Misconception and mismanagement of invasive species: The paradoxical case of an alien ungulate in Spain

Received: 20 October 2017 Accepted: 21 January 2018
DOI: 10.1111/conl.12440
POLICY PERSPECTIVE
Misconception and mismanagement of invasive species:
The paradoxical case of an alien ungulate in Spain
Jorge Cassinello
Estación Experimental de Zonas Áridas
(EEZA-CSIC), Carretera de Sacramento
s/n, La Cañada de San Urbano, 04120 Almería,
Spain
Correspondence
JorgeCassinello,EstaciónExperimental de
ZonasÁridas (EEZA-CSIC), Carretera de
Sacramento s/n, La Cañada de SanUrbano,
04120 Almería, Spain.
Email: jorge.cassinello@csic.es
Abstract
Scientific evidence should dominate in any management decision dealing with alien
species. It is also essential for all stakeholders to agree on the terminology used to
avoid undesirable misinterpretations. A well-known example is the use of the term
“invasive,” which has two basic meanings, one as a biogeographic criterion and the
other as an impact criterion. The aoudad (Ammotragus lervia) is a North African
ungulate introduced in Spain, whichwas labeled “invasive” by Spanish authorities due
to misreading of the term used by early studies. Indeed, to date, there are no conclusive
empirical data showing negative effects of the aoudad on native flora and fauna.
Recent studies have shown that its closest native ungulate, the Iberian ibex (Capra
pyrenaica), has expanded throughout territories already occupied by the aoudad, without
any apparent conflict.Aoudad diet selection studies also showthem to be markedly
grazers, so its role in the Mediterranean trophic network might be similar to that of
extinct wild ungulates that fed in natural meadows, maintaining landscapes heterogeneous.
New opportunities for its study are opening, particularly in Iberian semiarid
lands. Unfortunately though, its current simplistic definition as an invasive species
keeps in suspense its eventual eradication throughout the country.
KEYWORDS
Alien species, Ammotragus, biodiversity conservation, biological invasions, conservation policy, ecological
knowledge, empirical data, invasive species, native species, wildlife management
1 INTRODUCTION
Public and private environmental institutions are making
tremendous economic and legislative efforts to protect and
conserve biodiversity and natural resources from so-called
“invasive alien species,” generally considered a major worldwide
threat to biodiversity (Bergmans & Blom, 2001). Not in
vain, as in the United States alone they have been estimated
to cause environmental damage and economic loss of about
$120 billion per year (Pimentel, Zuniga, & Morrison, 2005).
The great majority of natural ecosystems are already suffer-
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Copyright and Photocopying: © 2018 The Authors. Conservation Letters published by Wiley Periodicals, Inc.
ing from some degree of alteration caused by human activity
(habitats altered by roadways, rural areas, or agricultural fields
and crop lands), so that some of the first aliens that appeared
in these areas tended to be human commensals, species associated
with human-altered habitats (Sax & Brown, 2000).
However, when the new discipline in invasion ecology
emerged, no definition of the term “invasive species” was
attempted (Elton, 1958). This has given rise to a multitude
of disagreements, misconceptions, and misunderstanding of
the growing amount of literature on the phenomenon being
published and has led to numerous initiatives calling for a
Conservation Letters. 2018;e12440. wileyonlinelibrary.com/journal/conl 1 of 5
https://doi.org/10.1111/conl.12440
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FIGURE 1 Aoudad males kept in captivity at the EEZA facilities.
© EEZA-CSIC.
consensus (Colautti & MacIsaac, 2004; Valéry, Fritz,
Lefeuvre, & Simberloff, 2008).
2 DEFINING INVASIVENESS
In the scientific literature, two definitions predominate, one
referring to a biogeographic invasion (equivalent to merely
colonizing in time and space) and the other indicative of
negative impacts on the environment, i.e., a biogeographic
criterion versus an impact criterion (Valéry et al., 2008).
Early studies on the subject tended to relate invasion to the
geographic expansion of species, whether human-mediated
or not (Vermeij, 1996; Williamson, 1996). However, at the
beginning of the 21st Century, the International Union for
Nature Conservation (IUCN) and the Convention on Biological
Diversity (CBD) defined alien invasive species as alien
species that threaten the biodiversity of the host ecosystem,
disregarding their capacity for spreading (CBD, 2002; IUCN,
2000). Consequently, and under this premise, public and private
institutions devoted to the protection of biodiversity have
embraced this definition, which is currently the one used
by most managers, politicians, and environmentalists, despite
there still not being agreement on its use among ecologists
and zoologists (see a recent review by Wijesundara, 2010).
As a consequence of this lack of consensus, when referring
to particular studies and references dealingwith “invasive
species,” it is crucial to identify precisely what the authors
meant by it, in order to cite them properly and understand their
results or conclusions. Unfortunately, this is not always done,
and therefore, misinterpretations may emerge.
3 INVASIVE SPECIES
Alien species which are harmful to the environment require
special attention by authorities and managers to decrease
their deleterious effects (Pallewatta, Reaser, & Gutierrez,
2003). Under some circumstances, eradication programs
should be carried out (Myers, Simberloff, Kuris, & Carey,
2000), whereas in others, coexistence of native and nonnative
species might be the most reasonable management
strategy (Schlaepfer, Sherman, Blossey, & Runge, 2005). Furthermore,
although the precautionary principle should be followed
when dealing with alien species (Rogers, Sindent, &
De Lacy, 1997), in many instances there is no actual or
updated knowledge on their ecological effects (Thomas &
Palmer, 2015), and taking a decision on their management
strategy may be untimely, controversial or just plain wrong
(see below). Therefore, defining how to handle the impact of
alien species is a must (Jeschke et al., 2014).
Habitat alteration, along with the decline in natural predator
populations, associated with human activities (e.g., persecution,
poaching, and unsustainable hunting), can exacerbate
an increase in numbers of native species (Côté, Rooney, Tremblay,
Dussault, & Waller, 2004; Garrott, White, & Vanderbilt
White, 1993), which in turn may become invasive, i.e., harmful
to their environment (Carey, Sanderson, Barnas, & Olden,
2012). A paradigmatic example is that of the wild boar (Sus
scrofa) in its native range of distribution, where it tends to be
associated with human sources of food (e.g., food containers
and trashcans in the outskirts of towns), increasing in numbers
in such high densities that it causes adverse effects (Apollonio,
Andersen, & Putman, 2010). Consequently, identifying invasive
native species is also crucial in any profound examination
of ecological issues related to wildlife management and
policy.
Therefore, the term “invasive” should be applicable to
native species as well as non-native species.
4 THE CASE OF THE AOUDAD
The aoudad or Barbary sheep (Ammotragus lervia Pallas,
1777; Figure 1) is a North African caprid widely introduced
in several countries for hunting (Cassinello, 2015; Cassinello
et al., 2008). The main wild-ranging alien populations are
found in the United States (mainly Texas, New Mexico, and
California) and Spain (southeastern mainland and La Palma
Island, Canary Islands). Paradoxically, while these alien populations
have settled and expanded their ranges, the species is
threatened in its native area of distribution (Cassinello et al.,
2008). So far, and apart from the population located in La
Palma Island, where its Macaronesian flora is not evolutionarily
adapted to the presence of large herbivores such as the
aoudad, there is no empirical evidence related to any negative
impact on native fauna or flora (Cassinello, 2015).
The first studies dealing with the presence of the species in
Spain expressed serious concern for potential harm to native
flora and competition for resources with the native Iberian
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ibex (Capra pyrenaica Schinz, 1838), taxonomically the
closest kin among native Iberian ungulates (Acevedo,
Cassinello, Hortal, & Gortázar, 2007; Cassinello, Acevedo,
& Hortal, 2006). In these studies, the species was depicted
as invasive, but used the term in its biogeographic sense
(“The aoudad has shown a formidable capacity to establish,
spread, and extend its distribution (…), characteristics typical
of biological invasions (Williamson, 1996)”). In the Region
of Murcia alone, the aoudad population is as high as 2,000
free-ranging individuals.
Not critically reading the term “invasive” led to the inclusion
of the aoudad in the first Spanish Catalogue of Invasive
Alien Species (Ministerio deMedio Ambiente, yMedio Rural
yMarino, 2011), although with some basically political peculiarities
which prevented the populations present in the Region
of Murcia from being included in the Catalogue. This bizarre
procedure led environmental associations to appeal for a general
classification of the aoudad as an invasive alien species
throughout the country, an appeal which was finally approved
by the Spanish High Court (Tribunal Supremo, 2016).
However, recent studies dealing with aoudad feeding habits
have shown that the species is primarily a grazer, actively
selecting forbs and grasses when available (Ben Mimoun &
Nouira, 2015; Miranda et al., 2012); while their incidence on
woody plants is similar to that of native herbivore ungulates,
not showing particularly higher negative effects on threatened
plants (Velamazán, San Miguel, Escribano, & Perea, 2017).
The presence of wild grazers may be crucial to the preservation
of mosaic landscapes in Mediterranean habitats (Malek
& Verburg, 2017), as it is widely acknowledged that grazers,
along with browsers, allow open pastures to be maintained
by reducing shrubland colonization (Odum, 1969). These heterogeneous
landscapes are fundamental to the preservation of
biodiversity and species richness in ecosystems (Stein, Gerstner,
& Kreft, 2014). The fact is that extant large wild herbivores
in the Iberian Peninsula are basically browsers (Gebert
& Verheyden-Tixier, 2001; Martínez, 2010), and apart from
decreasing livestock activity, no specialist grazers are present
any longer. Thus, it would not be venturous to expect beneficial
outputs from the presence of new wild grazers, although
from an exotic origin (Fernández-Olalla, Martínez-Jauregui,
Perea, Velamazán, & San Miguel, 2016).
Furthermore, Iberian ibex populations have recently been
showing impressive recolonization in southeastern Spain,
reaching areas previously occupied by aoudads. However, the
presence of theNorth African ungulate does not seem to affect
ibex range expansion. In fact, it is rather the opposite, as in
some mountainous areas the native ungulate seems to be displacing
the exotic one (Eguía et al., 2015).
Despite current empirical evidence showing that the effects
of the aoudad, both in the United States and the Spanish mainland,
are not harmful, if not beneficial (Cassinello, 2015),
the species is still classed as invasive by Spanish authorities
(Ministerio de Agricultura, Alimentación yMedio Ambiente,
2013), leading to the startup of eradication programs in some
of its distribution areas (Consejería de Agua, Agricultura y
Medio Ambiente, 2017). Another consequence of this policy
is that a threatened species in its native range of distribution is
being subject to eradication in exotic areas, which might well
become species reservoirs if no harmful effects are detected
(Garzon-Machado, del-Arco-Aguilar, & Perez-de-Paz, 2012;
Marchetti, & Engstrom, 2016).
This is the first evidence of an unprecedented management
policy based on an erroneous application of scientific
evidence due to the misleading terminology applied to alien
species, interpreting “invasive” as “harmful” instead of “colonizing.”
5 CONCLUSIONS
Knowledge of whether an alien species poses a risk to the
host environment, based on scientific data and proper identification
of the results and conclusions in the available literature,
is crucial to its management (Valéry et al., 2008). Invasive
species, sensu impact criterion, may be either exotic or
native (Carey et al., 2012), and their management and control
should always be implemented according to scientific and
empirical evidence. Apart from proper management policies,
it is also important to implement further evaluation procedures
enabling institutions to find out what benefits, if any,
have been achieved (Ferraro & Pattanayak, 2006).
The alien aoudad, depicted as harmful in all the territories
where it is present, is currently included in the Spanish Catalogue
of Invasive Alien Species. This inclusion is based on
a misinterpretation of the scientific literature available, and
according to current findings, consideration of the populations
located in the southeast of the Iberian Peninsula as invasive
is ungrounded (Cassinello, 2015). A recent ruling by the
Spanish High Court promotes its total eradication in the country,
even though the ecological consequences of a massive
eradication program are unforeseeable. Nevertheless, political
commitments may still vary, as the Spanish Ministry of
Environment is currently holding new meetings on this issue
with concerned aoudad management stakeholders, including
scientists devoted to their study. Hope for a better management
policy based on actual ecological facts is still in the air.
6 ADDENDUM
A few days after this manuscript was submitted, the Spanish
Parliament approved a modification of the Spanish Law
42/2007 on the Natural Heritage and Biodiversity (Jefatura
del Estado, 2007), so that invasive species that can be of eco4
of 5 CASSINELLO
nomic interest through fishing or hunting will be allowed to be
sustainably managed in areas where they were present before
Ley 42/2007 was approved, in December 2007; whereas in
recently colonized areas, they should be controlled and eventually
eradicated (Proposición de Ley, 2017). This legal modification,
however, does not raise any change in invasiveness
status of such species, as it is only based on socioeconomic
profits in rural areas; it may also change over time if parliamentarymajorities
do so. Therefore, the issue on aoudad invasiveness
status remains to be addressed and resolved.
ORCID
Jorge Cassinello http://orcid.org/0000-0001-8781-2009
REFERENCES
Acevedo, P., Cassinello, J., Hortal, J., & Gortázar, C. (2007). Invasive
exotic aoudad (Ammotragus lervia) as a major threat to native Iberian
ibex (Capra pyrenaica): A habitat suitability model approach. Diversity
and Distributions, 13, 587–597.
Apollonio, M., Andersen, R., & Putman, R. (2010). Present status and
future challenges for European ungulate management. In M. Apollonio,
R. Andersen, & R. Putman (Eds.), European ungulates and
their management in the 21st Century (pp. 578–604). Cambridge,
UK: Cambridge University Press.
Ben Mimoun, J., & Nouira, S. (2015). Food habits of the aoudad
Ammotragus lervia in the Bou Hedma mountains, Tunisia. South
African Journal of Science, 111, Art. #2014-0448. https://doi.org/
10.17159/sajs.2015/20140448
Bergmans,W.,&Blom, E. (Eds.). (2001). Invasive plants and animals. Is
there a way out? Amsterdam: The Netherlands Committee for IUCN.
Carey, M. P., Sanderson, B. L., Barnas, K. A., & Olden, J. D. (2012).
Native invaders – challenges for science, management, policy, and
society. Frontiers in Ecology and the Environment, 10, 373–381.
Cassinello, J. (2015). Ammotragus lervia (aoudad). In CABI (Ed.),
Invasive species compendium. Wallingford, UK: CAB International.
Retrieved from http://www.cabi.org/isc
Cassinello, J., Acevedo, P., & Hortal, J. (2006). Prospects for population
expansion of the exotic aoudad (Ammotragus lervia; Bovidae) in the
Iberian Peninsula: Clues from habitat suitability modelling. Diversity
and Distributions, 12, 666–678.
Cassinello, J., Cuzin, F., Jdeidi, T., Masseti, M., Nader, I., & de
Smet, K. (2008). Ammotragus lervia. The IUCN Red List of
Threatened Species 2008: e.T1151A3288917. https://doi.org/
10.2305/IUCN.UK.2008.RLTS.T1151A3288917.en. Downloaded
on 10 February 2018.
CBD. (2002). Decision VI/23: Alien species that threaten ecosystems,
habitats or species. Retrieved from https://www.cbd.int/kb/record/
decision/7197?RecordType=decision&Subject=IAS
Colautti, R. I., & MacIsaac, H. J. (2004). A neutral terminology to define
‘invasive’ species. Diversity and Distributions, 10, 135–141.
Consejería de Agua, Agricultura yMedio Ambiente. (2017). Proyecto de
Plan de Gestión para el Control y Erradicación del Arruí (Ammotragus
lervia) en la Región de Murcia. Unpublished Report.
Côté, S. D., Rooney, T. P., Tremblay, J. P., Dussault, C., &Waller, D. M.
(2004). Ecological impacts of deer overabundance. Annual Review of
Ecology, Evolution, and Systematics, S 35, 113–147.
Eguía, S., Martínez-Noguera, E., Botella, F., Pascual, R., Giménez-
Casalduero, A., & Sánchez-Zapata, J. A. (2015). Evolución del área
de distribución del arruí (Ammotragus lervia Pallas 1777) y la cabra
montés (Capra pirenaica Schinz, 1838) en la Región de Murcia. V
Congreso de la Naturaleza de la Región de Murcia, 2015. Asociación
de Naturalistas del Sureste, Murcia, Spain.
Elton, C. S. (1958). The ecology of invasions by animals and plants.
London, UK: Methuen.
Fernández-Olalla,M., Martínez-Jauregui,M., Perea, R., Velamazán,M.,
& San Miguel, A. (2016). Threat or opportunity? Effects of an alien
ungulate on the highly diverse vegetation of southeastern Spain. Journal
of Arid Environments, 129, 9–15.
Ferraro, P. J., & Pattanayak, S. K. (2006). Money for nothing? A call for
empirical evaluation of biodiversity conservation investments. PLoS
Biol, 4, e105.
Garrott, R. A.,White, P. J., & Vanderbilt White, C. A. (1993). Overabundance:
An issue for conservation biologists? Conservation Biology,
7, 946–949.
Garzon-Machado, V., del-Arco-Aguilar, M. J., & Perez-de-Paz, P. L.
(2012). Threat or threatened species? A paradox in conservation biology.
Journal for Nature Conservation, 20, 228–230.
Gebert, C., & Verheyden-Tixier, H. (2001). Variations of diet composition
of red deer (Cervus elaphus L.) in Europe. Mammal Review, 31,
189–201.
IUCN. (2000). IUCN guidelines for the prevention of biodiversity
loss due to biological invasion. The World Conservation Union
(approved by the IUCN Council, February, 2000). Retrieved from
https://portals.iucn.org/library/efiles/documents/Rep-2000-052.pdf.
Jefatura del Estado. (2007). Ley 42/2007, de 13 de diciembre, del Patrimonio
Natural y de la Biodiversidad. B.O.E, 299, 51275–51327.
Jeschke, J. M., Bacher, S., Blackburn, T. M., Dick, J. T. A., Essl, F.,
Evans, T., … Kumschick, S. (2014). Defining the impact of nonnative
species. Conservation Biology, 28, 1188–1194.
Malek, Z., & Verburg, P. (2017). Mediterranean land systems: Representing
diversity and intensity of complex land systems in a dynamic
region. Landscape Urban Plan, 165, 102–116.
Marchetti, M. P., & Engstrom, T. (2016). The conservation paradox of
endangered and invasive species. Conservation Biology, 30, 434–
437.
Martínez, T. (2010). Selección y estrategia alimentaria de los machos,
hembras y jóvenes de cabra montés (Capra pyrenaica Schinz, 1838)
en el sureste de España. Galemys, 22, 483–515.
Ministerio de Agricultura, Alimentación y Medio Ambiente. (2013).
Real Decreto 630/2013, de 2 de agosto, por el que se regula el
Catálogo español de especies exóticas invasoras. B.O.E, 185, 56764–
56786.
Ministerio de Medio Ambiente, y Medio Rural y Marino. (2011). Real
Decreto 1628/2011, de 14 de noviembre, por el que se regula el listado
y catálogo español de especies exóticas invasoras. B.O.E, 298,
132711–132735.
Miranda, M., Sicilia, M., Bartolomé, J., Molina-Alcaide, E., Gálvez-
Bravo, L., & Cassinello, J. (2012). Contrasting feeding patterns of
CASSINELLO 5 of 5
native red deer and two exotic ungulates in a Mediterranean ecosystem.
Wildlife Research, 39, 171–182.
Myers, J. H., Simberloff, D., Kuris, A. M., & Carey, J. R. (2000). Eradication
revisited: Dealing with exotic species. Trends in Ecology &
Evolution, 15, 316–320.
Odum, E. P. (1969). The strategy of ecosystem development. Science,
164, 262–270.
Pallewatta, N., Reaser, J.K., & Gutierrez, A. (Eds.). (2003). Prevention
and management of invasive alien species: Proceedings of a workshop
on forging cooperation throughout South and Southeast Asia.
Cape Town, South Africa: Global Invasive Species Programme.
Pimentel, D., Zuniga, R., & Morrison, D. (2005). Update on the environmental
economic costs associated with alien-invasive species in the
United States. Ecological Economics, 52, 273–288.
Proposición de Ley. (2017). 122/000137 Proposición de Ley de modificación
de la Ley 42/2007, de 13 de diciembre, del Patrimonio Natural
y de la Biodiversidad. B.O.C.G. Serie B, 170–1, 1–5.
Rogers, M. F., Sindent, J. A., & De Lacy, T. (1997). The precautionary
principle for environmental management: A defensive-expenditure
application. Journal of Environmental Management, 51, 343–360.
Sax, D. F., & Brown, J. H. (2000). The paradox of invasion. Global Ecology
and Biogeography, 9, 363–371.
Schlaepfer, M. A., Sherman, P.W., Blossey, B., & Runge, M. C. (2005).
Introduced species as evolutionary traps. Ecology Letters, 8, 241–
246.
Stein, A., Gerstner, K., & Kreft, H. (2014). Environmental heterogeneity
as a universal driver of species richness across taxa, biomes and
spatial scales. Ecology Letters, 17, 866–880.
Thomas, C. D.,&Palmer, G. (2015). Non-native plants add to the British
flora without negative consequences for native diversity. Proceedings
of the National Academy of Sciences of the United States of America,
112, 4387–4392.
Tribunal Supremo. (2016). Sentencia de 16 de marzo de 2016, de la Sala
Tercera del Tribunal Supremo. B.O.E, 146, 41761–41762.
Valéry, L., Fritz, H., Lefeuvre, J. -C., & Simberloff, D. (2008). In search
of a real definition of the biological invasion phenomenon itself. Biological
Invasions, 10, 1345–1351.
Velamazán, M., San Miguel, A., Escribano, R., & Perea, R. (2017).
Threatened woody flora as an ecological indicator of large herbivore
introductions. Biodiversity and Conservation, 26, 917–930.
Vermeij, G. J. (1996). An agenda for invasion biology. Biological Conservation,
78, 3–9.
Williamson, M. (1996). Biological invasions. London, UK: Chapman
and Hall.
Wijesundara, S. (2010). Defining invasive alien species. In B. Marambe,
P. Silva, S.Wijesundara, & N. Atapattu (Eds.), Invasive alien species
in Sri Lanka – strengthening capacity to control their introduction
and spread (pp. 1–6). Sri Lanka: Biodiversity Secretariat of the Ministry
of Environment.
How to cite this article: Cassinello J. Misconception
and mismanagement of invasive species: The
paradoxical case of an alien ungulate in Spain.
Conservation Letters. 2018;e12440. https://doi.org/
10.1111/conl.12440