BIOLOGICAL
CONSERVATION
Biological Conservation 118 (2004) 175–181
www.elsevier.com/locate/biocon
Non-commercial collection of spur-thighed tortoises(Testudo graeca graeca): a cultural problem in southeast Spain
Irene P�erez a,*, Andr�es Gim�enez b, Jos�e Antonio S�anchez-Zapata b, Jos�e Daniel Anad�on b,Marcelo Mart�ınez a, Miguel �Angel Esteve a
a Dpto. Ecolog�ıa e Hidrolog�ıa, Facultad de Biolog�ıa, Universidad de Murcia, Campus de Espinardo, 30100 Espinardo (Murcia), Spainb �Area de Ecolog�ıa, Dpto. Biolog�ıa Aplicada, Universidad Miguel Hern�andez, Campus de Orihuela, 03312 Orihuela (Alicante), Spain
Received 3 September 2002; received in revised form 31 July 2003; accepted 31 July 2003
Abstract
Collecting tortoises for the pet trade is one of the factors threatening species of Testudo in the Mediterranean area. The collection
of Testudo graeca graeca for pets is described in southeast Spain, where the main European population of this subspecies coincides
with an area where keeping tortoises in captivity is a long-established custom. This present paper, based on inquiries made to
children, reveals that this practice continues to be a common activity, and estimates a captive population in the order of tens of
thousand of tortoises. Tortoises are collected as a result of chance encounters with wild animals by local inhabitants, and without
any commercial objectives. The captive breeding and the release of tortoises without any institutional control is also common. These
activities could be an important threat for the species. Implications for conservation are discussed and a critical review of the
conservation strategies developed in relation to this threat (trade control and re-introduction programmes) are presented. We
suggest that environmental education programmes are necessary to reduce casual collection and to change the social perception of
tortoises as pets.
� 2003 Elsevier Ltd. All rights reserved.
Keywords: Species conservation; Captivity; Non-commercial collecting; Wildlife attitudes and value scales; Testudo graeca graeca
1. Introduction
Human collection of plants and wild animals is a
response to several needs and its origins lie in the har-
vesting of plants and fruits and in hunting and fishing
for human consumption by local populations. In mod-
ern societies, these activities have led, on the one hand,to sport hunting and fishing, and, on the other, to an
increase in the scale of collection for economic and
commercial motives. This has become especially signif-
icant in the harvesting of animals in large-scale fishing
(Caughley and Gunn, 1996) or for their skins (Shine
et al., 1996; Fitzgerald et al., 1993), as well as the use of
animal parts in traditional medicine (Hemley and Mills,
1999) and the trade and traffic of live animals for use as
* Corresponding author.
E-mail address: [email protected] (I. P�erez).
0006-3207/$ - see front matter � 2003 Elsevier Ltd. All rights reserved.
doi:10.1016/j.biocon.2003.07.019
pets, as is the case for birds (Christian et al., 1996) or
tortoises and turtles (Thorbjarnarson et al., 2000).
The survival of wild species can be threatened by
direct activities, e.g. elephants hunted for their ivory
(Milner-Gulland and Mace, 1991; Tchamba, 1996), or
through indirect activities such as the capture of ceta-
ceans or marine turtles in fishing nets designed for otherspecies (Chan et al., 1988). Thirdly, species may be
collected through chance encounters, although the ef-
fects of this practice have seldom been studied.
Many species of tortoises face conservation problems
induced by humans, which have even led to the recent
extinction of some species (Honneger, 1981; Thorb-
jarnarson et al., 2000). In most cases, threats include the
alteration or loss of suitable habitats, and the collectionof animals for food or for the pet trade (Klemens and
Thorbjarnarson, 1995; Thorbjarnarson et al., 2000).
The collection of tortoises for the pet trade is un-
doubtedly an important threat for some species, for
Fig. 1. (a) Distribution of T. graeca graeca in the Mediterranean area; (b) distribution of T. graeca graeca in Southeastern Spain, provinces of
Almer�ıa (from Andreu, 1988) and Murcia (from Gim�enez et al., 2001); (c) study area in the province of Murcia. Dark grey indicates the districts
inside the distribution area of the species and light grey indicates the districts outside the distribution area of the species.
176 I. P�erez et al. / Biological Conservation 118 (2004) 175–181
example Geochelone chilensis in Argentina (Buskirk,
1993; Waller, 1997; Pujol, 1998) or the different species
of the genus Testudo in the Mediterranean and Asia
Minor (Lambert, 1979). In the latter case, the consoli-
dation of the pet trade during the 19th century led to an
international export trade involving thousands of cir-
cum-Mediterranean species per year and which include
Testudo hermanni from the Balkans, T. horsfieldii fromthe southwest of the former Soviet Union, T. graeca
ibera from Turkey and T. graeca graeca from Morocco
(Lambert, 1979).
In Spain, this trade has never reached international
proportions, although a regular national trade existed
within the natural range of the species (T. graeca gra-
eca comes from southeast Spain and T. hermanni from
the Balearic islands) (Fig. 1) towards urban centressuch as Madrid and Barcelona (L�opez-Jurado et al.,
1979).
T. graeca graeca – commonly named the spur-thighed
tortoise – is one of six subspecies of T. graeca native to
the Mediterranean and Asia Minor (Iverson, 1992;
Gmira, 1993; David, 1994). It is distributed throughout
North Africa, from the Atlantic coast of Morocco to
Northeast Libya, and in small patches in the Do~nanaBiological Reserve (southwest Spain), Mallorca and
parts of southeast Spain (provinces of Murcia and Al-
mer�ıa) (Andreu and L�opez-Jurado, 1998) (Fig. 1a and
b). The main population of T. graeca graeca in Europe
inhabits semiarid coastal mountains on metamorphic
substrates in southeast Spain. Annual precipitation here
ranges from 214 to 351 mm and vegetation cover con-
sists basically of sparse scrub with small patches of openPinus halepensis and Quercus rotundifolia woodland and
dry farming (Gim�enez et al., 2001). This tortoise has a
high international, national and local protection status.
It is included in Appendix II of the Convention on In-
ternational Trade in Endangered Species (http://
www.cites.org), in Appendix II of the Bern Convention
(http://www.nature.coe.int/english/cadres/bern.htm) and
is classified as vulnerable in the IUCN Red List of
Threatened Species (IUCN, 2002). In the European
Union the species is inluded in Appendix II and IV of
the Habitat Directive (http://www.europa.eu.int/comm/
environment/nature/themes.htm) and �243,000 ha of its
habitat has been proposed for inclusion in the Natura
2000 network, while in Spain this tortoise is considered
as being endangered (Pleguezuelos et al., 2002).
Although it is illegal to collect or to sell this speciesof tortoise, in southeast Spain the custom exists of
keeping tortoises in captivity and large numbers of
tortoises are collected from wild populations. This ac-
tivity seems to be a very common custom in many local
cultures and also threatens other species of endangered
terrestrial tortoises (L�opez-Jurado et al., 1979; Curl
et al., 1985; Fritts and Jennings, 1994; Waller, 1997;
Pujol, 1998). However, this collection on a local scalewith no commercial objectives in mind has not been
diagnosed as a possible threat in most cases. The
present study aims to: (i) describe the collection of
T. graeca graeca in southeast Spain, (ii) calculate the
numbers of animals kept in captivity, and (iii) deter-
mine the implications of this process on the conserva-
tion of the species, and thereby carry out a critical
review of the conservation strategies developed inconnection with this conservation issue.
2. Methods
In order to address the objectives of this study, we
carried out surveys of children in schools, given the easy
accessibility to this sector of the population, and becausewe considered them to be an important part of those
who keep tortoises as pets.
We made 796 interviews of school children, mainly
between the ages of 12 and 15 (87% of pupils inter-
viewed) (Fig. 2). Surveys were carried out in all the
districts of the province of Murcia within the distribu-
tion area of T. graeca graeca, as well as in five peripheral
districts (Fig. 1c, Table 1). All rural schools and a rep-
Fig. 2. Frequency distribution of age of the children polled.
I. P�erez et al. / Biological Conservation 118 (2004) 175–181 177
resentative sample of urban schools were surveyed,
which in total amounted to 26 schools in 22 towns and
cities.
The surveys were conducted in the classroom by a
person with experience in environmental education and
consisted of seven open questions: whether pupils had or
had had tortoises in captivity as pets, the number of
captive tortoises, their origin and the way they wereobtained, the destination of these tortoises if they had
got rid of them, and whether they had bred. The chil-
dren were also asked their ages and addresses.
Children were classified as rural or urban inhabitants,
taking rural to mean from villages with less than 250
inhabitants. Also, children were distinguished as living
inside or outside the distribution range of T. graeca
graeca.We performed an independent test (v2, significance at
5% level) to study the relationship between answers and
these two characteristics of the children. If the null hy-
Table 1
Number of surveys made per district and representation of the school age
Estad�ıstica de Murcia, 1991)
District Location Number of interview
Aledo Outside 17
Alhama Outside 11�Aguilas Inside 259
Cartagena Outside 106
Lorca Inside 187
Fuente �Alamo Outside 74
Mazarr�on Inside 23
Murcia Outside 37
Puerto Lumbreras Inside 64
Totana Outside 18
Total 796
Inside, districts inside the distribution area of the species; outside, district
pothesis was rejected, the contingency coefficient (C) wascalculated. This coefficient varied between 0 (no associ-
ation) and the maximum association valuepððq� 1Þ=qÞ,
where q was the minimum number of rows or columns of
the contingency table. In our case, the number of rowsand columns was always two, and so the maximum
contingency coefficient was 0.71.
For each question, responses were described by their
proportion within the sample and by their confidence
interval (CI). CI was calculated using the normal ap-
proximation method (significance at 5% level) (Zar,
1984). We have indicated the partial and global values
when there was a significant difference in the differentcategories of the variables.
Regarding the question of the number of captive
tortoises per person, we utilised the Mann–Whitney test
in order to show if there were statistical differences be-
tween the mean number of tortoises in the different
categories of children. We have indicated the CI for the
population mean (significance at 5% level).
On the basis of the proportion of children with cap-tive tortoises and the mean number of captive tortoises
per child, we estimated the number of tortoises kept in
captivity in the study area. We made this estimation
using only 13-year-old children (the most frequent age in
our sample) to avoid double counting of families with
children of similar ages. For this estimate we did not
take into consideration the survey carried out in the city
of Murcia (Table 1), since we considered that it is notrepresentative of the district as a whole. In the results,
we have indicated the CI for the population mean (sig-
nificance at 5% level).
3. Results
3.1. Quantification of captivity
The mean proportion of children that had or had
had a tortoise in captivity was 64.5%. For CIs see
population (between 7 and 19 years old) polled (Centro Regional de
s Population (7–19 years old) Polled population (%)
134 12.60
2578 0.42
5313 4.87
31,988 0.33
12,366 1.51
1393 5.31
3177 0.72
63,366 0.05
1782 3.59
3274 0.54
125,371 0.63
s in the periphery of the distribution area of the species.
178 I. P�erez et al. / Biological Conservation 118 (2004) 175–181
Table 2. This proportion was significantly higher in the
districts inside the distribution area of the species than
in the districts outside of the distribution area
(v2 ¼ 27:81; df¼ 1; P < 0:001; C ¼ 0:18). Inside, the
mean proportion of children with tortoises was 70.5%,while in the periphery it was 51.5%. The proportion of
children that had or had had a tortoise in captivity is
also higher in urban schools (v2 ¼ 5:44; df¼ 1;
P < 0:02; C ¼ 0:08). The mean proportion of urban
children with tortoises was 69%, while in rural areas it
was 61.5%.
Of those children that had or had had tortoises,
nearly three-quarters (71%) had only one or two but afew had much larger numbers (6% had 10 or more). The
mean number of captive tortoises per child for the whole
study area was 2.9. Mean value was significantly higher
in districts inside the distribution area of the species than
in the peripheral districts (U ¼ 3:33; P < 0:001) (Table2). However, there were no significant differences
between rural and urban populations (U ¼ 1:208;P > 0:05).
3.2. Origin, captive breeding and destination of captive
tortoises
On average, only 7.5% of children had bought their
tortoise, 63.5%hadobtained them fromwild populations,
directly or through somebody else, and the remaining
29% did not know the origin of their tortoise (CI in Table2). Inside the distribution area, 74.5% of the children had
obtained their tortoises from wild populations, while in
peripheral districts the mean proportion fell to 37.5%
(v2 ¼ 60:26; df¼ 1; P < 0:001; C ¼ 0:32). Again, within
Table 2
Results of the surveys in the study area, inside and outside the distribution
n Whole area Inside O
Captive tortoises (%) 796 61–68 67–74 4
Tortoises per person 513 2.5–3.4 2.8–3.9 1
Origin 513
Wild population (%) 60–68 71–78 2
Trade (%) 5–10 1–5 1
Middleman (%) 25–33 21–30 3
Captive breeding (%) 513 14–22 – –
Destination 306
Release (%) 12–18 14–22
Transfer (%) 10–15 8–14 1
Lost (%) 11–17 – –
Died (%) 14–20 18–33 1
Organization (%) 1–4 0.3–3
n.s.¼not significant.
CIs for percentage of children that have tortoises in captivity, the mean nu
and captive breeding.* P < 0:05.
** P < 0:01.*** P < 0:001.
the distribution area, only 3% of children had bought
their tortoises compared to 21% outside the area
(v2 ¼ 60:26; df¼ 1; P < 0:001;C ¼ 0:29). The proportionof tortoises transferred by another person who did not
know the origin of the tortoise was higher in peripheraldistricts (39.5%) than districts inside the distribution area
(25.5%) (v2 ¼ 9:80; df¼ 1; P < 0:01; C ¼ 0:14).In relation to captive breeding, 18% of the children
had had tortoises that bred in captivity. There were no
differences either between core and peripheral districts
(v2 ¼ 2:00; df¼ 1; P < 0:05) or between the urban and
rural schools (v2 ¼ 3:07; df¼ 1; P > 0:05).With regards to the destination of the captive tor-
toises, 15% of the children answered that they had re-
introduced their tortoises into the wild, 12.5% had given
their tortoises to another person, 14% had lost their
tortoises and only 2.5% had donated their tortoises to
organisations or wildlife protection institutions. Finally,
17% of the children answered that their captive tortoise
had died. In comparing core and peripheral districts,
there were significant differences between children withinand outside the core areas for the proportions released
in the wild (v2 ¼ 10:15; df¼ 1; P < 0:01; C ¼ 0:14),those dying in captivity (v2 ¼ 8:5; df¼ 1; P < 0:01;C ¼ 0:13) and those donated to organisations or wildlife
protection institutions (v2 ¼ 5:87; df¼ 1; P < 0:05;C ¼ 0:11) (Table 2).
3.3. Captive population estimation
For the subsample of 13-year-old children surveyed,
there were even larger differences than in the whole
sample between schools inside and outside the species�
area of T. graeca graeca for rural and urban schools
utside P Urban Rural P
5–58 ��� 64–74 57–66 �
.7–2.7 ��� – – n.s.
– –
9–46 ��� n.s.
4–28 ��� – – n.s.
1–48 �� n.s.
n.s. – – n.s.
3–12 �� – – n.s.
0–15 n.s. – – n.s.
– – – –
1–18 �� – – n.s.
2–10 n.s. – – n.s.
mber of tortoises per child, the origin and destination of these tortoises
Table 3
CIs estimates of the captive tortoise populations in the study area
Inside Outside P Study area
Captive tortoises (%) 63–77 44–65 � –
Tortoises per person 3–6 1–4 � –
13 years old population 1734 2982 4716
Number of families 29,796 55,143 84,939
Estimate a 3527–7565 1711–7051 5237–14,617
Estimate b 60,600-129,994 31,631–13,0378 92,231–260,373
(a) Number of tortoises in the subpopulation of 13-year-old children. (b) Number of tortoises in all families in the study area.* P < 0:05.
I. P�erez et al. / Biological Conservation 118 (2004) 175–181 179
range; this applies to the proportions having captive
tortoises (v2 ¼ 6:54; df¼ 1; P < 0:05), and for the
numbers kept per child (U ¼ 1:971; P < 0:05), (thoughthe levels of significance were lower because of the
smaller numbers sampled – Table 3).The total number of families having a 13-year-old
child in the whole sample was 1734 (Centro Regional de
Estad�ıstica de Murcia, 1991) from which we estimate
that the total number of captive tortoises in the whole
study area was �10,000, with very wide confidence
limits (Table 3). The extrapolation of this estimate to all
families (instead of just the 5.5% that had a 13-year-old;
Centro Regional de Estad�ıstica de Murcia, 1991) leadsto a total figure of about 176,000 with confidence limits
of 92,231–260,373 (Table 3). However, this is certain to
be an overestimate since we know that families without
children of school age are less likely to have tortoises.
Overall, we therefore consider that the number of tor-
toises kept in captivity in the study area is in the order of
tens of thousands.
4. Discussion
4.1. Captivity and collection process
Our results reveal that, at present, the capture of
T. graeca graeca for trade is a marginal issue in
southeastern Spain. This contradicts recent local and
national reviews concerning the conservation status of
this tortoise (Castanedo et al., 1991; Blanco and
Gonz�alez, 1992; Blasco, 1992; Andreu and L�opez-Jurado, 1998; Garc�ıa, 1999), in which trade was iden-tified as one of the main threats facing the species in
this area. These studies probably reflect a past situa-
tion, when locally collected animals were more widely
sold in markets and pet shops both here and in other
geographical areas in Spain where wild tortoises do not
occur (L�opez-Jurado et al., 1979). In those other parts
of Spain, the demand for tortoises may be supplied at
present by animals from North Africa, where com-merce and export are still common activities (Dupre,
2002; Ferr�andez, 2003).
However, in southeast Spain the custom of keeping
tortoises in captivity is still very common. The estimate
of tens of thousand of animals is an indication of its
magnitude but there is a need to carry out more precise
studies to refine these figures. The way most tortoisesreach captivity is by direct collection from wild popu-
lations through chance encounters by local inhabitants,
and not through active search for the species with
commercial objectives in mind. This is mainly a local
activity, since the proportion of people who have
captive tortoises and the number of captive tortoises
per person decreases considerably from within the
distribution range of the species to the peripheral area.There is quite an important stock of tortoises that
breed in captivity, and a significant flow of tortoises
from one person to another, but few individuals
are donated to organisations or wildlife protection
institutions.
The custom of keeping tortoises in captivity is
maintained by popular belief regarding its benefits and,
above all, by their attraction to children as pets. Thiscustom was firmly rooted in rural areas before being
exported to urban centres by street sellers. At present,
through notable rural depopulation and the develop-
ment of legislation concerning the conservation of wild
animals, the regular collection and trade in tortoises has
gradually declined.
4.2. Implications for conservation
The high proportion of people who collect tortoises
from wild populations suggests that this disturbance of
T. graeca graeca populations may have demographicconsequences which may include local extinction in
areas around villages. Furthermore, the release of cap-
tive tortoises into the wild without any institutional
control may also severely affect established populations
by disease transmission (Dodd and Seigel, 1991; Jac-
obson, 1993; Cunningham, 1996; Deem et al., 2001).
This has been suggested as the prime agent in the
rapid decline of some populations of desert tortoise(Gopherus agassizii) in the western Mojave Desert where
180 I. P�erez et al. / Biological Conservation 118 (2004) 175–181
individuals suffering from the upper respiratory disease
syndrome (URSD) were released (Jacobson, 1993;
Brown et al., 1994; Jacobson et al., 1995). There is also
the possibility of creating outbreeding depression, that
is, a decline in fitness associated with mating amonggenetically distinct populations (Templeton, 1994; Seigel
and Dodd, 2000).
Conservation strategies for T. graeca graeca have
focussed on the control of trade in the species and on re-
introduction programmes of captive tortoises. In the
first case, national and international strategies designed
to combat pet traffic have been essential in the past and
in Spain have almost ended the trade in tortoises. In thesecond case, re-introductions seem irrelevant when
compared to threats such as habitat destruction
(Gim�enez et al., 2001) and continued chance collection.
Besides, the effectiveness of these techniques of manip-
ulation, especially in reptiles, are debatable (Dodd and
Seigel, 1991; Wolf et al., 1996; Seigel and Dodd, 2000)
and need significant economic and human resources
(Griffith et al., 1989; Lindbeurg, 1992; Kleiman et al.,1994). There is a predisposition to use re-introductions
as a quick and easy solution to complex conservation
issues rather than tackling the real causes of population
declines (Dodd and Seigel, 1991; Fischer and Linden-
mayer, 2000).
4.3. Conservation recommendations
There is a social perception of the spur-thighed tor-
toise as a pet, which reveals lack of popular knowledge
about its legal situation, the threatened status of the
species and its place as a typical element of semiarid
landscapes of southeast Spain. All of this implies a need
to develop environmental education programmes to-
wards a perception of the tortoise as a wild animal. T.
graeca graeca inhabits arid and semiarid areas of highecological value, but the local inhabitants and general
public do not appreciate the worth of these landscapes.
At present these systems are strongly threatened, mainly
by irrigated farming and urban development (Mart�ınez,2001; Gim�enez et al., 2001). TheNatura 2000 programme
is an important policy for conserving European biodi-
versity and, in particular, for preserving the habitat of T.
graeca graeca in Spain. The spur-thighed tortoise couldbe promoted as a flagship species (Caro and O�Doherty,
1999) to help safeguard these semiarid ecosystems.
Acknowledgements
We wish to thank Rosa Pardo for carrying out the
surveys and Dr. Kaldo for his comments and statisticalassistance. Financial support was provided by the
Consejer�ıa de Agricultura, Agua y Medio Ambiente de
la Regi�on de Murcia. We also thank Dr. B.N.K. Davis
and an anonymous reviewer for their suggestions on the
manuscript.
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