Biological Conservation 159 (2013) 539–547
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Biological Conservation
journal homepage: www.elsevier.com/locate/biocon
Review
Preventing the development of dogmatic approaches in conservation
biology: A review
Alejandro Martínez-Abraín a,b,⇑, Daniel Oro b
a
b
Departamento de Bioloxía Animal, Bioloxía Vexetal e Ecoloxía, Universidade da Coruña, Facultade de Ciencias, Campus da Zapateira s/n, 15071 A Coruña, Spain
Population Ecology Group, IMEDEA (CSIC-UIB), Miquel Marquès 21, 07190 Esporles, Mallorca, Spain
a r t i c l e
i n f o
Article history:
Received 12 March 2012
Received in revised form 8 October 2012
Accepted 20 October 2012
Available online 9 February 2013
Keywords:
Dogma development
Global change
Economic crisis
Evidence-based conservation
Resource allocation
Management effectiveness
a b s t r a c t
The application of management practices based on dogmas may lead to unexpected results, and hence to
the bad allocation of economic resources. This is an especially relevant subject today given that, in a context of deep economic crisis, conservation has very limited resources. Here, we review e-alerts from 20 of
the most important journals in the field of applied conservation ecology to identify topics that are vulnerable to dogma development, and then to suggest strategies to prevent this to happen. After examining
525 pre-selected papers, we identified several major questions within the sphere of some of the main
agents of anthropogenic global change based on 129 papers. Specifically we reviewed knowledge accumulated during recent decades on the resilience of wildlife to cope with two of those agents, namely
(a) habitat fragmentation, alteration and loss; and (b) the arrival of exotic invasive species. We critically
discuss four common conservation questions within those two major areas: the pros and cons of supplementary feeding for conservation purposes, the ubiquity of the detrimental effect of invasive species and
the feasibility of its eradication, as well as the efficiency of controlling generalist predators for both game
and conservation purposes. We finally provide a list of five good practices to prevent the generation of
dogma when applying the science of conservation biology to the abovementioned agents of global
change, and as a way of optimizing the effectiveness and efficiency of biodiversity management.
Ó 2012 Elsevier Ltd. All rights reserved.
Contents
1.
2.
3.
4.
Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Methods . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Results and discussion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
3.1.
Dealing with habitat fragmentation, alteration and loss . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
3.2.
Dealing with exotic species . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Conclusions. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Appendix A. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Appendix B . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
1. Introduction
As in discussions about sport, many lay people seem to have
well-formed ideas about the most complex of conservation topics,
opinions that are often in fact based on the creation of dogmas.
⇑ Corresponding author at: Population Ecology Group, IMEDEA (CSIC-UIB),
Miquel Marquès 21, 07190 Esporles, Mallorca, Spain.
E-mail address: [email protected] (A. Martínez-Abraín).
0006-3207/$ - see front matter Ó 2012 Elsevier Ltd. All rights reserved.
http://dx.doi.org/10.1016/j.biocon.2012.10.020
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This problem, which other basic and applied sciences such as physics, chemistry or engineering do not have to confront, seriously affects the realm of biodiversity conservation, since applying
management practices based upon dogmatic ideas often leads to
unexpected results (Possingham et al., 2002; Kareiva and Marvier,
2003; Martínez-Abraín et al., 2004; Halpern et al., 2006; MartínLópez et al., 2009), with undesirable ecological and economic consequences (Cawardine et al., 2008; Floerl and Coutts, 2009; Farley,
2010; Speth, 2011). In conservation, concepts such the existence of
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‘bad’ alien species, the necessary loss of genetic diversity following
habitat fragmentation, and the probity of reintroductions, culling
programs, biological corridors and supplementary feeding have
some dogmatic component, because they are considered a priori
to be correct and efficient principles and practices. For example,
worldwide many large gull species of the genus Larus are tagged
as ‘bad’ species and are subject to culling, often without evidence
to justify such actions (e.g. Oro and Martínez-Abraín, 2006). Specifically, in the Balearic Islands, where many endemic animal and
plant species occur, ca. 25% of the regional conservation budget
during the period 1989–2003 was invested in unsuccessful campaigns to cull local yellow-legged gulls (Larus michahellis) (authors,
unpublished). Yet, gull populations decrease rapidly as soon as the
human causes of their abundance (such as landfills and fishing discards) are properly managed and today some large gull species are
even included on IUCN Red Lists (Lynas et al., 2007). As a way of
preventing undesirable situations such as the one described above,
conservation biologists began in the previous decade to send out
clear messages to managers underlining the fact that decisionmaking should be informed by accumulated scientific evidence
rather than based on personal experiences and feelings, which
may only serve to reinforce the acceptance of scientific dogma
(see e.g. Sutherland et al., 2004; Linquist, 2008). Despite the great
uncertainty that exists when dealing with the heterogeneity
inherent to biodiversity responses to environmental change and
management (Regan et al., 2005), whenever possible it is important to base decision-making on available evidence from the fields
of population, community and behavioral ecology, as well as
evolution (Soulé, 1985; Simberloff, 1988; Sutherland et al., 2004;
Martínez-Abraín and Oro, 2010). We do not claim that creation
of dogma is widespread in our times in conservation biology but
rather we aim to review counterpoints to well establish management practices as a precautionary exercise. To a large extent the
crux of the problem may stem from poor communication and
transfer of new knowledge to managers, rather than on lack of willingness of managers to keep pace with scientific advances. However it is also true that applied science is often inconclusive,
partly because dogma development not only affects managers
but also conservation scientists, and hence it becomes impossible
to advise wildlife managers properly.
Stakeholders dealing with global change often tend to take for
granted that animal and plant species have little capacity for coping with change and severe perturbations in their environments,
without human intervention (see e.g. Conant, 1988; HoeghGuldberg et al., 2008; Seddon et al., 2009; Seddon, 2010; but see
Ricciardi and Simberloff, 2008). However, change – including
long-lasting climate change – and perturbations are common factors in the evolution of organisms; thus, it is to be expected that
many such species will have behavioral and/or evolutionary mechanisms that can deal with change (Mace et al., 1998), even at its rapid current pace and severity (Oro et al., 2012). For example, many
of the plant species considered to be typical of the Mediterranean
Basin scrublands (e.g. Chamaerops, Smilax, Arbutus, Olea, Pistacia
and Phillyrea) are actually plants that evolved during the Eocene,
Oligocene and Miocene under very different environmental conditions compared to present ones, that have survived several climate
changes, in addition to profound historical anthropogenic modifications in their habitats (Herrera, 1995).
Global anthropogenic change has two major components,
namely, climate change and the set of human activities that directly affect wildlife at a global scale (MA, 2003). We chose not
to assess the ability of fauna and flora to respond to global climate
change because we wanted to focus on proximate factors whose
management by conservation practitioners (i.e. wildlife managers
from the public, private or NGO sectors) is practical in the short
term; nevertheless, the overall picture of change is more likely to
consist of an interaction between climate change and direct
anthropogenic factors (Carroll, 2007; van der Wal et al., 2008;
Heller and Zavaleta, 2009). Indeed, the linking of so many negative
trends with climate change may in fact mask the role of proximate
human-caused factors such as direct persecution or overharvesting
(see e.g. Munilla et al., 2007).
Here, we review knowledge accumulated during recent decades
on the capacity of wildlife (i.e. its resilience) to cope with (a) habitat fragmentation, alteration and loss; and (b) the arrival of exotic
invasive species. We selected within the two above-mentioned
subject areas four major topics of interest in applied management
for which substantial knowledge has been accumulated in recent
decades and for which evidence is lately accumulating in the form
of counterpoints to widespread and commonly accepted principles
and practices. This procedure echoes the selection of questions of
conservation concern carried out by Sutherland et al. (2006,
2009) for both the conservation of biodiversity in the UK and global
biological diversity preservation. In this regard, reviews are a necessary approach to the synthesis of knowledge obtained using the
ecological tools employed by conservation practitioners (Norris,
2004) and to optimize management actions, especially in an era
characterized by large cuts in funding for conservation agencies
and the uneven distribution of conservation spending vis-à-vis
conservation priorities (Hoekstra et al., 2005; Brooks et al., 2006;
Halpern et al., 2006).
2. Methods
This is necessarily a traditional qualitative review given that our
aim was to provide an overview of four different topics (see
below). Specific topics such as the efficacy of removing opportunistic predators have been already subject to quantitative meta-analysis in the literature (see e.g. Smith et al., 2010a, 2010b).
We used some of the main agents of global change, namely (a)
habitat fragmentation, alteration and loss and (b) the arrival of
invasive exotic species, as major topics to identify questions of
conservation interest for which substantial accumulated knowledge is available.
Considering that a direct literature search using conventional
search procedures and engines for counterpoints rather than rules
in conservation biology was not possible (because exceptions are
not typically registered as such in titles, abstracts and keywords),
we reviewed on a weekly basis over a 3-year period (March
2008–2011) the e-alerts from the main scientific journals in the
fields of ecology, conservation, invasion biology and biogeography.
The 20 journals whose e-alerts were reviewed by both authors
(with a journal overlap of 88%) are indicated in Appendix A. From
the e-alerts of these journals we selected articles embracing either
views defending a position against well-established conservation
theoretical paradigms (without a predetermined set list) under a
framework of global anthropogenic change or applied strategies
to cope with this change in an effective and efficient way. From selected articles, we checked the reference lists and selected additional papers, which included journals other than those sending
e-alerts and years outside the initial 3-year sampling period. Specifically, articles from 30 additional journals were selected (Appendix
A). This combined procedure enabled us to select initially a total of
525 papers and in all cases we read at least the abstracts in search of
some exception to what we considered to be an established rule or
practice in conservation biology; we used the existence of unexpected exceptions or counterarguments to established rules as a
criterion to identify topics that are prone to dogma development
A. Martínez-Abraín, D. Oro / Biological Conservation 159 (2013) 539–547
within the areas in which we have developed most of our research
(i.e. predator–prey interactions, effectiveness and unexpected consequences of management actions). Out of these papers a subset of
129 was selected, which dealt mainly with faunal applied problems,
out of which only 70 provided useful information. Once selected,
the papers were read and information was gathered across the papers and classified under four different major questions, two of
them dealing with habitat fragmentation, alteration and loss and
two with exotic species management: (1) is supplementary feeding
of vertebrates always a good conservation measure?, (2) can generalist predators be a conservation problem and, if so, is the control of
opportunistic predators an effective conservation strategy, (3) are
introduced species always detrimental?, and (4) can invasive species be eradicated without unwanted ecological and economic side
effects?. The devising of the abovementioned questions was done
by allocating the selected literature into several major groups discussing around the same topics. Hence the questions selected were
not decided beforehand but selected as a result of the literature
search and classification.
When a review on one of our study topics was available we discussed and cited the review rather than the individual papers as a
means of reducing the number of references cited. The largest
number of papers dealt with question 3 (n = 24), followed by question 1 (n = 20). Literature on question 2 was more scarce (n = 16),
followed by that on question 4 (n = 10). Ca. 30% of the papers selected were published in just five journals (Appendix A).
3. Results and discussion
3.1. Dealing with habitat fragmentation, alteration and loss
One consequence of habitat alteration is the unwanted increase
in food supplies for some animal species (e.g. creation of dumps).
The other side of the same coin is intervention designed to
compensate for habitat deterioration involving supplementary
food provision, a management action usually regarded as positive.
Question 1a. Pros and cons of supplementary feeding for conservation purposes.
Supplementary feeding may be intentional (with a conservation
objective) or unintentional (e.g. dumps, fishing discards). In all instances, it is known to have profound effects and to enhance all major
demographic parameters, but also to alter other components of
animal ecology (Boutin, 1990; Robb et al., 2008). One of the main
conservation consequences of supplementary feeding is improved
population trends in large scavenger raptors (García-Ripollés and
López-López, 2011), although the ‘restaurants’ built for these species
are also used by corvids and generalist raptors and mammals.
Although historically vulture feeders have been considered as
appropriate conservation measures, critical views of their usefulness
have recently begun to emerge (e.g. Margalida et al., 2010). Vulture
feeding stations encourage the growth of colonies close by and hence
juveniles are less inclined to disperse to new territories (see
López-López et al., 2004). Such lack of dispersal, together with good
feeding conditions, can lead to undesirable situations such as skewed
sex-ratios due to the differential recruitment of immature females
(Blanco et al., 1997), which may lead to the formation of reproductive
trios and an overall reduction in breeding success (Carrete et al.,
2006a,b). Bretagnolle et al. (2004) and Oro et al. (2008) found that
artificial feeding sites were not effective in reversing decline in
vulture populations affected by threats such as poison; rather, they
simply delayed population extinction, although they were suitable
for preventing further immature mortality caused by poisoning.
Vulture feeders have also been shown to promote nest predation
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by non-target facultative scavenger predators of the ground-nesting
species that breed nearby (Cortés-Avizanda et al., 2009). Hence some
evidence suggests that conservation practitioners could encourage a
model based on numerous small feeding stations supplied with
small quantities of food, which would imitate the original conditions
of food unpredictability in space and time with which scavengers
have evolved (Deygout et al., 2009; Cortés-Avizanda et al., 2010;
Margalida et al., 2010; Martínez-Abraín et al., 2011). More
importantly, conservation efforts should be targeted on combating
the anthropogenic causes of adult mortality (e.g. the illegal use of
poison) in these long-lived raptors (Oro et al., 2008).
Dilemmas concerning food supplementation are not only restricted to large avian scavengers as the management of many
other bird groups and mammal species has increasingly begun to
incorporate this practice. As in the case of vultures, unwanted
side-effects have already been identified. Supplemented polygynous birds such as the critically endangered kakapo parrot (Strigops
habroptilus) produce nestlings with skewed sex ratios because females in good body condition (i.e. food-supplemented females)
maximize their fitness by producing more offspring of the most
costly sex to be reared, in this case males (Clout et al., 2002).
Hence, changes are now needed in the conservation programme
to increase the recruitment of females and prevent counterproductive results. Supplementary feeding is used to redistribute moose
(Alces alces) during the final phase of their migrations in their wintering quarters, but is useless if applied during the early migration
period (Sahlsten et al., 2010). Although food supplementation in
the critically endangered Iberian lynx (Lynx pardinus) was useful
as it kept range sizes within their normal range of values by
contracting core areas, dispersal rates (and hence the full extent
of home-ranges) were not reduced and productivity did not increase (Palomares et al., 2011). Recently, Chauvenet et al. (in press)
reported that the supplemental feeding of a cavity-nesting passerine from New Zealand, the hihi Notiomystis cincta, affected positively the survival of adult translocated birds, but they also found
evidence of negative density-dependence on recruitment. Interestingly, supplementary feeding can be used successfully to reduce
predation rates of game birds by raptors when these have become
a conservation problem (Redpath et al., 2001).
Question 1b. The efficiency of controlling generalist predators for
both game and conservation purposes.
One of the unwanted consequences of supplementary feeding
associated with habitat modification is the subsidization of mesopredators resulting in important effects at community level. Habitat modification typically leads to less area available for wildlife
and this in turn translates into the so-called ‘ecological decay’, a
process characterized by a progressive loss of species that starts
with top predators with extensive home ranges. As in the case of
undesirable supplementary feeding, a lack of top predators can
contribute to an overabundance of mesopredators (Palomares
et al., 1995; Gomper and Vanak, 2008) and thus might present
an important challenge for wildlife managers (Conover, 2002).
Until just a few decades ago, many carnivores were the subject
of human persecution worldwide (e.g. Martínez-Abraín et al., 2008,
2009). Biodiversity protection laws and the abandonment of rural
areas in the industrialized world have allowed many predator populations to recover rapidly, although in many other parts of the
planet with subsistence economies persecution is still a concern.
In many instances, predator communities are subsidized by human
alteration of resource availability (this is for example the case of
gull populations in Europe taking advantage of massive discards
from trawling boats and landfills) and artificially inflated predator
densities may have a severe impact on prey populations (see
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Gomper and Vanak, 2008). In these cases, lower abundances of
opportunistic predators are synonymous with a more natural situation. A similar scenario occurs when predator communities experience the so-called ‘mesopredator release’ due to the absence or
scarcity of top predators (Gomper and Vanak, 2008). A particular
case of predator subsidization occurs when the presence of a
non-native prey species leads to increases in native predator densities that, in turn, have an impact on a native prey species; this
well-known phenomenon is known as hyperpredation (see e.g.
Courchamp et al., 2000; Roemer et al., 2001, 2002; Zhang et al.,
2006; Tablado et al., 2010). Ground-nesting birds, many of which
are gamebirds, are one of the prey groups most affected by predation by generalist mesopredators. Empirical results show that predators can reduce the brood size of tetraonid species by 40% and
productivity by 23% (Marcström et al., 1988). Results of simulations suggest that predators can limit prey populations but generally do not drive prey populations to extinction, except in the case
of islands and small isolated populations (MacDonald et al., 1999).
Predation is only a threat when predators take a constant proportion of prey (as happens in the rare cases in which predators follow
a Type-I functional response) rather than adjusting predation rates
to prey abundance, and when predation affects all age classes
(MacDonald et al., 1999). A review by Valkama et al. (2005) concluded that raptor predation may limit gamebird populations and
reduce gamebird harvests, but only under certain conditions such
as having several generalist predators acting together on a
ground-nesting species when alternative prey, such as vole, become scarce. The same authors also point out that most such results come from studies performed in northern Europe (although
in recent years this trend has been decreased noticeably) and that
this precludes extrapolation to more diverse southern ecosystems.
These results have often generated proposals for removing predators with conservation aims in mind (Reynolds and Tapper,
1996), although typically there is little subsequent assessment of
the results of controls (Conover, 2002).
Predators can have unexpected positive effects in spatially
structured prey populations. Although predation at patch level is
recorded initially as a negative perturbation for the prey population or the community, it may have a globally positive effect at
metapopulation level, because predation commonly triggers prey
dispersal, thereby enhancing the colonization of empty patches
or change in the dynamics of source-sink systems (Tavecchia
et al., 2007; Oro et al., 2009; Almaraz and Oro, 2011). Hence, we
should bear in mind that it is not possible to increase population
numbers of a spatially-structured target species evenly (for instance a gamebird species) because patch quality is spatially heterogeneous. It is mostly after perturbations that high-quality
individuals become prone to move from a high to a lower quality
patch, as habitat exploitation in metapopulations typically follows
an ideally despotic distribution (see e.g. Oro, 2008; Almaraz and
Oro, 2011; but see Sebastián-González et al., 2010). Additionally,
terrestrial and marine animal species with poor dispersal capabilities (i.e. amphibians, reptiles, small mammals and corals) and,
especially, plants will experience the effect of changed predation
mechanisms resulting from the alteration and loss of habitat more
strongly than non-sessile marine animals, birds or large mammals
with greater dispersal abilities (Genovart et al., 2007; Alcaide et al.,
2008; Oro et al., 2012).
In their pioneer review about the effectiveness of predator management as a conservation tool, Côté and Sutherland (1997) found
that removing predators had a large positive effect on both hatching success in target bird species and on post-breeding population
sizes, but not on breeding population sizes. Hence, they concluded
that predator removal often fulfils the goal of game management
but is much less consistent in accomplishing the aims of conservation managers. Along these lines Nordström (2003) summarized 38
predator removal experiments and found that nest success of
ground-nesting prey birds increased in 83.9% of the cases, postbreeding numbers increased in 70% of the studies and breeding
numbers increased in 60.9% of the cases. However the review by
Lavers et al. (2010) of more than 800 predator removal programs
concluded that although predator removal increases productivity
on average by ca. 25% modelling predicts that predator removal
alone is insufficient to reverse predicted declining trends in
30–67% of the avian prey species considered. However, the systematic review by Smith et al. (2010a) concluded that removing predators increases hatching and fledging success and strengthens
breeding populations and as such is an effective strategy for the
conservation of vulnerable bird populations. Although the same
authors found that predator exclusion (using either fences or
nest-cages) increased hatching success, it was not clear whether
it resulted in increased breeding populations (Smith et al., 2010b).
Although predator removal can be an effective tool for both
hunting and conservation goals, under certain circumstances, it is
important to remember that, because it fails to get to the root of
problems, it may not be a cost-effective measure. This may not be
a problem within the context of game activities which have an
economic reward, but it is certainly a problem when applied from
a biodiversity conservation perspective in which public money
has no economic returns and hence needs to be used as efficiently
as possible. This is especially the case in spatially structured populations of both predators and prey with heterogeneity in patch quality, in which management actions in individual patches cannot be
assessed without reference to the whole metapopulation (see e.g.
Rushton et al., 2006; Paracuellos and Nevado, 2010). Alternatives
such as the management of food sources or habitat changes at metapopulation level that go straight to the heart of the problem are
more cost-effective because they get long-lasting and quick results
(see e.g. Fernández-Olalla et al., 2012; Martínez-Abraín et al., 2011).
3.2. Dealing with exotic species
Although exotic species have been traded and translocated for
centuries, the present enormous mobility of human beings and
their produce at global level has made exotic species one of the
main problems for biodiversity conservation in recent decades.
However, a dogmatic picture could be emerging on the role of
exotics in recipient ecosystems since doubts exist, under some particular circumstances, regarding both the negative effects of exotic
species (question 2a) and the feasibility of eradicating invasive
species without having unwanted ecological side-effects (question
2b). Some exotic species have been socially tagged as ‘bad’ (for
example, rats; interestingly, we often forget that some archipelagos have endemic rat species) and others as ‘good’ (species such
as the prickly-cactuses of the genus Opuntia in the Mediterranean)
despite strict scientific evidence not supporting such an anthropocentric distinction (see e.g. Slobodkin, 1988; Ruffino et al., 2009).
Question 2a. The ubiquity of the detrimental effect of invasive
species.
There is no doubt that exotic invasive species can have devastating effects on ecosystem structure and functioning through
complex cascading effects and can also have high economic costs
(Pimentel et al., 2000; Roemer et al., 2002). For example, Towns
et al. (2006) reviewed critically the impact of introduced rats on
islands and noted that Pacific rats (Rattus exulans), Norway rats
(Rattus norvegicus) and ship rats (Rattus rattus) have been found
to suppress certain forest plants and are associated with declines
of flightless invertebrates, ground-dwelling reptiles, land birds,
burrowing seabirds and small mammals, including native rodents.
These results are accepted by Traveset et al. (2009) for the Balearic
A. Martínez-Abraín, D. Oro / Biological Conservation 159 (2013) 539–547
and Canary Islands, who add the disruption of native plant–seed
dispersal mutualisms to the list of concerns (Traveset and Richardson, 2006). However, Ruffino et al. (2009) suggest that, despite the
long-standing introduction of the ship rat on most islands, the
survival of long-lived endemic Mediterranean seabirds is a conservation paradox. Actually the presence of rats is only a limiting factor for the storm-petrel (Hydrobates pelagicus), the smallest
Mediterranean petrel, whereas three shearwater species were
found to be little affected by and to have coexisted with invasive
rodents. Most seabirds have managed to survive on Mediterranean
islands for 2000 years after the introduction of ship rats (Drake and
Hunt, 2009; Igual et al., 2007). Broadly similar conclusions have
been reported by Martin et al. (2000) and in the global meta-analysis performed by Jones et al. (2008), whereby Laridae and other
large ground-nesting seabirds were not found to be vulnerable to
rats to the extent that Hydrobatidae and other small ground-nesting seabirds are. The disruption of mutualisms by invasive species
altering ecosystem functional diversity is clearly recorded in the
literature (Davis et al., 2009); nevertheless, to date it has not been
proven whether or not exotic pollinators can increase the density
of pollinated plants so that there are enough plants to forage on
and to be pollinated by both native and exotic pollinators. In such
a situation, the monopolization of native plants would only be a
conservation problem in a closed or limited system in which plant
numbers remain constant in the presence of both native and exotic
pollinators. Greenhouse experiments in this sense are necessary.
Likewise, we tend to overlook the fact that the interaction between
exotics and natives is most likely characterized by non-linear
dynamics in which resistance and resilience are driven by unknown thresholds (Suding and Hobbs, 2009; Andersen et al., 2008).
Interestingly, invasive species can have facilitative effects on
native tropical tree species, including endemic species. This is the
case of Cinchona species, for which species richness was found to
be 20% higher in invaded plots that had an almost 50% greater proportion of endemic species compared to controls (Fischer et al.,
2009). Introduced species can also act as functional equivalents
(Zamora, 2000) of native species locally driven to extinction by
human action as, for example, introduced birds in Hawaii, which
have been found to help disperse the seeds of common understory
native plants that, in turn, may facilitate the perpetuation of the
native forest (Foster and Robinson, 2007). A similar case occurs
on the Bonin Islands of Japan where introduced birds compensate
for extinct native dispersers (Kawakami et al., 2009). In the Balearic
Islands the alien pine marten is the main disperser of the native
shrub Cneorum tricoccon in substitution of the endemic lizard
(Podarcis lilfordi), that performed this role in the past, before being
driven to extinction on Mallorca Island by introduced weasels
(Mustela nivalis) (see Traveset and Richardson, 2011 and references
therein). Introduced rabbits perform relevant ecosystem services
for nationally rare UK species by maintaining short sward heights
in heathland and grassland ecosystems and also serve as prey for
populations of predators (Lees and Bell, 2008). Introduced prey
species such as exotic crayfish can increase native predator
numbers, although this may have negative consequences for native
prey due to hyperpredation (Roemer et al., 2002; Tablado et al.,
2010). Invaders may confer benefits on native competitors by
perturbing the natural host–parasite interaction by means of a
dilution effect (Kopp and Jokela, 2007).
The presence of exotic species can also have evolutionary consequences. As described by Vellend et al. (2007) and reviewed by
Genovart (2009), exotic species may promote evolutionary diversification via increased genetic differentiation among populations of
both exotic and native species and the creation of new hybrid lineages. This can be viewed as negative in the short term (e.g. loss of
local adaptation and genetic diversity in animals) but also can
543
create new evolutionary avenues in the long run (e.g. hybridization
is one common mechanism of rapid speciation among plant
species which could be positive in species-poor sites, although detrimental in hot spots of plant diversity). The translocation of
domestic goats to the island of Fuerteventura (Canary Islands) by
the first human settlers ca. 2500 years ago encouraged the arrival
and subsequent genetic differentiation of Egyptian vultures
(Neophron percnopterus) (Agudo et al., 2010), which have become
3% larger and 16% heavier than those in Iberia in less than 200 generations. However, negative evolutionary effects are also possible
because hybridization can lead to net losses in biodiversity due
to introgression (McDonald et al., 2008). A conclusion regarding
the net effects (both at ecological and evolutionary scales) of exotic
invasive species hence will require a consideration of both diversification and the loss of biodiversity and consequent alterations to
ecosystem functioning it can cause. Finally, invasive species can
become cultural keystone species (Nuñez and Simberloff, 2005):
for example, New World cactuses introduced into Europe (e.g.
the invasive Opuntia) have important cultural values because they
have been used for food, cattle shelters, the fixation of slopes and
to rear an insect from which a purple dye is derived; furthermore,
many medical applications for this plant have recently been
discovered, including anti-oxidant, hypoglycaemic, analgesic,
anti-inflammatory and anti-carcinogenic properties, which could
generate important economic benefits (see e.g. Ibañez-Camacho
et al., 1983). However, this social tagging of exotic species is highly
context dependent. Prickly-cactuses, for example, are not seen as
useful species in many parts of the world where they have an invasive behavior, with detrimental impacts on local people relying on
land for survival.
Invasive species can also be used as unintentional experiments
across large spatial and temporal scales as a means of better understanding the natural world (Sax et al., 2007). Each individual case
of invasion needs to be carefully analyzed to determine the overall
balance between their positive and negative effects on biodiversity
(see Gozlan, 2008 and Gozlan et al., 2010 for an assessment of nonnative freshwater fish introductions) because many different types
of complex ecological, economic, social and evolutionary interactions are possible. Probably the best way to prevent unwanted
ecological and economic costs is to apply a risk analysis at the ecosystem level to potential invasive species, as suggested by Andreu
and Vilà (2010).
Question 2b. The feasibility of eradication of invasive species.
In many cases, removing exotic species or maintaining them at
low densities seem to be viable strategies (Simberloff, 2009).
However, it is advisable to bear in mind the fact that the removal
of invasive species may have unwanted or/and unexpected cascading side-effects (Zavaleta et al., 2001), ecologically equivalent
to mesopredator release when native top predators are locally removed (Gomper and Vanak, 2008). For example, Rayner et al.
(2007) showed that the eradication of cats (Felis catus) from an
oceanic island led to a severe decrease in the breeding success
of Cook’s petrel (Pterodroma cookii) due to a demographic explosion of Pacific rats (R. exulans), which preyed on petrel chicks and
eggs. However, despite the depression of productivity by rats, it is
to be expected that this long-lived bird will do better without
cats because survival, the vital rate with the proportionally greatest influence on population growth rate in long-lived species, was
not affected by rats. A similar case was analyzed by Bergstrom
et al. (2009), whereby a management intervention to eradicate
cats on Macquarie Island, precipitated a rapid landscape-wide
change because rabbit (Oryctolagus cuniculus) numbers increased
substantially, despite the control effect of the Myxoma virus that
544
A. Martínez-Abraín, D. Oro / Biological Conservation 159 (2013) 539–547
was present. Owing to these unexpected results, the cost of further conservation action on this site will exceed AU$24 million.
Unexpected effects can also arise due to competition after the removal of invasive species. Brodier et al. (2011) analyzed the longterm effects of the eradication of introduced rabbits on a small island of the Kerguelen archipelago and found that blue petrels
(Halobaena caerulea) benefited from the cessation of burrow disturbance by rabbits. Their density increased eightfold during the
6 years following eradication. This burrowing petrel’s predator,
the brown skua (Catharacta skua), was not affected negatively
by rabbit removal and indeed benefited from the increase in its
preferred prey. However, there was a parallel fourfold reduction
in the density of the Antarctic prion (Pachyptila desolata), probably due to a competitive exclusion process from nesting areas
by blue petrels. Competitor release can also affect mice populations if rats are removed (Caut et al., 2007) and cases of mice negatively affecting albatross and petrel productivity have been
reported (Wanless et al., 2007). Competition between introduced
rabbits and native birds may take place indirectly (i.e. apparent
competition) if a native or introduced predator is subsidized by
rabbit presence (Carlsson et al., 2009) and eventually hyperpredation may take place on the native prey species mediated by the
exotic prey (Zhang et al., 2006). Dietary shifts can also occur if
invasive species are controlled by depriving them of their main
food sources. Caut et al. (2008) warn of this risk in the case of
black rats on islands: rats may compensate by preying more
heavily upon the sea turtle Chelonia mydas, an endangered species, in the absence of seabirds. However, these dietary shifts
may be an unavoidable short-term consequence of removing food
subsidies (which is a correct management strategy attacking the
roots of the problem) until a new dynamic equilibrium is established with a lower carrying capacity (see e.g. Votier et al.,
2004). Hence, the answer to question 2b is that it is essential to
characterize on a case-by-case basis the life history of invasive
species and their trophic relationships with the invaded community as a means of obtaining a holistic perspective of the situation
that will enable us to adapt the proposed control program accordingly (Zavaleta et al., 2001; Buhle et al., 2005; Caut et al., 2009).
Management interventions must explicitly consider and plan for
possible indirect effects or otherwise may have to face unwanted
ecological effects and potentially elevated economic costs (Bergstrom et al., 2009). The fact that a growing literature is pointing
out the mistakes done in the past in this field of removal of exotics, and suggesting alternative approaches, is a positive sign
against the perpetuation of dogmatic ideas in this area but transfer of knowledge from conservation science to wildlife managers
should be improved so that this becomes a reality.
4. Conclusions
We can extract from this review a set of five good management
principles to prevent the creation of dogmatic approaches in some
conservation topics:
2. The introduction of food supplements of human origin, mismatching in the human-derived recovery of top-predators
versus mesopredators in most animal communities, and
the introduction of exotic prey, can affect local predator–
prey dynamics and lead to hyperpredation and the consequent extinction of prey locally. Thus, under these particular
circumstances generalist mesopredators can cause conservation problems.
3. Control of generalist predators is usually an effective strategy for solving game conflicts in which solutions are
needed in the short-term and private investments usually
have economic returns. However, this type of control cannot be considered to be a cost-efficient conservation
approach because the situation reverts quickly to its original state as soon as culling is stopped. Hence, public money,
without economic return, is simply wasted. More efficient
conservation solutions include the management of habitat
to decrease predation rates rather than predators per se,
and the removal of food subsidies, including exotic prey.
This may be costly initially but there is a clear end to this
type of expenditure and unexpected results (costly to counteract) are less likely.
4. Exotic invasive species usually have very detrimental
effects on community structure and functioning but under
some particular local circumstances can have positive synecological effects, especially in human-impoverished communities (such as in oceanic islands) where these species
can sometimes act as functional equivalents of lost pieces
of the community puzzle. Hence, when analyzing the
effects of invasive species in a recipient community the
net result between diversity gains and loses must be considered on an individual basis that also takes into account
local human cultural considerations.
5. Removing invasive exotic species is a desirable conservation
goal but in some circumstances (for instance, when the invasion lasts for a long time) removal can have complex
unwanted cascading side-effects via predation, competition,
habitat changes and dietary behavioral shifts. To avoid creating these unwanted effects managers need to characterize
the inter-specific relationships between the invasive species
and the invaded community with great care and to approach
control from a holistic perspective.
Otherwise, results may be contrary to expected and large private or public funding may become necessary to reverse unexpected ecosystem-wide effects.
From a more general perspective, the best strategy to prevent
dogma generation in conservation biology is to replicate experiments in space and time and have results, both positive and negative,
published in outlets which are easy to be consulted by all sorts of
conservation practitioners. Available information is optimally synthesized by means of systematic review and quantitative meta-analysis whose results must reach a wide conservation audience.
Acknowledgements
1. Supplementary feeding has spurred population recovery
and increase in many opportunistic animal species worldwide and hence is often perceived as a recommendable
management practice. However, it can also cause certain
unexpected demographic problems with unwanted conservation consequences. The optimal strategy – to be carried
out before any such action is implemented – is to replicate
as much as possible the original situation of food unpredictability in space and time that many animal species have
evolved with, and to study existing trophic relationships
within the community.
This study has been funded by the Spanish Ministry of Science
(Grant Ref. CGL2009-08298) and the Regional Government of Balearic Islands (FEDER funding). We also thank three anonymous
reviewers and Andrew Pullin for helping us to improve the manuscript. A.M.A. was funded by a Parga-Pondal postdoctoral contract
from Xunta de Galicia.
Appendix A
See Table A1.
A. Martínez-Abraín, D. Oro / Biological Conservation 159 (2013) 539–547
Table A1
List of journals whose e-alerts were inspected during the period March 2008–2011 in
search of papers with counter-intuitive findings regarding conservation biology (left),
and list of journals from which additional papers were added to this review as they
had been cited by the initial papers selected (right).
Journals for which e-alerts were
inspected
Additional journals added secondarily
Journal of Animal Ecology
Journal of Applied Ecology
Biology Letters
Nature
Science
Biological Conservation
Conservation Biology
Conservation Letters
Behavioral Ecology
Oikos
Journal of Biogeography
Ecography
Proceedings of the National
Academy of Sciences
Ecology Letters
Oryx
Animal Conservation
Mammalian reviews
PLoS One
Journal of Zoology
Ibis
Journal of Raptor Research
Ecological Modelling
Ecological Applications
Global Change Biology
Endangered Species Research
Evolutionary Ecology Research
Mathematical Biosciences
Austral Ecology
BioScience
Biological Invasions
Frontiers in Ecology and the
Environment
Trends in Ecology and Evolution
Proceedings of the Royal Society
of London Series B
BMC Evolutionary Biology
The American Naturalist
Annual Reviews of Ecology and
Systematics
Urban Ecosystems
Ecology and Society
Ardeola
International Journal of
Biometeorology
Biological reviews
Ecology
Restoration Ecology
Journal of Ornithology
Plant Ecology
Wildlife Biology
International Journal of Primatology
Journal of Fish Biology
Fish and Fisheries
Canadian Journal of Zoology
Appendix B
See Table A2.
Table A2
List of journals with at least six articles selected. In bold the three journals with the
highest percentage of articles selected.
Journal name
No. papers
%
Biological Conservation
Conservation Biology
Journal of Applied Ecology
Biological Invasions
Trends in Ecology and Evolution
14
9
8
7
6
10.8
6.9
6.2
5.4
4.6
References
Agudo, R., Rico, C., Vilà, C., Hiraldo, F., Donázar, J.A., 2010. The role of humans in the
diversification of a threatened island raptor. BMC Evol. Biol. 10, 384.
Alcaide, M., Serrano, D., Negro, J.J., Tella, J.L., Laaksonen, T., Muller, C., Gal, A.,
Korpimaki, E., 2008. Population fragmentation leads to isolation by distance but
not genetic impoverishment in the philopatric Lesser Kestrel: a comparison
with the widespread and sympatric Eurasian Kestrel. Heredity 102, 190–198.
Almaraz, P., Oro, D., 2011. Size-mediated non-trophic interactions and stochastic
predation drive assembly and dynamics in a seabird community. Ecology 92,
1948–1958.
Andersen, T., Carstensen, J., Hernández-García, E., Duarte, C.M., 2008. Ecological
thresholds and regime shifts: approaches to identification. Trends Ecol. Evol. 24,
49–57.
Andreu, J., Vilà, M., 2010. Risk analysis of potential invasive plants in Spain. J. Nat.
Conserv. 18, 34–44.
545
Bergstrom, D.M., Lucieer, A., Kiefer, K., Wasley, J., Belbin, L., Pedrsen, T.K., Chown,
S.L., 2009. Indirect effects of invasive specie removal devastate World Heritage
Island. J. Appl. Ecol. 46, 73–81.
Blanco, G., Martínez, F., Traverso, J.M., 1997. Pair bond and age distribution of
breeding Griffon vultures (Gyps fulvus) in relation to reproductive status and
geographic area in Spain. Ibis 139, 180–183.
Boutin, S., 1990. Food supplementation experiments with terrestrial vertebrates:
patterns, problems, and future. Can. J. Zool. 68, 203–220.
Bretagnolle, V., Inchausti, P., Seguin, J.-F., Thibault, J.-C., 2004. Evaluation of the
extinction risk and of conservation alternatives for a very small insular
population: the bearded vulture Gypaetus barbatus in Corsica. Biol. Conserv.
120, 19–30.
Brodier, S., Pisanu, B., Villers, A., Pettex, E., Lioret, M., Chapuis, J.-L., Bretagnolle, V.,
2011. Responses of seabirds to the rabbit eradication on Ile Verte, sub-Antarctic
Kerguelen archipelago. Anim. Conserv. 14, 459–465.
Brooks, T.M., Mittermeier, R.A., da Fonseca, G.A.B., Gerlach, J., Hoffman, M.,
Lamoreux, J.F., Mittermeier, C.G., Pilgrim, J.D., Rodrigues, A.S.L., 2006. Global
biodiversity conservation priorities. Science 313, 58–61.
Buhle, E.R., Margolis, M., Ruesink, J.L., 2005. Bang for buck: cost-effective control of
invasive species with different life histories. Ecol. Econ. 52, 355–366.
Carlsson, N.O.L., Sarnelle, O., Strayer, D.L., 2009. Native predators and exotic prey:
an acquired taste? Front. Ecol. Evol. 7, 525–532.
Carrete, M., Donázar, J.A., Margalida, A., 2006a. Density-dependent productivity
depression in Pyrenean bearded-vultures: implications for conservation. Ecol.
Appl. 16, 1674–1682.
Carrete, M., Donázar, J.A., Margalida, A., Bertran, J., 2006b. Linking ecology,
behaviour and conservation: does habitat saturation change the mating
system of bearded vultures. Biol. Lett. 2, 624–627.
Carroll, C., 2007. Interacting effects of climate change, landscape conversion, and
harvest on carnivore populations at the range margin: Marten and Lynx in the
northern Appalachians. Conserv. Biol. 21, 1092–1104.
Caut, S., Casanovas, J.G., Virgos, E., Lozano, J., Witmer, G.W., Courchamp, F., 2007.
Rats dying for mice: modelling the competitor release effect. Austral Ecol. 32,
858–868.
Caut, S., Angulo, E., Courchamp, F., 2008. Dietary shift of an invasive predator: rats,
seabirds and sea turtles. J. Appl. Ecol. 45, 428–437.
Caut, S., Angulo, E., Courchamp, F., 2009. Avoiding surprise on Surprise Island: alien
species control in a multitrophic level perspective. Biol. Invas. 11, 1689–1703.
Cawardine, J., Wilson, K.A., Watts, M., Etter, A., Klein, C.J., Possingham, H.P., 2008.
Avoiding costly conservation mistakes: the importance of defining actions and
costs in spatial priority setting. PLoS One 3, e2586.
Chauvenet, A.L.M., Ewen, J.G., Armstrong, D.P., Coulson, T., Blackburn, T.M., Adams,
L., Walker, L.K., Pettorelli, N., 2012. Does supplemental feeding affect the
viability of translocated populations? The example of the hihi. Anim. Conserv.
15, 337–350.
Clout, M.N., Elliott, G.P., Robertson, B.C., 2002. Effects of supplementary feeding on
the offspring sex ratio of kakapo: a dilemma for the conservation of a
polygynous parrot. Biol. Conserv. 107, 13–18.
Conant, S., 1988. Saving endangered species by translocation. Bioscience 38, 254–257.
Conover, J., 2002. Resolving Human–Wildlife Conflicts: The Science of Wildlife
Damage Management. CRC Press, Boca Raton, FL, USA.
Cortés-Avizanda, A., Carrete, M., Serrano, D., Donázar, J.A., 2009. Carcasses increase
the probability of predation of ground-nesting birds: a caveat regarding the
conservation value of vulture restaurants. Anim. Conserv. 12, 85–88.
Cortés-Avizanda, A., Carrete, M., Donázar, J.A., 2010. Managing supplementary
feeding for avian scavengers: guidelines for optimal design using ecological
criteria. Biol. Conserv. 143, 1707–1715.
Côté, I., Sutherland, W.J., 1997. The effectiveness of removing predators to protect
bird populations. Conserv. Biol. 11, 395–405.
Courchamp, F., Lanlais, M., Sugihara, G., 2000. Rabbits killing birds: modelling the
hyperpredation process. J. Anim. Ecol. 69, 154–164.
Davis, N.E., O’Dowd, D.J., Mac Nally, R., Green, P.T., 2009. Invasive ants disrupt
frugivory by endemic island birds. Biol. Lett. 6, 85–88.
Deygout, C., Gault, A., Sarrazin, F., Bessa-Gomes, C., 2009. Modelling the impact of
feeding stations on vulture scavenging service efficiency. Ecol. Model. 220,
1826–1835.
Drake, D.R., Hunt, T.L., 2009. Invasive rodents on islands: integrating historical and
contemporary ecology. Biol. Invasions 11, 1483–1487.
Farley, J., 2010. Conservation through the economics lens. Environ. Manage. 45, 26–38.
Fernández-Olalla, M., Martínez-Abraín, A., Canut, J., García-Ferre, Afonso, I.,
González, L.M., 2012. Assessing different Management scenarios to reverse
the declining trend of a relict capercaillie population: a modelling approach
within an adaptive Framework. Biol. Conserv. 148, 79–87.
Fischer, L.K., von der Lippe, M., Kowarik, I., 2009. Tree invasion in managed tropical
forests facilitates endemic species. J. Biogeogr. 36, 2251–2263.
Floerl, O., Coutts, A., 2009. Potential ramifications of the global economic crisis on
human-mediated dispersal of marine non-indigenous species. Mar. Pollut. Bull.
58, 1595–1598.
Foster, J.T., Robinson, S.K., 2007. Introduced birds and the fate of Hawaiian
rainforests. Conserv. Biol. 21, 1248–1257.
García-Ripollés, C., López-López, P., 2011. Integrating effects of supplementary
feeding, poisoning, pollutant ingestion and wind farms of two vulture species in
Spain using a population viability analysis. J. Ornithol. 152, 879–888.
Genovart, M., 2009. Natural hybridization and conservation. Biodivers. Conserv. 18,
1435–1439.
546
A. Martínez-Abraín, D. Oro / Biological Conservation 159 (2013) 539–547
Genovart, M., Oro, D., Juste, J., Bertorelle, G., 2007. What genetics tell us about the
conservation of the critically endangered Balearic Shearwater? Biol. Conserv.
137, 283–293.
Gomper, M.E., Vanak, T., 2008. Sudsidized predators, landscapes of fear and
disarticulated carnivore communities. Anim. Conserv. 11, 13–14.
Gozlan, R.E., 2008. Introduction of non-native freshwater fish: is it all bad? Fish Fish.
9, 106–115.
Gozlan, R.E., Britton, J.R., Cowx, I., Copp, G.H., 2010. Current knowledge on nonnative freshwater fish introductions. J. Fish Biol. 76, 751–786.
Halpern, B.S., Pyke, C.R., Fox, H.E., Haney, J.C., Schlaepfer, M.A., Zaradic, P., 2006.
Gaps and mismatches between global conservation priorities and spending.
Conserv. Biol. 20, 56–64.
Heller, N.E., Zavaleta, E.S., 2009. Biodiversity management in the face of
climate change: a review of 22 years of recommendations. Biol. Conserv. 142,
14–32.
Herrera, C.M., 1995. Plant–vertebrate seed dispersal systems in the Mediterranean:
ecological, evolutionary and historical determinants. Annu. Rev. Ecol. Syst. 265,
705–727.
Hoegh-Guldberg, O., Hughes, L., McIntyre, S., Lindenmayer, D.B., Parmesan, C.,
Possingham, H.P., Thomas, C.D., 2008. Assisted colonization and rapid climate
change. Science 321, 345–346.
Hoekstra, J.M., Boucher, T.M., Ricketts, T.H., Roberts, C., 2005. Confronting a biome
crisis: global disparities of habitat loss and protection. Ecol. Lett. 8, 23–29.
Ibañez-Camacho, R., Meckes-Lozoya, M., Mellado-Campos, V., 1983. The
hypoglucemic effect of Opuntia streptacantha studied in different animal
models. J. Ethnopharmacol. 7, 175–181.
Igual, J.M., Forero, M.G., Gomez, T., Oro, D., 2007. Can an introduced predator trigger
an evolutionary trap in a colonial seabird. Biol. Conserv. 137, 189–196.
Jones, H.P., Tershy, B.R., Zavaleta, E.S., Croll, D.A., Keitt, B.S., Finkelstein, M.E.,
Howald, G.R., 2008. Severity of the effects of invasive rats on seabirds: a global
review. Conserv. Biol. 22, 16–26.
Kareiva, P., Marvier, M., 2003. Conserving biodiversity coldspots. Am. Sci. 91, 344–
351.
Kawakami, K., Mizusawa, L., Higuchi, H., 2009. Reestablished mutualism in a seeddispersal system consisting of native and introduced birds and plants on the
Bonin Islands, Japan. Ecol. Res. 24, 741–748.
Kopp, K., Jokela, J., 2007. Resistant invaders can convey benefits to native species.
Oikos 116, 295–301.
Lavers, J.L., Wilcox, C., Donlan, C.J., 2010. Bird demographic responses to predator
removal programs. Biol. Invasions 12, 2839–3859.
Lees, A.C., Bell, D.J., 2008. A conservation paradox for the 21st century: the European
wild rabbit Oryctolagus cuniculus, an invasive alien and an endangered species.
Mamm. Rev. 38, 304–320.
Linquist, S., 2008. But is it progress? On the alleged advances of conservation
biology over ecology. Biol. Philos. 23, 529–544.
López-López, P., García-Ripollés, C., Verdejo, J., 2004. Population status and
reproductive performance of Eurasian griffons (Gyps fulvus) in Eastern Spain.
J. Raptor Res. 38, 350–356.
Lynas, P., Newton, S.F., Robinson, J.A., 2007. The status of birds in Ireland: an
analysis of conservation concern 2008–2013. Irish Birds 8, 149–167.
MA (Millennium Ecosystem Assessment), 2003. Ecosystems and Human Wellbeing: A Framework for Assessment. Island Press, Washington, DC.
MacDonald, D.W., Mace, G.M., Barretto, G.R., 1999. The effects of predators on
fragmented prey populations: a case study for the conservation of endangered
prey. J. Zool. Soc. Lond. 247, 487–506.
Mace, G., Balmford, A., Ginsberg, J.R., 1998. Conservation in a Changing World.
Cambridge University Press, Cambridge.
Marcström, V., Kenward, R.E., Engren, E., 1988. The impact of predation on boreal
tetraonids during vole cycles: an experimental study. J. Anim. Ecol. 57, 859–
872.
Margalida, A., Donázar, J.A., Carrete, M., Sánchez-Zapata, J.A., 2010. Sanitary versus
environmental policies: fitting together two pieces of the puzzle of European
vulture conservation. J. Appl. Conserv. 47, 931–935.
Martin, J.-L., Thibault, J.-D., Bretagnolle, V., 2000. Black rats, island characteristics,
and colonial nesting birds in the Mediterranean: consequences of an ancient
introduction. Conserv. Biol. 14, 1452–1466.
Martínez-Abraín, A., Oro, D., 2010. Applied conservation services of the evolutionary
theory. Evol. Ecol. 24, 1381–1392.
Martínez-Abraín, A., Sarzo, B., Villuendas, E., Bartolomé, M.A., Oro, D., 2004.
Unforseen effects of ecosystem restoration on yellow-legged gulls in a small
western Mediterranean island. Environ. Conserv. 31, 219–224.
Martínez-Abraín, A., Crespo, J., Jiménez, J., Pullin, A., Stewart, G., Oro, D., 2008.
Friend or foe: societal shifts from intense persecution to active conservation of
top predators. Ardeola 55, 111–119.
Martínez-Abraín, A., Crespo, J., Jiménez, J., Gómez, J.A., Oro, D., 2009. Is the
historical war against wildlife over in southern Europe? Anim. Conserv. 12,
204–208.
Martínez-Abraín, A., Regan, H.M., Viedma, C., Villuendas, E., Bartolomé, M.A.,
Gómez, J.A., Oro, D., 2011. Cost-effectiveness of translocation options for a
threatened waterbird. Conserv. Biol. 25, 726–735.
Martín-López, B., Montes, C., Ramírez, L., Benayas, J., 2009. What drives policy
decision-making related to species conservation? Biol. Conserv. 142, 1370–
1380.
McDonald, D.B., Parchman, T.L., Bower, M.R., Hubert, W.A., Rahel, F.J., 2008. An
introduced and a native vertebrate hybridize to forma a genetic bridge to a
second native species. Proc. Natl. Acad. Sci. USA 105, 10837–10842.
Munilla, I., Díez, C., Velando, A., 2007. Are edge bird populations doomed to
extinction? A retrospective analysis of the common guillemot collapse in Iberia.
Biol. Conserv. 137, 359–371.
Nordström, M., 2003. Introduced predator in the Baltic Sea: variable effects of feral
mink removal on bird and small mammal populations in the outer archipelago.
Ann. Univ. Turkuensis AI I, 158.
Norris, K., 2004. Managing threatened species: the ecological toolbox, evolutionary
theory and declining-population paradigm. J. Appl. Ecol. 41, 413–426.
Nuñez, M.A., Simberloff, D., 2005. Invasive species and the cultural keystone species
concept. Ecol. Soc. 10, r4.
Oro, D., 2008. Living in a ghetto within a local population: an empirical example of
an ideal despotic distribution. Ecology 89, 838–846.
Oro, D., Martínez-Abraín, A., 2006. Deconstructing myths on large gulls and their
impact on threatened sympatric waterbirds. Anim. Conserv. 10, 117–126.
Oro, D., Margalida, A., Carrete, M., Heredia, R., Donázar, J.A., 2008. Testing the
goodness of supplementary feeding to enhance population viability in an
endangered vulture. PLoS One, e4084.
Oro, D., Pérez-Rodríguez, A., Martínez-Vilalta, A., Bertolero, A., Vidal, F., Genovart, X.,
2009. Interference competition in a threatened seabird community: a paradox
for a successful conservation. Biol. Conserv. 142, 1830–1835.
Oro, D., Jimenez, J., Curcó, A., 2012. Some clouds have a silver lining: paradoxes of
anthropogenic perturbations from study cases on long-lived social birds. PLoS
One, e42753.
Palomares, F., Gaona, P., Ferreras, P., Delibes, M., 1995. Positive effects on game
species of top predators by controlling smaller predator populations: an
example with Lynx, mongooses, and rabbits. Conserv. Biol. 9, 295–305.
Palomares, F., Rodríguez, A., Revilla, E., López-Bao, J.V., Calzada, J., 2011. Assessment
of the conservation efforts to prevent extinction of the Iberian Lynx. Conserv.
Biol. 25, 4–8.
Paracuellos, M., Nevado, J.C., 2010. Culling yellow-legged gulls Larus michahellis
benefits Audouin’s gulls Larus audouinii at a small and remote colony. Bird
Study 57, 26–30.
Pimentel, D., Lach, L., Zuniga, R., Morrison, Doug, 2000. Environmental and
economic costs of nonindigenous species in the United States. Bioscience 50,
53–65.
Possingham, H.P., Andelman, S.J., Burgman, M.A., Medellín, R.A., Master, L.L., Keith,
D.A., 2002. Limits to the use of threatened species list. Trends Ecol. Evol. 17,
503–507.
Rayner, M.J., Hauber, M.E., Imber, M.J., Stamp, R.K., Clout, M.N., 2007. Spatial
heterogeneity of mesopredator release within an oceanic island system. Proc.
Natl. Acad. Sci. USA 104, 20862–20865.
Redpath, S.M., Thirgood, S.J., Leckie, F.M., 2001. Does supplementary feeding reduce
predation of red grouse by hen harriers? J. Appl. Ecol. 38, 1157–1168.
Regan, H.M., Ben-Haim, Y., Langford, B., Wilson, W.G., Lundberg, P., Andelman, S.J.,
Burgman, M.A., 2005. Robust decision-making under severe uncertainty for
conservation management. Ecol. Appl. 15, 1471–1477.
Reynolds, J.C., Tapper, S.C., 1996. Control of mammalian predators in game
management and conservation. Mamm. Rev. 26, 127–156.
Ricciardi, A., Simberloff, D., 2008. Assisted colonization is not a viable conservation
strategy. Trends Ecol. Evol. 24, 248–253.
Robb, G.N., McDonald, R.A., Chamberlain, D.E., Bearhop, S., 2008. Food for thought:
supplementary feeding as a driver of ecological change in avian populations.
Front. Ecol. Environ. 6, 476–485.
Roemer, G.W., Coonan, T.J., Garcelon, D.K., Bascompte, J., Laughrin, L., 2001. Feral
pigs facilitate hyperpredation by golden eagles and indirectly cause the decline
of the island fox. Anim. Conserv. 4, 307–318.
Roemer, G.W., Donlan, C.J., Courchamp, F., 2002. Golden eagles, feral pigs, and
insular carnivores: how exotic species turn native predators into prey. Proc.
Natl. Acad. Sci. USA 99, 791–796.
Ruffino, L., Bourgeois, K., Vidal, E., Duhem, C., Paracuellos, M., Escribano, F., Sposimo,
P., Bacetti, N., Pascal, M., Oro, D., 2009. Invasive rats and seabirds after
2000 years of an unwanted coexistence on Mediterranean islands. Biol.
Invasions 11, 1631–1650.
Rushton, S.P., Shirley, M.D.F., Macdonald, D.W., Reynolds, J.C., 2006. Effects of
culling fox populations at the landscape scale: a spatially explicit population
modelling approach. J. Wildlife Manage. 70, 1102–1110.
Sahlsten, J., Bunnefeld, N., Mansson, J., Ericsson, G., Bergstrom, R., Dettki, H., 2010.
Can supplementary feeding be used to redistribute moose Alces alces? Wildlife
Biol. 16, 85–92.
Sax, D.F., Stachowicz, J.J., Brown, J.H., Bruno, J.F., Dawson, M.N., Gaines, S.D.,
Grosberg, R.K., Hastings, A., Holt, R.D., Mayfield, M.M., O’Connor, M.I., Rice, W.R.,
2007. Ecological and evolutionary insights from species invasions. Trends Ecol.
Evol. 22, 465–471.
Sebastián-González, E., Botella, F., Sempere, R., Sánchez-Zapata, J.A., 2010. An
empirical demonstration of the ideal free distribution: little Grebes
(Tachybaptus ruficollis) breeding in intensive agricultural landscapes. Ibis 152,
643–650.
Seddon, P.J., 2010. From reintroduction to assisted colonization: moving along the
conservation translocation spectrum. Restor. Ecol. 18, 796–802.
Seddon, P.J., Armstrong, D.P., Soorae, P., Launay, F., Walker, S., Ruiz-Miranda, C.R.,
Molur, S., Kodewey, H., Kleiman, D.G., 2009. The risks of assisted colonization.
Conserv. Biol. 23, 788–789.
Simberloff, D., 1988. The contribution of population and community biology to
conservation science. Annu. Rev. Ecol. Syst. 19, 473–511.
Simberloff, D., 2009. We can eliminate invasions or live with them. Successful
management projects. Biol. Invasions 11, 149–157.
A. Martínez-Abraín, D. Oro / Biological Conservation 159 (2013) 539–547
Slobodkin, L.B., 1988. Intellectual problems of applied ecology. Bioscience 38, 337–
342.
Smith, R.K., Pullin, A.S., Stewart, G.B., Sutherland, W.J., 2010a. Effectiveness of
predator removal for enhancing bird populations. Conserv. Biol. 24, 820–829.
Smith, R.K., Pullin, A.S., Stewart, G.B., Sutherland, W.J., 2010b. Is nest predator
exclusion an effective strategy for enhancing bird populations? Biol. Conserv.
144, 1–10.
Soulé, M.E., 1985. What is conservation biology? Bioscience 35, 727–734.
Speth, J.G., 2011. American passage: towards a new economy and a new politics.
Ecol. Econ. http://dx.doi.org/10.1016/j.ecolecon.2011.01.018.
Suding, K.N., Hobbs, R.J., 2009. Threshold models in restoration and conservation: a
developing framework. Trends Ecol. Evol. 24, 271–279.
Sutherland, W.J., Pullin, A.S., Dolan, P.M., Knight, T.M., 2004. The need for evidencebased conservation. Trends Ecol. Evol. 19, 305–308.
Sutherland, W.J., Armstrong-Brown, S., Armsworth, P.R., Tom, B., Brickland, J.,
Campbell, C.D., Chamberlain, D.E., Cooke, A.I., Dulvy, N.K., Dusic, N.R., Fitton, M.,
Freckleton, R.P., Godfray, H.C.J., Grout, N., Harvey, H.J., Hedley, C., Hopkins, J.J.,
Kift, N.B., Kirby, J., Kunin, W.E., Macdonald, D.W., Marker, B., Naura, M., Neale,
A.R., Oliver, T., Osborn, D., Pullin, A.S., Shardlow, M.E.A., Showler, D.A., Smith,
P.J., Smithers, R.J., Solandt, J.-L., Spencer, J., Spray, C.J., Thomas, C.D., Thompson,
J., Webb, S.A., Yalden, D.W., Watkinson, A.R., 2006. The identification of 100
ecological questions of high policy relevance in the UK. J. Appl. Ecol. 43, 617–
627.
Sutherland, W.J., Adams, W.M., Aronson, R.B., Aveling, R., Blackburn, T.M., Broad, S.,
Ceballos, G., Côté, I.M., Cowling, R.M., Da Fonseca, G.A.B., Dinerstein, E., Ferraro,
P.J., Fleishman, E., Gascon, C., Hunter Jr., M., Hutton, J., Kareiva, P., Kuria, A.,
Macdonald, D.W., Mackinnon, K., Madgwick, F.J., Mascia, M.B., Mcneely, J.,
Milner-Gulland, E.J., Moon, S., Morley, C.J., Nelson, S., Osborn, D., Pai, M.,
Parsons, E.C.M., Peck, L.S., Possingham, H., Prior, S.V., Pullin, A.S., Rands, M.R.W.,
Ranganathan, J., Redford, K.H., Rodriguez, J.P., Seymour, F., Sobel, J., Sodhi, N.S.,
Stott, A., Vance-Borland, K.And., Watkinson, A.R., 2009. One hundred questions
of importance to the conservation of global biological diversity. Conserv. Biol.
23, 557–567.
Tablado, Z., Tella, J.L., Sánchez-Zapata, J.A., Hiraldo, F., 2010. The paradox of the
long-term positive effects of a North American crayfish on a European
community of predators. Conserv. Biol. 24, 1230–1238.
547
Tavecchia, G., Pradel, R., Genovart, M., Oro, D., 2007. Density-dependent parameters
and demographic equilibrium in open populations. Oikos 116, 1481–1492.
Towns, D.R., Atkinson, I.A.E., Daugherty, C.H., 2006. Have the harmful effects of
introduced rats on islands been exaggerated? Biol. Invasions 8, 863–891.
Traveset, A., Richardson, D.M., 2006. Biological invasions as disruptors of plant
reproductive mutualisms. Trends Ecol. Evol. 21, 208–216.
Traveset, A., Richardson, D.M., 2011. Mutualisms: key drivers of invasions, key
casualties of invasions. In: Richardson, D.M. (Ed.), Fifty years of Invasion
Ecology: The Legacy of Charles Elton, first ed. Blackwell Publishing Ltd., pp.
143–160.
Traveset, A., Nogales, M., Alcover, J.A., Delgado, J.D., López Darias, M., Godoy, D.,
Igual, J.M., Bover, P., 2009. A review on the effects of alien rodents in the Balearic
(Western Mediterranean Sea) and Canary Islands (Eastern Atlantic Ocean). Biol.
Invasions 11, 1653–1670.
Valkama, J., Korpimaki, E., Arroyo, B., Beja, P., Bretagnolle, V., Bro, E., Kenward, R.,
Mañosa, S., Redpath, S.M., Thirgood, S., Viñuela, J., 2005. Birds of prey as limiting
factors of gamebird populations in Europe: a review. Biol. Rev. 80, 171–203.
Van der Wal, R., Truscott, A.-M., Pearce, I.S.K., Cole, L., Harris, M.P., Wanless, S., 2008.
Multiple anthropogenic changes cause biodiversity loss through plant invasion.
Global Change Biol. 14, 1428–1436.
Vellend, M., Harmon, L.J., Lockwood, J.L., Mayfield, M.M., Hughes, A.R., Wares, J.P.,
Sax, D.F., 2007. Effects of exotic species on evolutionary diversification. Trends
Ecol. Evol. 22, 481–488.
Votier, S.C., Furness, R.W., Bearhop, S., Crane, J.E., Caldow, R.W.G., Catry, P., Ensor, K.,
Hamer, K.C., Hudson, A.V., Kalmbach, E., Klomp, N.I., Pfeifer, S., Philips, R.A.,
Prieto, I., Thompson, D.R., 2004. Changes in fisheries discard rates and seabird
communities. Nature 427, 727–730.
Wanless, R.M., Angel, A., Cuthbert, R.J., Hilton, G.M., Ryan, P.G., 2007. Can predation
by invasive mice drive seabird extinctions? Biol. Lett. 3, 241–244.
Zamora, R., 2000. Functional equivalence in plant–animal interactions: ecological
and evolutionary consequences. Oikos 88, 442–447.
Zavaleta, E.S., Hobbs, R.J., Mooney, H.A., 2001. Viewing invasive species removal in a
whole-ecosystem context. Trends Ecol. Evol. 16, 454–459.
Zhang, J., Fan, M., Kuang, Y., 2006. Rabbits killing birds revisited. Math. Biosci. 203,
100–123.