Biol Invasions (2010) 12:3627–3636
DOI 10.1007/s10530-010-9755-2
ORIGINAL PAPER
The risk of zoological parks as potential pathways
for the introduction of non-indigenous species
Marı́a C. Fàbregas • Federico Guillén-Salazar
Carlos Garcés-Narro
Received: 10 November 2009 / Accepted: 29 March 2010 / Published online: 4 April 2010
Ó Springer Science+Business Media B.V. 2010
Abstract Zoological parks have been associated
with an increasingly frequent origin for accidentally
released animal species. Such species have become
invasive in some cases. The goals of this study are to
evaluate the risk of potential animal escape at
zoological parks by assessing the security of animal
enclosures, and to identify which factors could be
affecting such security. We visited a random sample
of 1,568 animal enclosures belonging to 63 Spanish
zoological parks, and assessed their security with a
defined criteria based on the suitability of the physical
barrier of the enclosure and the impossibility for the
public to release the animals. To our criteria, we found
221 enclosures which were non-secure against animal
escape. Such enclosures were unevenly distributed
among 47 zoological parks (74.60% of the sample),
and housed non-indigenous species in 79.64% of the
cases (21 species listed by the European Inventory of
Invasive Species). Seven factors were analyzed to
assess their effect on enclosure security. Six of them
M. C. Fàbregas (&)
F. Guillén-Salazar
Departamento de Fisiologı́a, Farmacologı́a y Toxicologı́a,
Facultad de Ciencias de la Salud, Universidad Cardenal
Herrera, 46113 Moncada (Valencia), Spain
e-mail: maria.fabregas@uch.ceu.es
C. Garcés-Narro
Departamento de Producción Animal, Sanidad Animal
y Ciencia y Tecnologı́a de los Alimentos, Facultad de
Veterinaria, Universidad Cardenal Herrera, 46113
Moncada (Valencia), Spain
•
were found to have an effect, and three were selected
by a logistic regression model as the main predictors
for secure enclosures. Such factors are discussed, and
measures are suggested to reduce the risk of zoolog-
ical parks as a potential pathway for the introduction
of non-indigenous species.
Keywords Non-indigenous species

Invasive alien species
Zoological parks

Introduction pathways
Enclosure security

Animal escapes
Introduction
Biological invasions are a significant component of
human caused global change (Vitousek et al. 1997).
Over the past few centuries, non-indigenous species
(hereafter NIS), defined as species or lower taxon
introduced outside its natural past or present distri-
bution (CBD-COP 2002), have caused untold damage
to the human population, negatively affecting health
(Bright 1998) and agriculture (Mack et al. 2000;
Pimentel et al. 2000), as well as economy (Pimentel
et al. 2001). According to the Convention on
Biological Diversity, those NIS whose introduction
and/or spread threaten biological diversity become
invasive alien species or IAS (CBD-COP 2002). This
phenomenon has been widely documented (Simberl-
off 1996; Parker et al. 1999) to the point of being
recognized as the second major threat to global
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biodiversity, right after habitat loss and landscape
fragmentation (Schmitz and Simberloff 1997; Walker
and Steffen 1997; Macdonald and Thom 2001). This
threat is the principle for the inclusion of biological
invasions under ‘‘Threats to Biodiversity’’ in the
framework of the Convention on Biological Diversity
(BIP 2006).
The goal of the Convention on Biological Diversity
regarding biological invasions is to control threats
from IAS through two specific targets: to prevent their
introduction by controlling their routes of entry and to
develop management plans for major NIS that
threaten ecosystems, habitats or other species (UNEP
2004a, 2004b, 2005). Once a NIS is established,
eradication is often impossible, and mitigation and
control are difficult and expensive (Kolar and Lodge
2001). Therefore, a reduction in the introduction of
NIS via routes of entry is the single most direct and
potentially effective means of reducing the threat to
biodiversity from IAS (Carlton and Ruiz 2005).
Non-indigenous species can reach an ecosystem
through a variety of pathways (DAISIE 2008). Escape
from captivity (either for production or leisure pur-
poses) is one of the most common ways of vertebrate
introduction (Williamson 1996). In that regard, zoo-
logical parks seem to be more and more frequently the
origin of accidentally released animals (Clergeau and
Yésou 2006). These centers house great numbers of
wildlife species in their facilities, and although some
of them have native fauna in their collections, most
animal species are not indigenous to the place where
the zoological park is located, therefore becoming a
potential source of NIS if animals escape (IUCN
2002a). In fact, animal escapes from zoological parks
worldwide have been previously documented (Csur-
hes 2003; Jiguet et al. 2008), and some of these
escaped species have become invasive (Roll et al.
2008; Clergeau and Yésou 2006; Jousson et al. 2000).
In Europe, 82 non-indigenous terrestrial vertebrate
species have been introduced as a consequence of
escapes from zoological parks, becoming such centers
the second most important known pathway for the
introduction of NIS in this region (DAISIE 2008).
Considering the importance of zoological parks as
introduction pathways for NIS, our first goal is to
evaluate the risk of potential animal escape at
zoological parks by assessing the security of the
enclosures housing the animal collection. Also, given
that the security of an animal enclosure within a
123
M. C. Fàbregas et al.
zoological park can be affected by several factors,
including the nature of the species housed, the design
of the enclosure assessed, or the management of the
zoological park itself, our second goal is to determine
which factors affect such security and propose
measures to better address IAS within the zoo com-
munity.
Methods
Data collection took place in Spain, where 63 out of
the 83 existing zoological parks (defined as permanent
establishments where animals of wild species are kept
for exhibition to the public, with the exception of
circuses and pet shops, hereafter ‘‘zoos’’) officially
registered at the country in 2003, participated in the
study (unpublished report of the Spanish Ministry for
the Environment). These centers voluntarily agreed to
participate in a broader study aimed at assessing the
situation of Spanish zoos when the national legislation
relating to the keeping of wild animals in zoos (Ley
31/2003) came into force due to the incorporation of
the European Community Zoos Directive 99/22/EC
into national legislation (Rodrı́guez-Guerra and Guil-
lén-Salazar 2006). The participating zoos filled out a
comprehensive questionnaire that included, amongst
other data, a complete list of the species and spec-
imens which made up their zoological collections.
The study sample comprised 1568 enclosures
(Table 1); 1,469 enclosures to which the public had
no access (i.e. the animals were observed from
outside) and 99 enclosures where the public could
access the exhibits, either in a vehicle or by foot (i.e.
walk-in enclosures). We randomly chose 30 species
from each participating zoo. When a zoo had less
than 30 species, all the enclosures were evaluated.
Prior to the selection process, the following domes-
ticated species were excluded from the analysis:
honey bee (Apis mellifera), mithan (Bos frontalis),
yak (Bos grunniens), zebu (Bos indicus), Bali cattle
(Bos javanicus), European cattle (Bos taurus), water
buffalo (Bubalus bubalis), Bactrian camel (Camelus
bactrianus), dromedary (Camelus dromedarius), dog
(Canis familiaris), goat (Capra hircus), goldfish
(Carassius auratus), Guinea pig (Cavia porcellus),
pigeon (Columba livia), donkey (Equus asinus),
horse (Equus caballus), cat (Felis catus), chicken
(Gallus gallus), llama (Lama glama), alpaca (Lama
The risk of zoological parks 3629

Table 1 Security of
Zoological group Number of Number of Percentage of Number of species
enclosures by taxonomic
enclosures non-secure non-secure encl in non-secure
classification of housed
in the sample enclosures osures within the enclosures
species
taxon

Mammalia 444 42 9.46 37

Artiodactyla 119 18 15.13 15
Primates 90 6 6.67 6
Rodentia 31 6 19.35 5
Carnivora 153 5 3.27 4
Other 51 7 13.73 7
Aves 569 124 21.79 98
Anseriformes 96 46 47.92 33
Psittaciformes 158 23 14.56 20
Passeriformes 41 11 26.83 10
Galliformes 61 6 9.84 6
Pelecaniformes 11 7 63.64 5
Other 202 31 15.35 24
Reptilia 219 36 16.44 30
Squamata 149 15 10.08 14
Testudines 53 18 33.96 13
Crocodylia 17 3 17.65 3
Amphibia 14 2 18.18 2
Anura 11 1 9.09 1
Caudata 3 1 33.33 1
Fish 229 15 6.55 14
Perciformes 128 7 5.47 7
Characiformes 17 0 0 0
Other 84 8 9.52 7
Invertebrates 93 2 2.22 2
Lepidoptera 32 1 2.15 1
Actiniaria 3 1 33.33 1
Other 58 0 0 0
Total 1,568 221 183

pacos), turkey (Meleagris gallopavo), house mouse
(Mus musculus), helmeted guineafowl (Numida mel-
eagris), rabbit (Oryctolagus cuniculus), sheep (Ovis
aries), brown rat (Rattus norvegicus), and pig (Sus
scrofa). As the evaluation of zoos as potential
pathways for NIS was studied by assessing enclosure
security against escape, free-flying birds or any other
species which were not housed in an enclosure but
wandered freely in the zoo were not considered in the
study.
The evaluation of the participating zoos, including
the security of their enclosures, was carried out
through the application of an evaluation guide
specifically developed for this task (Guillén-Salazar
2003). A team of seven biologists and veterinarians
with broad experience in the zoo profession and/or in
zoo inspection processes participated in the design of
the evaluation guide. This guide was based on the
standards of modern zoo practice (DETR 2000) as
well as on the accreditation systems of the American
Association of Zoos and Aquariums and the Euro-
pean Association of Zoos and Aquaria. In order to
assess enclosure security, two aspects of the enclo-
sure were examined: (1) The existence of a complete,
well maintained, and appropriate physical barrier to
prevent the escape of the animals housed at the

123
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enclosure (including sewage lines, filtration systems
and, in general, any opening or valve that could allow
the escape of an animal or part of it such as eggs) and
(2) The impossibility for the public to release the
animals directly (i.e. capturing the animal and
removing it from the enclosure) or indirectly (i.e.
opening doors or windows not properly locked or
supervised by the staff). For the purpose of this study
an enclosure was considered ‘‘secure’’ only when
both conditions were simultaneously met. Otherwise
the enclosure was categorized as ‘‘non-secure’’.
Data were collected by three evaluators between
October 2003 and May 2004. They were previously
trained by the research director on the application of
the evaluation guide, and started the evaluations once
the indexes of concordance (Martin and Bateson
1993) used to assure inter-observer reliability reached
95% amongst them. Visits to the participating zoos
were arranged and performed together with the
person in charge of each center, who provided any
information requested by the evaluators. Each zoo
was visited (and its enclosures assessed) by a single
evaluator, who took photographs of each enclosure
and performed the evaluation supported by a data
sheet (‘‘Appendix 1’’). When a species was held in
more than one enclosure in the same zoo, the
enclosure with more specimens was selected for
evaluation. After the visit, the evaluators and the
research director met, to review and confirm the
results.
Once the enclosures were classified as secure and
non-secure, seven variables were analyzed to assess
their effect on the variable ‘‘enclosure security’’: (1)
Taxonomic group of the species held: mammals,
birds, reptiles, amphibians, fish and invertebrates; (2)
Species hazardousness to people (defined as species
capable of causing harm to their keepers or to the
public due to their physical strength or specific
weapons including poison and behavior; EAZA
2008): harmless versus hazardous species, according
to the list of hazardous species of the European
Association of Zoos and Aquaria (hereafter EAZA);
(3) Species natural distribution: indigenous versus
non-indigenous species (i.e. NIS) to the Spanish
territory, according to the National Catalogue of
Threatened Species (Spanish Ministry for the Envi-
ronment 2003); (4) Species invasiveness: invasive
(i.e. IAS) versus non-invasive species, according to
the European Inventory of Invasive Species for the
123
M. C. Fàbregas et al.
Spanish region (DAISIE 2008); (5) Enclosure acces-
sibility: walk-in enclosures (i.e. where the public is
allowed to enter the enclosure) versus enclosures
observable from outside; (6) Existence of a qualified
curator (i.e. a curator with at least a MSc in Biology)
in charge of the zoological collection at the zoo where
the evaluated enclosure belonged to: presence versus
absence of a qualified curator in staff; (7) Membership
of the center being evaluated to a professional
association of zoos (in this case, Asociación Ibérica
de Zoos y Acuarios, hereafter AIZA): AIZA members
versus non-AIZA members. Firstly, each of the
explanatory variables was analyzed with a bivariate
procedure (chi-squared test) to assess its effect on the
dependent variable (i.e. enclosure security). Then all
variables were analyzed together using a multivariate
analysis (forward stepwise logistic regression model)
to detect which of them better predicted enclosure
security (secure/non-secure) while addressing inter-
dependence relationships among the explanatory
variables. The chi-squared based Hosmer and Lem-
eshow test was used to test the overall fit of the logistic
model, and the Wald statistic to test the significance of
individual logistic regression coefficients for each of
the explanatory variables (Likelihood Ratio method).
Statistical significance was set at a = 0.05 for all
tests.
Results
We found that 221 out of the 1,568 evaluated
enclosures were non-secure so therefore the animals
could possibly escape (14.09% of the total). Such
enclosures were widely distributed among 47 out of
the 63 participating zoos, revealing that 74.60% of
the zoos in the sample had at least one non-secure
enclosure in their facilities (Fig. 1). A deficiency in
the suitability of the physical barrier was the main
cause for lack of security, affecting 71% of the non-
secure enclosures (157 enclosures). Animal release
by the public was possible in 44.30% of the 221 cases
(98 enclosures), and in 15.38% of the cases (34
enclosures), lack of security was a combination of
both aspects.
Table 1 summarizes the results regarding taxo-
nomic classification of the animals held at the
evaluated enclosures. Our data indicated that over
half of the non-secure enclosures housed birds
The risk of zoological parks
40
Error bars: 95,00% CI
30
20
10
0 0.006) and enclosures in zoos belonging to AIZA
1-20% 21-40% 41-60% 61-80%
Fig. 1 Zoological parks classified by their percentage of non-
secure enclosures in the evaluated sample. The horizontal axis
represents the percentage of non-secure enclosures in a
zoological park. Numbers in the vertical axis stand for the
frequency of zoological parks within each of the categories
indicated in the horizontal axis
(56.11%), followed by mammals and then reptiles.
Birds not only had the highest representation in the
sample (36.28% of the evaluated enclosures held
birds), but also were the zoological group with the
highest proportion of non-secure enclosures (21.79%
of the birds were held at non-secure enclosures).
Pelecanifomes and Anseriformes were the taxonomic
orders with highest proportion of non-secure enclo-
sures (63.34 and 47.92% respectively).
Non-secure enclosures held 183 different species
(Table 1), 141 of these were NIS to the Spanish
territory. As some species were housed in more than
one zoo, the total number of non-secure enclosures
housing NIS was higher (167 enclosures). Addition-
ally, 21 enclosures were found to house species listed
in the European Inventory of Alien Invasive Species
(DAISIE 2008). The animals held at those 21 non-
secure enclosures belonged to 17 species, where ten
of them were reported as established (i.e. the species
has formed self-reproducing populations where intro-
duced, DAISIE 2008) in some Spanish areas
(Table 2), and three species (coypu, Myocastor coy-
pus; sacred ibis, Threskiornis aethiopicus, and red-
eared slider, Trachemys scripta) were identified as
IAS (DAISIE 2008). It is worth mentioning that
although the sacred ibis was eradicated from the
Spanish peninsula in 2001 (Clergeau and Yésou
2006), we found a non-secure enclosure housing this
3631
species at one zoo located near the area where the
species had once been eradicated.
Six of the seven explanatory variables analyzed
were found to have an effect on enclosure security.
The distribution of secure and non-secure enclosures
varied depending on the taxonomic group of the
species under evaluation (v2 = 58.444, df = 5,
P \ 0.0001). Likewise, enclosures housing hazard-
ous species (v2 = 4.578, df = 1, P = 0.032), walk-in
enclosures (v2 = 22.409, df = 1, P \ 0.0001), enclo-
sures in zoos with a qualified curator in charge of
the zoological collection (v2 = 7.596, df = 1, P =
(v2 = 32.580, df = 1, P \ 0.0001) tended to be
secure against animal escape. Additionally, the distri-
bution of secure and non-secure enclosures was also
significantly different for the variable ‘‘invasiveness
of the species’’ (v2 = 5.360, df = 1, P = 0.021), but
in this case the percentage of non-secure enclosures
was higher when the enclosures held an IAS
(22.10%) than when the species held was a non-
invasive one (13.58%). The only variable that did not
significantly affect enclosure security was the species
natural distribution (indigenous vs. non-indigenous
species or NIS) (v2 = 0.030, df = 1, P = 0.863).
The model generated in the logistic regression
procedure fitted the analyzed data (Hosmer and
Lemeshow test: v2 = 16.731, df = 6, P = 0.019),
selecting the species taxonomic group, enclosure
accessibility, and membership to a professional
association of zoos (i.e. AIZA) as the independent
variables that better explained enclosure security
(Table 3). Such variables predicted 86.60% of the
cases correctly.
Discussion
Reports of animals escaping from zoos have been
previously documented worldwide (Csurhes 2003;
Jiguet et al. 2008). The data presented here relates to
the risk of potential escape of zoo animals due to lack
of security at their enclosures, instead of examples
about actual escapes. We found that 14% of the
evaluated enclosures were non-secure against animal
escape, either due to problems associated with the
physical barrier surrounding the enclosure and/or the
possibility of the public to release the animals. Given
that 75% of all the Spanish zoos participated in the
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Table 2 Species listed in the alien invasive species European inventory for the Spanish region (DAISIE 2008) and housed at non-
secure enclosures
Alien species Number of Colonization Colonization Colonization Invasive
non-secure status in Spanish status in Balearic status in Canary
enclosures Peninsula Islands Islands

Mammalia
Myocastor coypus 1 Established Absent Absent Yes
Aves
Agapornis personatus 1 Established Not established Not established No
Alopochen aegyptiacus 1 Not established Not established Absent No
Amazona aestiva 1 Not established Not established Absent No
Aratinga acuticaudata 1 Established Absent Absent No
Cygnus atratus 2 Not established Not established Absent No
Lamprotornis purpureus 1 Absent Absent Not established No
Nandayus nenday 1 Not established Absent Established No
Pavo cristatus 1 Absent Absent Not established No
Phasianus colchicus 1 Established Absent Absent No
Poicephalus senegalus 1 Not established Not established Established No
Streptopelia roseogrisea 1 Established Absent Established No
Threskiornis aethiopicus 1 Extinct Absent Not established Yes
Reptilia
Elaphe guttata 1 Not established Absent Not established No
Iguana iguana 2 Not established Absent Established No
Testudo graeca 1 Absent Established Not established No
Trachemys scripta 3 Established Established Established Yes
Total 21
Colonization status: Extinct (Once established, now extinct); Not established (the species has not formed self-reproducing
populations); Established (the species has formed self-reproducing populations where introduced); Absent (no records of presence of
the species for that region). (DAISIE 2008)

study, we consider that our results reflect quite
accurately the situation in Spain. As our results
correspond to a sample, and free-flying birds were not
analyzed in our study (but comprise part of some
zoological collections), the actual number of enclo-
sures from which animals could potentially escape
could reach near one thousand. This is the first time
(to our knowledge) that the risk of escape from zoo
enclosures has been evaluated. Similar analyses in
other regions would help to address the importance of
zoos as potential pathways for the introduction of
NIS, especially considering that in Europe alone, 82
non-indigenous terrestrial vertebrate species have
been introduced as a consequence of escapes from
zoos (DAISIE 2008).
Preventing the introduction of NIS has been
regarded as the most direct and potentially effective
means to reduce the threat to biodiversity from IAS
(Carlton and Ruiz 2005). However, not all the species
liable to escape represent an actual threat to the
ecosystem. First of all, as a general trend most
organisms die in transit or soon after release (Lodge
1993). Moreover, in the particular case of escapes,
the success of any given animal in completely
achieving freedom (other than chance) depends on
its particular physical features and behavior. We
would expect large body-sized species less capable of
succeeding at their escape than small ones, as the
former are more conspicuous to people. In the same
way, hazardous species are probably less capable to
reach the wild due to the imminent hazard they
represent to the general public. Locomotion patterns
also play an important role in the escape, both in
terms of speed and fashion; those animals able to fly
are more prone to succeed in their escape, simply
because they become harder to catch successfully.

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The risk of zoological parks 3633

Table 3 The relative importance of the independent variables ecosystems were former pets once released or
on enclosure security in the forward stepwise logistic regres- escaped into the wild (e.g. green iguanas, Iguana
sion model. Likelihood ratio test was used for significance
iguana or red-eared sliders, Trachemys scripta).
Variables in the equation Walda df P-value Considering that these species are quite frequent in
zoos, they represent an excellent opportunity to raise
AIZA membership 25.432 1 \0.001
awareness among the visiting public about the
Taxonomic group 59.672 5 \0.001
ecological harm associated with the release of non-
Enclosure accessibility 35.606 1 \0.001
indigenous fauna into the wild.
Constant 24.727 1 \0.001
Zoos belonging to a professional association (i.e.
b
Variables not in the equation Score df P-value AIZA in the case of Spain) were found to have less
Species hazardousness 2.254 1 0.133
non-secure enclosures than non-members. This could
be explained by several factors. Firstly, professional
Species natural distribution .625 1 0.429
associations are strongly committed to global con-
Species invasiveness .307 1 0.580
servation as stated in the Zoo and Aquaria Conser-
Qualified curator in staff .015 1 0.903
vation Strategy (WAZA 2005). In fact, the Strategy
a
Wald statistic specifically acknowledges the problem of biological
b
Rao’s efficient score invasions by stating that zoos ‘‘should ensure that
exotic (i.e. non-indigenous) animals in their care do
Unfortunately, over half of the non-secure enclosures not escape and do not pose a risk to indigenous
in the sample held birds, most of them NIS to the species’’ (WAZA 2005). Another important factor is
Spanish territory. Thirteen of those non-secure qualifying for membership of professional associa-
enclosures held bird species listed by the European tions. In order to qualify zoos are evaluated on a
Inventory of Alien Invasive Species, one of them comprehensive set of aspects, including security of
(Threskiornis aethiopicus) already invasive (DAISIE the enclosures to prevent animal escape, where the
2008). The fact that birds are the zoological group suitability of the physical barrier (in terms of the
with more enclosures with potential risk of escape is design and the construction materials) as well as its
a reason for concern as many species within this maintenance are assessed. However, as we detected
group have all the characteristics mentioned above. non-secure enclosures at AIZA zoos, establishing
Therefore, special attention should be paid to those stricter accreditation processes in the future could
enclosures holding species that are capable of flying, probably reduce the number of non-secure enclo-
harmless to the public (especially if they are appar- sures, and therefore the potential risk of zoos as
ently naı̈ve, like former pet species), are small sized, introduction routes for NIS. In this regard, the
or satisfy all the criteria discussed above. existence of a legal framework within the European
Although IAS are acknowledged as a threat to Union that requires governments and/or local author-
biodiversity by the mission statements and codes of ities of all Member States to carry out inspection and
practice of the zoo community (AIZA 2008; EAZA authorization processes of existing and new zoos,
2001, 2008; IUCN 2002b; WAZA 2005), according also represents a powerful way to improve zoo
to our results, the potential environmental risk posed security.
by NIS or IAS is not reflected in the security of their
enclosures. The fact that most IAS are not directly Management perspective and future directions
harmful to humans could explain this lack of security.
Our data seem to support such an idea, as none of the Non-indigenous species are a global concern and their
non-secure enclosures housing NIS (listed by the control should be promoted internationally (Mooney
European Inventory of Invasive Species, DAISIE 1999). Although our study sample was limited to
2008) were hazardous to humans. Furthermore, none Spain, a similar situation might be occurring in other
of the species (other than a few jellyfishes) listed in European countries, as well as in other regions
‘‘the 100 worst invasive species for Europe’’ (DAI- worldwide. We consider that enclosure security in
SIE 2008) are directly hazardous to humans. In this zoos should be taken more seriously as these centers
sense, some NIS that have succeeded in invading new (as shown in our results) are a potential pathway for

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the introduction of NIS. From our point of view, the
situation could be managed better by the zoo commu-
nity itself through a specific set of measures, including
more demanding accreditation processes by profes-
sional associations. Other strategies could include the
identification and labelling of those species especially
harmful for the environment, both to warn zoo
personnel about the potential risk of NIS within their
animal collection as well as raising awareness
amongst the public about the risk of releasing NIS
into the wild. Governmental agencies and departments
in those countries which already consider IAS in their
legal frameworks and policies should accurately
address enclosure security in their official inspections
and authorization processes. As for those countries
which still lack specific legislation regarding mainte-
nance of NIS or IAS in zoos, it is now an urgent issue
that policymakers take action as preventing the
introduction of NIS is the most effective (and less
expensive) measure to protect ecosystems against
biological invasions.
Acknowledgments We thank the Spanish Ministry for the
Environment for funding the broader study that generated the
data we used in this paper. We also want to thank the par-
ticipating zoos for their assistance during this study. The
manuscript greatly benefited from comments from Dr.
V. Rodilla (Universidad Cardenal Herrera, Spain) and Dr.
S. Sánchez-Peña (Universidad Autónoma Agraria Antonio
Narro, México), as well as from those made by two anon-
ymous referees.
Appendix 1
Questions regarding the security of the enclosures
against animal escape included in the data sheets used
by the evaluators when assessing enclosure security
(from Guillén-Salazar 2003). For the purpose of this
study an enclosure was considered ‘‘secure’’ only when
both conditions were simultaneously met. Otherwise
the enclosure was categorized as ‘‘non-secure’’.
Condition 1 The enclosure has a complete, well
maintained, and appropriate physical barrier to
prevent the escape of the animals housed within
(including sewage lines, filtration systems and, in
general, any opening or valve that could allow the
escape of an animal or part of it such as eggs). Each
of the following questions should be answered
negatively to meet this condition.
123
M. C. Fàbregas et al.
a. Could the barrier be knocked down by the
animals held in the enclosure?
b. Could the animals exit the enclosure by leaping
or climbing the barrier (including the use of
vegetation, tools, etc.)?
c. Could the animals escape by digging under the
barrier?
d. Could the animals go through the barrier (espe-
cially young individuals)?
e. Are there any pipes or ducts (sewage lines, water
channels, etc.) in the enclosure that could allow
the escape of the animals held in it?
f. In the case of being a drive through or walk
through enclosure, a double gate entry and exit
system should be in place with sufficient space to
allow the gates to be securely closed at the front
and rear of any vehicle (or person) which may
enter or need to enter the enclosure. Could the
animals held inside exit the enclosure through
any of the gates?
g. Could the integrity of the barrier be compro-
mised by any external factor (e.g. a fallen tree on
the barrier)?
Condition 2 The public cannot release the animals
held at the enclosure directly or indirectly. Each of
the following questions should be answered nega-
tively to meet this condition.
a. Could the public capture the animals and remove
them from the enclosure?
b. Are there any doors or windows that could be
opened by the public due to lack of continuous
supervision by zoo personnel and/or because they
are not properly locked?
c. Are there any objects surrounding the enclosure
such as rocks, branches or forgotten tools that
could be used to free the animals held at the
enclosure (e.g. by tearing down the fences
comprising the physical barrier of the enclosure)?
Note: Violations with premeditation, planning
and preparation that could be considered as an
offense are not considered.
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