, Inc, 19921999); (2) minimum distance travelled
(cumulative straight line distance between each 5-min fix);
(3) average speed of travel (minimum distance travelled divided
by time spent active); and (4) % time spent active. Parameters
were compared between treatment groups using ANOVA, with
sex as a between-subjects factor. Variables were log transformed where necessary to meet the assumptions of ANOVA.
Non-significant interaction terms were removed sequentially
from statistical models where appropriate. Post hoc differences
between groups were identified using Tukey tests.
Initially, analyses were conducted using data collected
across all weeks, with means calculated for individuals tracked
in more than one week. Subsequently, analyses were conducted
separately for weeks one, four and seven: the direct-translocated group was excluded from analysis during week seven because only one individual had survived to this stage.
Patterns of nest site use and retention were based on those
individuals for which we had >10 observations. The mean
number of days nest sites were used and the average distance
between nest sites were compared between treatment groups
using ANOVA, with sex included as a between-subjects factor.
533
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0.8
0.7
0.6
0.5
0.4
0.3
0
10
20
30
40
50
60
Time (days)
4.
Results
4.1.
Survival
Batch did not affect the mean survival time (days after release: ANOVA: F3, 101 = 0.390, p = 0.760), but treatment group
534
B I O L O G I C A L C O N S E RVAT I O N
60
50
40
b
30
20
10
0
R-wild
R-trans
D-trans
C-trans
C-wild
Treatment group
Fig. 2 Mean maximum % mass loss for each treatment
group (R-wild, recipient wild; R-trans, rehab-translocated;
D-trans, direct-translocated; C-trans, captive-translocated;
C-wild, control wild): error bars show 95% confidence
interval for the mean. Groups not significantly different
from each other are indicated with the same lower-case
letter in brackets.
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throughout the study (F4, 85 = 7.563, p < 0.001) (Table 2). The
mean distance travelled was significantly greater in recipient
wild and control wild hedgehogs at week one (F4, 50 = 3.524,
p = 0.013) and overall during the study (F4, 85 = 3.757,
p = 0.007), but there were no significant differences between
the treatment groups at week four (F4, 42 = 1.958, p = 0.119).
At week seven, captive-translocated hedgehogs travelled a
significantly smaller mean distance (F3, 34 = 3.016, p = 0.043)
and at a slower speed (F3, 34 = 3.185, p = 0.036) than the other
groups. No other significant differences were found in the
mean speed of travel between the groups (week one:
F4, 50 = 2.270, p = 0.095, week four: F4, 42 = 2.582, p = 0.051, overall: F4, 85 = 2.311, p = 0.064). No significant differences in mean
time spent active were found between the groups at week one
(F4, 50 = 1.646, p = 0.177), week four (F4, 42 = 0.842, p = 0.507), or
week seven (F3, 34 = 2.157, p = 0.111), but the direct-translocated group was significantly less active than the other
groups overall during the study (F4, 85 = 4.285, p = 0.003).
4.4.
Table 2 Untransformed nocturnal movement data for each group (R-wild, recipient wild; R-trans, rehab-translocated;
D-trans, direct-translocated; C-trans, captive-translocated; C-wild, control wild) at weeks one, four, seven and overall
during the monitoring period: the direct-translocated group was excluded from analysis during week seven because only
one individual survived to this stage
Group
Mean SD
% Time active
Mean SD
Mean SD
Week 1
R-wild
R-trans
D-trans
C-trans
C-wild
1.479 1.790
0.620 1.457
0.577 1.380
0.630 1.866
2.868 4.064
(a)
(b)
(b)
(b)
(a)
0.56 0.31
0.58 0.69
0.27 0.36
0.42 0.75
0.70 0.36
(a)
(b)
(b)
(b)
(a)
93.66 53.23 ()
96.34 116.25 ()
45.23 60.62 ()
69.36 124.91 ()
117.32 60.37 ()
71.92 14.15 ()
69.90 23.68 ()
53.44 24.69 ()
70.93 36.64 ()
87.39 9.98 ()
Week 4
R-wild
R-trans
D-trans
C-trans
C-wild
1.209 1.317
0.812 1.110
0.713 0.915
0.457 0.587
2.034 1.499
(a)
(b)
(b)
(b)
(a)
0.76 0.59
0.38 0.31
0.43 0.19
0.44 0.20
0.61 0.25
()
()
()
()
()
127.03 99.11
62.52 51.64
72.37 32.00
73.98 34.03
101.49 42.37
72.72 20.18
70.15 21.24
72.60 20.83
81.17 22.70
83.86 15.76
()
()
()
()
()
()
()
()
()
()
Week 7
R-wild
R-trans
D-trans
C-trans
C-wild
83.08 6.92 ()
66.23 19.77 ()
*
0.161 0.114 (b)
1.727 2.517 (a)
*
0.31 0.29 (a)
0.50 0.23 (b)
*
75.12 31.69 ()
89.42 7.78 ()
Overall
R-wild
R-trans
D-trans
C-trans
C-wild
1.673 1.294
0.576 0.992
0.848 1.417
0.606 1.438
1.882 1.634
0.65 0.36
0.49 0.55
0.35 0.34
0.46 0.56
0.59 0.30
109.62 57.67
82.34 91.35
58.83 58.01
77.12 94.94
98.93 44.89
(a)
(b)
(b)
(b)
(a)
(a)
(b)
(b)
(b)
(a)
()
()
()
()
()
Groups not significantly different from each other are indicated with the same lower-case letter in brackets; () indicates no significant
differences between groups.
B I O L O G I C A L C O N S E RVAT I O N
4.5.
Nest sites
5.
Discussion
1 3 0 ( 2 0 0 6 ) 5 3 0 5 3 7
535
or become accustomed to the stress associated with manipulation by and proximity to humans. Weight gain in captivity
due to generous feeding may facilitate greater survival by providing individuals with fat reserves whilst they acclimatise to
foraging in new habitats. Improved body condition/fat reserves are known to increase survival in a variety of species
(e.g., McMahon et al., 2000; Hill et al., 2003; Smith and Moore,
2005) and this is consistent with the patterns observed in this
study. Both rehab-translocated and captive-translocated
hedgehogs gained c. 20% of their body mass during >1 month
in captivity, whilst the direct-translocated group gained just
6% in the <6 days in captivity. Following release, the former
groups lost a maximum of 813% of their pre-release mass
compared to a maximum of 33% for the latter, indicating that
individuals in the direct-translocated group are likely to have
depleted their entire fat reserves and may have catabolised
body tissues in the eight weeks following their release, which
is likely to have reduced their chances of survival.
Translocating wild animals involves frequent handling by
people, e.g., at capture, health assessment, transportation,
transmitter/tag attachment and release, all of which are likely
to induce stress (McArthur et al., 1986; Boissy, 1995; Wingfield
et al., 1997). The energetic cost of mounting the stress response can lead to a reduction in body mass (McLaren et al.,
2004) and can lead to mortality from exhaustion after release
(Letty et al., 2000). Manipulation stress has also been identified as a factor influencing the post-release mortality of translocated red squirrels (Sciurus vulgaris: Wauters et al., 1997) and
European rabbits (Oryctolagus cuniculus: Letty et al., 2000). Conversely, a longer period of time in captivity, as was practiced
with the captive-translocated group in this study, may allow
animals to become accustomed to human proximity and handling and reduce the immediate deleterious effects of stress,
leading to an improvement in physical condition at the point
of release. However, there are likely to be differences between
species in the period before acclimatisation is achieved and
this will, in part, be related to the expected pattern of mass
loss following release. Further experimental analyses are
therefore needed to establish the threshold for reducing
manipulation stress and optimum mass gain in different species: on the basis of the treatment groups utilised in this
study, and the pattern of post-release mass change and survival, this period is between 6 and 30 days for the European
hedgehog.
Other factors that may affect the success or failure of
translocated animals in the time period immediately following release include the ability to navigate successfully in the
novel environment and avoid erratic movements (e.g., Robertson and Harris, 1995) and to recognise hazards (e.g., OBryon
and McCullough, 1985). However, our data indicate that the
direct-translocated group exhibited the same range size, distance travelled, speed of travel and amount of time spent active as the other groups that had also been translocated
(rehab-translocated and captive-translocated) and the total
distance travelled from the release site was not significantly
different between the direct- and captive-translocated
groups. Furthermore, there was no evidence of an early erratic phase: nocturnal behaviour remained the same over
weeks one, four and seven post-release. In addition, navigational ability was exhibited by all three groups of translocated
536
B I O L O G I C A L C O N S E RVAT I O N
6.
The impacts of introductions on the
recipient population
Unlike studies in other species (Webb et al., 1991; Evans, 1996),
there was no evidence of any immediate impact of the introduction of translocated individuals on the recipient population. Wild hedgehogs inhabiting the release areas (recipient
wild) did not suffer a lower survival rate after the releases of
the treatment groups: in fact, their survival rate was greater
than a second sample of wild hedgehogs at a control site
>3 km away (control wild). Furthermore, the nightly range
size, distance travelled and proportion of the night spent
active by both wild groups were not significantly different,
indicating that there was no evidence for an increase in
competition for, e.g., food or nest sites in those sites with
introduced animals. The absence of such competition may
be attributable to the fact that suburban gardens are frequently viewed as highly productive feeding sites that can
be utilised by a number of individuals on a given night (Reeve,
1994).
7.
Conclusions
Translocation is frequently used to return rehabilitated animals to the wild, and is an important tool for the population
management of species of conservation concern. Using an
experimental approach, this study has indicated that individuals held in captivity prior to translocation, whether they
have been treated for an injury or not, had a better survival
rate following release than individuals that were translocated
with a minimum time spent in captivity. Whilst there are
known negative effects of long-term captivity on survival that
may reduce the applicability of translocation as a conservation tool, e.g., inability to recognise natural foods and predators (McPhee, 2003) and other behavioural deficiencies
(Bremner-Harrison et al., 2004), these outcomes are, for the
most part, only applicable to captive-bred releases. Our data,
in contrast, suggest that using temporary captivity may actually be a beneficial strategy for wild-born translocation programmes, and may prove an alternative to other
unsuccessful methods for reducing handling stress, such as
tranquillisation (Letty et al., 2000). However, further analyses
1 3 0 ( 2 0 0 6 ) 5 3 0 5 3 7
are needed to establish the threshold for reducing manipulation stress and optimum mass gain in different species. In
addition, our data suggest that the introduction of new individuals did not have an immediate negative impact on the
survival or nocturnal ranging behaviour of the recipient wild
hedgehog population. Overall, therefore, rehabilitated hedgehogs released back into the wild attain post-release survival
rates equivalent to those observed for wild individuals, with
little or no impact on recipient populations in urban areas.
Acknowledgements
S.E.Ms work on rehabilitated hedgehogs was supported by
the RSPCA; additional funding for the translocation of Uist
hedgehogs was provided by The Wildlife Hospital Trust and
the International Fund for Animal Welfare. We thank all garden owners who allowed us to release hedgehogs on their
property, E. Bennitt, J. St-Clair and M. Taylor for field assistance, and Drs. M. Gorman, N. Reeve and two anonymous referees for comments on an earlier draft of the paper.
R E F E R E N C E S
Boissy, A., 1995. Fear and fearfulness in animals. Q. Rev. Biol. 70,
165191.
Bremner-Harrison, S., Prodohl, P.A., Elwood, R.W., 2004. Behavioral
trait assessment as a release criterion: boldness predicts early
death in a reintroduction programme of captive-bred swift fox
(Vulpes velox). Anim. Conserv. 7, 313320.
Chiarello, A.G., Chivers, D.J., Bassi, C., Maciel, M.A.F., Moreira, L.S.,
Bazzalo, M., 2004. A translocation experiment for the
conservation of maned sloths, Bradypus torquatus (Xenarthra,
Bradypodidae). Biol. Conserv. 118, 421430.
Doncaster, C.P., 1992. Testing the role of intraguild predation in
regulating hedgehog populations. Proc. R. Soc. Lond. B Biol.
Sci. 249, 113117.
Doncaster, C.P., 1994. Factors regulating local variations in
abundance: field tests on hedgehogs, Erinaceus europaeus.
Oikos 69, 182192.
Doncaster, C.P., Rondinini, C., Johnson, P.D., 2001. Field test for
environmental correlates of dispersal in hedgehogs Erinaceus
europaeus. J. Anim. Ecol. 70, 3346.
Evans, I., 1996. Criteria for the consideration of translocation as
an aid to conserving birds in the UK. In: Holmes, J.S., Simons,
J.R. (Eds.), The Introduction and Naturalisation of Birds. HMSO,
London, pp. 4956.
Fajardo, I., Babiloni, G., Miranda, Y., 2000. Rehabilitated and wild
barn owls (Tyto alba): dispersal, life expectancy and mortality
in Spain. Biol. Conserv. 94, 287295.
Goossens, B., Setchell, J.M., Tchidongo, E., Dilambaka, E., Vidal, C.,
Ancrenaz, M., Jamart, A., 2005. Survival, interactions with
conspecifics and reproduction in 37 chimpanzees released
into the wild. Biol. Conserv. 123, 461475.
Griffith, B., Scott, J.M., Carpenter, J.W., Reed, C., 1993. Animal
translocations and potential disease transmission. J. Zoo
Wildlife Med. 24, 231237.
Hill, M.R.J., Alisauskas, R.T., Ankney, C.D., Leafloor, J.O., 2003.
Influence of body size and condition on harvest and survival of
juvenile Canada geese. J. Wildlife Manage. 67,
530541.
Hodder, K.H., Bullock, J.M., 1997. Translocations of native species
in the UK: implications for biodiversity. J. Appl. Ecol. 34,
547565.
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