Content uploaded by Germán Garrote
Author content
All content in this area was uploaded by Germán Garrote on Oct 13, 2019
Content may be subject to copyright.
347
Animal Biodiversity and Conservation 42.2 (2019)
© 2019 Museu de Ciències Naturals de Barcelona
Papers are published under a
Creative Commons Attribution 4.0 International License
ISSN: 1578–665 X
eISSN: 2014–928 X
Garrote, G., Pérez de Ayala, R., 2019. Spatial segregation between Iberian lynx and other carnivores. Animal
Biodiversity and Conservation, 42.2: 347–354, Doi: https://doi.org/10.32800/abc.2019.42.0347
Abstract
Spatial segregation between Iberian lynx and other carnivores. The Iberian lynx (Lynx pardinus) is a specialist
predator. Rabbits represent the bulk of its diet as for many other Iberian predators. This study addresses how
the presence of the Iberian lynx affects the spatial distribution of the mesocarnivore community at landscape
scale in the Sierra de Andújar. We studied mesocarnivore presence by sampling at 230 camera trapping
stations, located in areas with and without lynx. We used a x2–test to compare the proportion of stations in
which each species of carnivore were recorded in the zones with and without lynx. The proportion of camera
trapping stations in which red fox (Vulpes vulpes), Egyptian mongoose (Herpestes ichneumon), beech marten
(Martes foina), wildcat (Felis sylvestris) and common genet (Genetta genetta) were detected was signicantly
lower in the area where lynx were present than in the area where it was absent. No signicant differences
between the two types of areas were found for badgers (Meles meles). Our results highlight the role of the
lynx as apex predators and the benets that the recovery of Iberian lynx populations would entail in terms of
trophic interactions and restored disrupted ecosystems processes.
Key words: Intraguild competition, Carnivores, Phototrapping, Apex predator
Resumen
Segregación espacial entre el lince ibérico y otros carnívoros. El lince ibérico (Lynx pardinus) es un depreda-
dor especialista. El conejo constituye el grueso de su dieta, al igual que la de otros depredadores ibéricos.
Este estudio analiza cómo la presencia del lince ibérico afecta a la distribución espacial de la comunidad de
mesocarnívoros a escala de paisaje en la sierra de Andújar. Se estudió la presencia de mesocarnívoros me-
diante 230 cámaras de fototrampeo, instaladas en zonas con y sin presencia de lince. Se utilizó la prueba de
la x2 para comparar la proporción de cámaras en las que se detectó cada una de las especies de carnívoros
en las zonas con y sin lince. La proporción de cámaras que detectaron zorros (Vulpes vulpes), meloncillos
(Herpestes ichneumon), garduñas (Martes foina), gatos monteses (Felis sylvestris) y ginetas (Genetta genetta)
fue signicativamente menor en las zonas con presencia de lince que en las zonas donde este estaba ausente.
No se encontraron diferencias signicativas en cuanto a la presencia de tejones (Meles meles) entre ambos
tipos de zona. Nuestros resultados ponen de relieve la importancia del lince como depredador apical y los
benecios que podría reportar la recuperación de las poblaciones de lince ibérico en lo que concierne a las
interacciones trócas y el restablecimiento de los procesos ecosistémicos interrumpidos.
Palabras clave: Competencia intragremial, Carnívoros, Fototrampeo, Depredador apical
Received: 08 XI 18; Conditional acceptance: 05 II 19; Final acceptance: 16 V 19
Germán Garrote, Instituto de Biología de la Conservación (IBiCo), c/ Nebli 13, 28232, Madrid, España (Spain).–
R. Pérez de Ayala, WWF/España, Gran Vía de San Francisco 8–D, 28005 Madrid, España (Spain).
Corresponding author: G. Garrote. E–mail: gergarrote@gmail.com
Spatial segregation between
Iberian lynx and other carnivores
G. Garrote, R. Pérez de Ayala
348 Garrote and Pérez de Ayala
Introduction
Direct interactions between predators and other species
can have indirect consequences further down the food
web via trophic cascades (Ripple et al., 2016). Large
carnivores play a key role in terrestrial ecosystems
when they exert an inuence on herbivores and so
indirectly prevent overgrazing (McShea, 2005). They
can also inuence carnivore communities via intraguild
interactions (Ritchie and Johnson, 2009) and indirectly
prevent excessive predation on prey species by meso-
carnivores (Elmhagen et al., 2010). This top–down
cascade can inuence ecosystem structures and
biodiversity at both local and larger scales (Terborgh,
2001; Elmhagen et al., 2010). If healthy populations
of top predators are to be maintained within ecosys-
tems, these ecosystems should also contain healthy
communities and populations of the many species that
perform ecosystem services at lower trophic levels
(Dobson et al., 2006; Haswell et al., 2017). However,
the functional roles of top predators cannot be fully
appreciated in isolation from bottom–up processes
because the effects of nutrients, productivity (Pace et
al., 1999) and anthropogenic habitat may bring about
change (Litvaitis and Villafuerte, 1996; Estes, 1998;
Elmhagen and Rushton, 2007).
Competitive intraguild interactions have been propo-
sed as highly important organizing mechanisms since,
due to similarities in ecological niches, they limit the
number of species that can be packed into an assem-
blage (Jaksic and Marone, 2007). Similar ecological
preferences increase the risk of competition, whereas
mechanisms such as resource partitioning, temporal
or spatial avoidance strategies (Voigt and Earle, 1983;
Johnson and Franklin, 1994; Kozlowski et al., 2008),
or alternative foraging strategies (Husseman et al.,
2003) facilitate coexistence. Interference interactions,
harassment and injury caused by larger carnivores pose
a risk to smaller mesopredators (Linnell and Strand,
2000; Haswell et al., 2018). Furthermore, as a result
of interference competition, subordinate species are
frequently restricted to suboptimal habitats (Tannerfeldt
et al., 2002; Macdonald et al., 2004; Mitchell and Banks,
2005), which can have important implications for the
demography and distribution of the species involved
(Thompson, 1988; Holt and Polis, 1997; Atwood and
Gese, 2008).
The Iberian lynx (Lynx pardinus) is the top pre-
dator of the terrestrial vertebrate community in the
Mediterranean ecosystem (Valverde, 1963). Listed as
Endangered by the IUCN (Rodríguez and Calzada,
2015), the species reached its all–time minimum in the
rst years of the twenty–rst century, when only 100
individuals in just two isolated populations –Andújar–
Cardeña and Doñana– were known to exist (Guzmán
et al., 2004; Simón et al., 2012). Since then, however,
the Iberian lynx has undergone a signicant increase
in population size and range due to the measures
implemented as part of conservation projects for
the species (Simón et al., 2012), which include the
creation of new populations through reintroduction.
The Iberian lynx is a specialist predator. Rabbits
represent the bulk of its diet in a similar manner to
that of many other Iberian predators (Cabezas–Díaz
et al., 2011), possibly leading to interference or
food competition. Previous studies of the relation-
ships between Iberian lynx and other carnivores
performed in Doñana have found that the Egyp-
tian mongoose (Herpestes ichneumon) and genet
(Genetta genetta) avoid lynx, while the Eurasian
badger (Meles meles) is apparently indifferent to
its presence. Although foxes (Vulpes vulpes) and
lynx exhibit temporal segregation in their use of
habitat (Fedriani et al., 1999), their spatial rela-
tionship remains unclear (Palomares et al., 1996).
The relationship between wildcat (Felix sylvestris)
and lynx has not been studied.
This study addresses how the presence of the
Iberian lynx affects the spatial distribution of the
mesocarnivore community at a landscape scale in the
Sierra de Andújar. We studied the spatial distribution
of several species of mesocarnivores in areas where
the lynx is absent and where it is present, taking into
account the abundance of rabbits.
Material and methods
Study area
The study area lies in the eastern Sierra Morena (SE
Spain; g. 1) and consists of a mountainous area
with an altitudinal range of 200–1,500 m covered by
well–preserved Mediterranean forests (Quercus ilex,
Q. faginea and Q. suber) and scrublands (Quercus
coccifera, Pistacia lentiscus, Arbutus unedo, Phillyrea
angustifolia and Myrtus communis). The area is ma-
naged for big–game hunting and has high densities
of red deer (Cervus elaphus) and wild boar (Sus
scrofa). It is partially protected by the Parque Natu-
ral Sierra de Andújar. During the study period, the
Andújar–Cardeña Iberian lynx population consisted
of 60–110 individuals, distributed over an area of
15,000 ha (Guzmán et al., 2004).
Camera trapping survey
The spatial distribution of the carnivore community was
estimated by sequential camera trapping surveys per-
formed in December 1999–February 2000, November
2000–February 2001 and November 2001–February
2002. We used camera trapping data from the annual
national Iberian lynx survey (Guzmán et al., 2004),
which covers 85 % of the area potentially used by the
Iberian lynx.
We divided the study area into 12 survey blocks,
each of which were surveyed by camera trapping for
periods of two months. Once one block was nis-
hed, cameras were moved to the next survey block.
We surveyed an almost continuous surface area of
7,800 ha using a total of 230 camera trapping stations
(1999/2000: n = 28; 2000/2001: n = 168; 2001/2002:
n = 39). In all, 115 out of 230 stations were located
in areas in which the lynx are present, as dened by
Guzman et al. (2004), and the other 115 stations were
placed in areas without lynx (g. 1).
Animal Biodiversity and Conservation 42.2 (2019) 349
Fig. 1. Study area map. Camera trap stations located in areas with and without lynx, and stations in
which each species of carnivore was recorded.
Fig. 1. Mapa de la zona de estudio donde se representa la ubicación de las estaciones de fototrampeo en
zonas con y sin lince, así como las estaciones donde se detectó cada una de las especies de carnívoros.
Camera trap
2002 Iberian lynx
distribution area
2 0 2 4 k m
Doñana
Felis sylvestris Meles meles
Vulpes vulpes Martes foina
Genetta genetta Herpestes ichneumon
Andújar–Cardeña
Spain
350 Garrote and Pérez de Ayala
We used 212 35–mm Canon Prima© classic photo
lm cameras with data registers and automatic ashes.
The cameras were modied to allow activation via an
external 25 × 25 cm pressure plate, positioned at a
distance of 170 cm that was triggered when stepped
on by an animal (Garrote et al., 2011). The cameras
were placed in a small wooden box on pillars 30 cm
above ground level. Urine from captive Iberian lynx,
placed on an inert adjacent support, 50 cm above
ground level and the pressure plate, was used as a
lure. Lynx urine has been reported to be an excellent
attractant for all carnivore species (Garrote et al., 2011;
Monterroso et al., 2016). This attractant was replaced
every 3–6 days. The distance between camera traps
was 400–800 m. Camera–trap locations were located
along suspected lynx travel routes (Garrote et al., 2012)
such as roads or paths, chosen to maximize capture
probabilities (Karanth and Nichols, 1998). Each camera
was continuously active throughout the entire survey
period for each block (two months).
To describe the species distribution in the area, we
calculated occupancy as the proportion of stations at
which a species was detected in relation to the total
number of stations (Sogbohossou et al., 2018).
Rabbit abundance and habitat variables
Rabbit abundances were estimated for each survey
block by on–foot constant–speed itineraries lasting
three hours. Rabbit latrines were counted every 15',
and these counts were taken as the survey unit for
the statistical analysis. Indirect surveys were carried
out at the same time of the year (end of spring,
when rabbit populations peak) under similar weather
conditions. Every 15' we estimated, in a 25 m radius
plot, the percentage of land surface covered by the
following habitat categories: trees, scrubland lower
than 50 cm in height, scrubland higher than 50 cm
in height, pastureland and rocks. The percentage of
covered land was divided into four categories scored
as follows: 1 (0–25 %), 2 (> 25–50 %), 3 (> 50–75 %)
and 4 (> 75).
Statistical analysis
We compared the mean values for rabbit abundance
and for each habitat category obtained in the areas
with and without lynx using a Mann–Whitney U–test.
We used a x2–test to compare the proportion of
stations in the zones with and without lynx in which
each species of mesocarnivore was present. The
carnivores with lower capture rates were grouped
together to perform statistical analysis (minimum ve
expected records).
Results
The following carnivores were detected in this study:
(Lynx pardinus, 9–15.9 kg), Eurasian badger (Meles
meles), red fox (Vulpes vulpes), Egyptian mongoo-
se (Herpestes ichneumon), beech marten (Martes
foina), wildcat (Felis sylvestris), and common genet
(Genetta genetta). The proportion of camera trapping
stations in which the fox and wildcat were detected
was signicantly lower in the area with lynx than in
the area without lynx (table 1; g. 1); no signicant
differences were found for the presence of the bad-
ger between both areas. Genet, beech marten and
Egyptian mongoose were grouped together to perform
the statistical analysis. The presence of this group of
mesocarnivores was found to be signicantly lower
in the areas where lynx were present.
No signicant difference was found between zones
with and without lynx for the habitat variables (ta-
ble 2). As expected, rabbit abundance in areas with
lynx was signicantly higher than that in lynx–free
areas since lynx distribution is dependent on rabbit
abundance (table 2).
Discussion
With the exception of the badger, the presence of the
Iberian lynx determines the distribution at the lands-
cape scale of the mesocarnivores community in the
study areas. No signicant habitat differences were
found between areas with and without lynx, while the
highest rabbit abundances were detected in areas with
lynx. As mentioned above, Iberian mesocarnivores
preferably select rabbits as prey (Cabezas–Díaz et
al., 2011). The most probable explanation for the ob-
served distribution of mesocarnivores at a landscape
scale is the interference competition between species
in which the lynx is the dominant species.
This is the rst study to address a relationship
between the Iberian lynx and wildcat, the only two
sympatric wild felids present in the Iberian peninsula.
Competition becomes greater as eco–morphological
similarities or phylogenetic proximity between compet-
ing species increase (Cruz et al., 2018), and generally
the larger dominant species exclude smaller or sub-
ordinate species from their territories by interference
competition. Therefore, as expected, the larger Iberian
lynx exerts strong interference competition on the
smaller wildcat. This leads to fewer wildcats in those
areas where lynx are present. Similar relationships
of dominance have been described for other species
of felines, such as the ocelot (Leopardus pardalis),
which acts as a dominant carnivore over other smaller
sympatric cats such as margay (Leopardus wiedii) and
jaguarundi (Puma yagouaroundi) and so inuences
their ecological parameters (de Oliveira et al., 2010;
Cruz et al., 2018).
Previous studies have shown a high overlap in the
diets, activity levels, habitat use and home range in
radio–tracked foxes and lynx (Fedriani et al., 1999).
Although it has been suggested that foxes mitigate
lynx predation by modifying their spatial behaviour
at home range level, no spatial segregation in these
species has ever been found. Using a landscape
approach, the present study demonstrates signicant
spatial segregation between foxes and lynx. These
differences with previous work might be attributable
to scale since certain studies have concluded that
approaches at different scales can generate different
Animal Biodiversity and Conservation 42.2 (2019) 351
conclusions regarding interspecic interactions bet-
ween species (e.g. (Tannerfeldt et al., 2002) for the
Arctic red fox (Cruz et al., 2018). Previous studies
(Palomares et al., 1996; Fedriani et al., 1999) have
covered smaller areas than our study, which was
performed at a much greater landscape scale. On the
other hand, the relative densities of the mesocarni-
vores and their prey may also inuence interactions
(Creel, 2001; Berger and Gese, 2007). However,
although no information is available for fox densities
to compare these two study areas, the density of Ma-
tasgordas rabbit population (8 rabbits/ha; Villafuerte
et al., 1997) is greater than that of Andújar (Simón
et al., 2012). In areas or during periods of lower prey
abundance, competition may play a more important
role and interspecic interactions may change, re-
sulting in increased interference competition (Creel,
2001). Lower prey densities can result in lower lynx
tolerance toward foxes and, consequently, greater
interference competition. Similar conclusions were
reached by (Gese et al., 1996) in Yellowstone National
Park, where coyotes tolerate red foxes during high
prey years but not at other times.
Although data regarding the presence of the smaller
mesocarnivores (Mongoose, martens and genets) are
scarce, our results concur with previously reports from
Doñana, where mongoose and genets avoid areas
where lynx are present.
Iberian lynx and badgers seem to be particularly
well predisposed to coexist (Palomares et al., 1996;
Fedriani et al., 1999), and our results suggest that
there is a complete spatial overlap between the
species. Kleiman and Eisenberg (1973) suggest that
this coexistence occurs as a result of a separation in
their ecological niches, which is likely a consequen-
ce of evolution of different social systems. Similar
interactions have been described between Eurasian
lynx and wolves in Białowieza Forest (Schmidt, 2008)
and between lynx and wolverine in northern Sweden
(Schmidt, 2008). The Iberian lynx is a crepuscular
species that preys mainly on rabbits (Fedriani et al.,
1999), whereas badgers are much more nocturnal
and are generalists with the capacity to survive on a
Table 1. Total number of camera stations, positive stations for each species in zones with/without
lynx, and positive stations per species. Genet, beech marten and Egyptian mongoose are grouped in
'others'. x2 results are shown.
Tabla 1. Número total de estaciones de fototrampeo, número de estaciones positivas para cada especie en
las zonas con y sin lince y estaciones totales positivas para cada especie. Las ginetas, las garduñas y los
meloncillos están agrupados en la categoría "others" (otras). Se muestran los resultados de las pruebas de la x2.
Total Badger Fox Wildcat Others
With lynx 115 20 10 6 2
Without lynx 115 26 53 29 17
Total 230 43 63 35 19
p 0.5 < 0.0001 0.0038 0.016
Table 2. Mann–Whitney U–test results for the
variables of habitat and rabbit abundance.
Tabla 2. Resultados de las pruebas U de
Mann–Whitney para las variables del hábitat y
la abundancia de conejos.
Z p–level
Pasture –0.64 0.52
Scrub < 50cm 0 1
Scrub > 50 cm 0.96 0.33
Tree –0.48 0.63
Rocks 1.28 0.2
Rabbit 2.08 0.03
greater diversity of resources (Roper, 1994; Neal and
Cheeseman, 1996; Revilla and Palomares, 2002).
The food available for badgers in Mediterranean ha-
bitats varies greatly and badgers respond by shifting
their diets accordingly between prey items (Virgós et
al., 2004). However, niche differences alone cannot
completely explain this coexistence. Foxes are even
more adaptable than badgers and could potentially
develop resource partitioning, temporal avoidance
strategies (Voigt and Earle, 1983; Johnson and
Franklin, 1994; Kozlowski et al., 2008), or different
foraging strategies (Husseman et al., 2003) to facili-
tate coexistence. However, fox distribution is clearly
inuenced by the presence of lynx while badger
distribution is not. The outcome of direct encounters
between lynx and badgers is unknown but probably
involves a risk of injury for both species. Therefore,
the observed sympatry between Iberian lynx and
badger is probably facilitated by a combination of
both factors –the avoidance of injury and different
foraging strategies.
352 Garrote and Pérez de Ayala
As a result of being a trophic specialist on rabbits,
the abundance of its staple prey determines the lynx’s
basic demographic parameters (Monterroso et al.,
2016) and distribution (Guzmán et al., 2004), which
thus implies that there is bottom–up control over Iberian
lynx dynamics. Likewise, the presence or absence of
the Iberian lynx, which is determined by rabbit abun-
dance, affects the dynamics of subordinate carnivore
species via a top–down control effect. The foraging
theory suggests that animals adjust their behaviour
accordingly to optimize foraging efciency and overall
tness, and trade–off harvesting rates with tness costs
(Haswell et al., 2018). In the absence of Iberian lynx,
sympatric mesocarnivores should ideally be distribu-
ted on the basis of habitat quality and preferred food
availability (Van Der Meer and Ens, 1997; Roemer et
al., 2009). The presence of the lynx forces smaller
species to invest in antipredator behavioural strate-
gies (Lima, 1998; Haswell et al., 2017) that can have
negative consequences. For example, their access to
high–quality foraging areas can be restricted (Ritchie
and Johnson, 2009), which forces them to seek an
alternative diet, adopt their life cycles to those of their
new prey items, and adjust their feeding behaviour
(Durant, 2000; Hayward and Slotow, 2009; Wikenros
et al., 2014). This in turn can affect the size of the
home range, increase travel costs or lead to shifts in
habitat use (Caro and Stoner, 2003). The tness costs
of these antipredator responses could affect survival
and reproduction, thereby ultimately having an impact
on population dynamics (Creel and Christianson,
2008). On the other hand, a fall in lynx numbers is
expected following rabbit declines, which will lead to a
lessening of the top–down control on mesocarnivores
numbers (Estes et al., 2011; Monterroso et al., 2016).
Conservation implications
Numerous studies have drawn attention to the impor-
tance of apex predators in suppressing populations
of smaller predators (mesopredators) and thus their
roles in moderating the impact of predation on sma-
ller prey species (Crooks and Soulé, 1999; Johnson
et al., 2007; Berger et al., 2008). The recovery and
re–establishment of apex predator populations con-
tribute not only to their conservation but also benet
biodiversity conservation via a relaxing of the impact
of mesopredators on their prey (Ritchie and Johnson,
2009). This is positive for the restoration of disrupted
ecosystem processes (Estes et al., 2011; Ritchie et
al., 2012), particularly in terms of trophic interactions
(Monterroso et al., 2016) but also for economic and
social reasons (ecosystem services). Some areas in
rural Spain have high rabbit densities and suitable
habitat for the lynx. Most such areas are occupied
by private, intensively managed, small–game hun-
ting areas (rabbit and partridge; Delibes–Mateos et
al., 2009). In these hunting estates strong predator
control is traditional and still persists nowadays, both
legally (leg–hold traps and snares when authorised
under certain exceptional circumstances) and illegally
(Villafuerte et al., 2000; Virgós and Travaini, 2005).
Despite the possible negative effect on non–target
species, this practice requires important time and
monetary expenditure, although the desired results
are not always achieved (Harding et al., 2001). Lynx
are viewed negatively by many hunters in the Iberian
Peninsula since, as a trophic specialist that preys on
rabbits, it competes for this highly important small–
game species. Nevertheless, the Iberian lynx presen-
ce could be an effective, natural and inexpensive tool
for predator control since it suppresses populations
of smaller predators and thereby mitigates the impact
that these mesopredators will have on game species
(Palomares et al., 1995). This is a key argument for
changing game managers’ opinions and for ensuring a
favourable response to any lynx reintroduction project
in its past range from where, ironically, it was eradi-
cated by indiscriminate predator control (Gil–Sánchez
and McCain, 2011).
Acknowledgements
This study was supported by DGCONA–MIMAM
project 'Censo–Diagnóstico de las poblaciones de
Lince Ibérico en España', and by IBiCO/WWF Spain/
Fundación Barcelona Zoo project 'Competencia inte-
respecíca y coexistencia entre el lince ibérico (Lynx
pardinus) y otros carnívoros'. We wish to express our
gratitude to Nicolas Guzmán, Paco García, Aquilino
Duque and Concha Iglesias who carried out eldwork
with us. We also thank the Organismo Autónomo de
Parques Nacionales (Lugar nuevo), Parque Natural
de la Sierra de Andújar, TRAGSA, Fundación CBD–
Habitat, WWF/España, EGMASA, CMA Junta de
Andalucía. We thank Jose Luis Tellería and Guillermo
López for their constructive comments.
References
Atwood, T. C., Gese, E. M., 2008. Coyotes and re-
colonizing wolves: social rank mediates risk–con-
ditional behaviour at ungulate carcasses. Animal
Behaviour, 75: 753–762.
Berger, K. M., Gese, E. M., 2007. Does interference
competition with wolves limit the distribution and
abundance of coyotes? Journal of Animal Ecology,
76: 1075–1085.
Berger, K. M., Gese, E. M., Berger, J., 2008. Iindirect
effects and traditional trophic cascades: a test in-
volving wolves, coyotes, and pronghorn. Ecology,
89: 818–828.
Cabezas–Díaz, S., Virgós, E., Mangas, J. G., Lozano,
Jorge, J. G., 2011. The presence of a "competitor pit
effect" compromises wild rabbit (Orcytolagus cunic-
ulus) conservation. Animal Biology, 61: 319–334.
Caro, T. M., Stoner, C. J., 2003. The potential for
interspecic competition among African carnivores.
Biological Conservation, 110: 67–75.
Creel, S., 2001. Four factors modifying the effect
of competition on carnivore population dynamics
as illustrated by African wild dogs. Conservation
Biology, 15: 271–274.
Creel, S., Christianson, D., 2008. Relationships be-
Animal Biodiversity and Conservation 42.2 (2019) 353
effect of attractant lures in camera trapping: a
case study of population estimates for the Iberian
lynx (Lynx pardinus). European Journal of Wildlife
Research, 58: 881.
Gese, E. M., Ruff, R. L., Crabtree, R. L., 1996.
Foraging ecology of coyotes (Canis latrans ): the
inuence of extrinsic factors and a dominance hie-
rarchy. Canadian Journal of Zoology, 74: 769–783.
Gil–Sánchez, J. M., McCain, E. B., 2011. Former
range and decline of the Iberian lynx (Lynx pardi-
nus) reconstructed using veried records. Journal
of Mammalogy, 92: 1081–1090.
Guzmán, J. N., García, F. J., Garrote, G., Pérez de
Ayala, R., Iglesias, C., 2004. El lince ibérico (Lynx
pardinus) en España y Portugal. Censo–diagnósti-
co de sus poblaciones. DGCN, Ministerio de Medio
Ambiente, Madrid.
Harding, E. K., Doak, D. F., Albertson, J. D., 2001.
Evaluating the effectiveness of predator control: the
non–native red fox as a case study. Conservation
Biology, 15: 1114–1122.
Haswell, P. M., Jones, K. A., Kusak, J., Hayward,
M. W., 2018. Fear, foraging and olfaction: how
mesopredators avoid costly interactions with apex
predators. Oecologia, 187: 573–583.
Haswell, P. M., Kusak, J., Hayward, M. W., 2017.
Large carnivore impacts are context–dependent.
Food Webs, 12: 3–13.
Hayward, M. W., Slotow, R., 2009. Temporal parti-
tioning of activity in large african carnivores: tests
of multiple hypotheses. South African Journal of
Wildlife Research, 39: 109–125.
Holt, R. D., Polis, G. A., 1997. A theoretical framework
for intraguild predation. The American Naturalist,
149: 745–764.
Husseman, J. S., Murray, D. L., Power, G., Mack,
C., Wenger, C. R., Quigley, H., 2003. Assessing
differential prey selection patterns between two
sympatric large carnivores. Oikos, 101: 591–601.
Jaksic, F., Marone, L., 2007. Ecología de comu-
nidades, segunda edición ampliada. Ediciones
Universidad Católica de Chile. Santiago.
Johnson, C. N., Isaac, J .L., Fisher, D. O., 2007.
Rarity of a top predator triggers continent–wide
collapse of mammal prey: dingoes and marsupials
in Australia. Proceedings of the Royal Society B:
Biological Sciences, 274: 341–346.
Johnson, W. E., Franklin, W. L., 1994. Spatial re-
source partitioning by sympatric grey fox (Dusicyon
griseus) and culpeo fox (Dusicyon culpaeus) in
southern Chile. Canadian Journal of Zoology, 72:
1788–1793.
Karanth, K. U., Nichols, J. D., 1998. Estimation of tiger
densities in India using photographic captures and
recaptures. Ecology, 79: 2852–2862.
Kleiman, D. G., Eisenberg, J. F., 1973. Comparisons
of canid and felid social systems from an evolution-
ary perspective. Animal behaviour, 21: 637–659.
Kozlowski, A. J., Gese, E. M., Arjo, W. M., 2008.
Niche overlap and resource partitioning between
sympatric kit foxes and coyotes in the great basin
desert of western Utah. The American Midland
Naturalist, 160: 191–208.
tween direct predation and risk effects. Trends in
Ecology & Evolution, 23: 194–201.
Crooks, K. R., Soulé, M. E., 1999. Mesopredator
release and avifaunal extinctions in a fragmented
system. Nature, 400: 563–566.
Cruz, P., Iezzi, M. E., De Angelo, C., Varela, D., Di
Bitetti, M. S., Paviolo, A., 2018. Effects of human
impacts on habitat use, activity patterns and ecolog-
ical relationships among medium and small felids
of the Atlantic Forest. Plos One, 13: e0200806.
de Oliveira, T. G., Tortato, M. A., Silveira, L., Kasper,
C. B., Mazim, F. D., Lucherini, M., Jácomo, A.
T., Soares, J. B. G., Marques, R. V., Sunquist,
M., 2010. Ocelot ecology and its effect on the
small–felid guild in the lowland neotropics. In:
Biology and Conservation of Eild Felids, chapter
27: 559–580 (D. Macdonald, A. Loveridge, Eds.).
Oxford University Press, Oxford.
Delibes–Mateos, M., Farfán, M. Á., Olivero, J.,
Márquez, A. L., Vargas, J. M., 2009. Long–term
changes in game species over a long period of
transformation in the Iberian Mediterranean land-
scape. Environmental Management, 43: 1256–1268.
Dobson, A., Lodge, D., Alder, J., Cumming, G. S.,
Keymer, J., McGlade, J., Mooney, H., Rusak, J. A.,
Sala, O., Wolters, V., 2006. Habitat loss, trophic
collapse, and the decline of ecosystem services.
Ecology, 87: 1915–1924.
Durant, S. M., 2000. Living with the enemy: avoidance
of hyenas and lions by cheetahs in the Serengeti.
Behavioral Ecology, 11: 624–632.
Elmhagen, B., Ludwig, G., Rushton, S. P., Helle, P.,
Lindén, H., 2010. Top predators, mesopredators
and their prey: interference ecosystems along bio-
climatic productivity gradients. Journal of Animal
Ecology, 79(4): 785–794, doi: 10.1111/j.1365–
2656.2010.01678.x
Elmhagen, B., Rushton, S. P., 2007. Trophic control of
mesopredators in terrestrial ecosystems: top–down
or bottom–up? Ecology Letters, 10: 197–206.
Estes, J. A., 1998. Killer whale predation on sea
otters linking oceanic and nearshore ecosystems.
Science, 282: 473–476.
Estes, J. A., Terborgh, J., Brashares, J. S., Power, M. E.,
Berger, J., Bond, W. J., Carpenter, S. R., Essington,
T. E., Holt, R. D., Jackson, J. B. C., Marquis, R. J.,
Oksanen, L., Oksanen, T., Paine, R. T., Pikitch, E. K.,
Ripple, W. J., Sandin, S. A., Scheffer, M., Schoener,
T. W., Shurin, J. B., Sinclair, A. R. E., Soulé, M. E.,
Virtanen, R., Wardle, D. A., 2011. Trophic downgrad-
ing of planet earth. Science, 333: 301–306.
Fedriani, J. M., Palomares, F., Delibes, M., 1999.
Niche relations among three sympatric Mediterra-
nean carnivores. Oecologia, 121: 138–148.
Garrote, G., De Ayala, R. P., Pereira, P., Robles, F.,
Guzman, N., García, F. J., Iglesias, M. C., Hervás,
J., Fajardo, I., Simón, M., 2011. Estimation of the
Iberian lynx (Lynx pardinus) population in the
Doñana area, SW Spain, using capture–recapture
analysis of camera–trapping data. European Jour-
nal of Wildlife Research, 57: 355–362.
Garrote, G., Gil–Sánchez, J. M., McCain, E. B. de
Lillo S., Tellería J. L., Simon M. A., 2012. The
354 Garrote and Pérez de Ayala
Lima, S. L., 1998. Nonlethal effects in the ecology of
predator–prey interactions. BioScience, 48: 25–34.
Linnell, J. D. C., Strand, O., 2000. Interference inter-
actions, co–existence and conservation of mam-
malian carnivores. Diversity and Distributions, 8.
Litvaitis, J. A., Villafuerte, R., 1996. Intraguild pre-
dation, mesopredator release, and prey stability.
Conservation Biology, 10: 676–677.
Macdonald, D. W., Loveridge, A. J., Atkinson, R. P.,
2004. A comparative study of side–striped jackals
in Zimbawe: the inuence of habitat and congeners.
In: Biology and conservation of wild canids: 255–270
(D. W. Macdonald, C. Sillero–Zubiri, Eds.). Oxford
University Press, Oxford, United Kingdom.
McShea, W. J., 2005. Forest ecosystems without car-
nivores: when ungulates rule the world. In: Large
carnivores and the conservation of biodiversity:
138–152 (J. C. Ray, K. H. Redford, R. Steneck,
J. Berger, Eds.). Island Press, Washington, DC.
Mitchell, B. D., Banks, P. B., 2005. Do wild dogs ex-
clude foxes? Evidence for competition from dietary
and spatial overlaps. Austral Ecology, 30: 581–591.
Monterroso, P., Garrote, G., Serronha, A., Santos, E.,
Delibes–Mateos, M., Abrantes, J., Perez de Ayala,
R., Silvestre, F., Carvalho, J., Vasco, I., Lopes, A. M.,
Maio, E., Magalhães, M. J., Mills, L. S., Esteves, P.
J., Simón, M. Á., Alves, P. C., 2016. Disease–medi-
ated bottom–up regulation: An emergent virus affects
a keystone prey, and alters the dynamics of trophic
webs. Scientic Reports, 6, doi: 10.1038/srep36072
Neal, E., Cheeseman, C. L., 1996. Badgers. T & AD
Poyser Natural History, London.
Pace, M. L., Cole, J. J., Carpenter, S. R., Kitchell, J. F.,
1999. Trophic cascades revealed in diverse ecosys-
tems. Trends in Ecology & Evolution, 14: 483–488.
Palomares, F., Ferreras, P., Fedriani, J. M., Delibes,
M., 1996. Spatial relationships between Iberian lynx
and other carnivores in an area of south–western
Spain. Journal of Applied Ecology, 33(11): 5–13.
Palomares, F., Gaona, P., Ferreras, P., Delibes, M.,
1995. Positive effects on game species of top pred-
ators by controlling smaller predator populations:
an example with lynx, mongooses, and rabbits.
Conservation Biology, 9: 295–305.
Revilla, E., Palomares, F., 2002. Does local feeding
specialization exist in Eurasian badgers? Canadian
Journal of Zoology, 80: 83–93.
Ripple, W. J., Estes, J. A., Schmitz, O. J., Constant,
V., Kaylor, M. J., Lenz, A., Motley, J. L., Self, K. E.,
Taylor, D. S., Wolf, C., 2016. What is a trophic cas-
cade? Trends in Ecology & Evolution, 31: 842–849.
Ritchie, E. G., Elmhagen, B., Glen, A. S., Letnic, M.,
Ludwig, G., McDonald, R. A., 2012. Ecosystem
restoration with teeth: what role for predators?
Trends in Ecology & Evolution, 27: 265–271.
Ritchie, E. G., Johnson, C. N., 2009. Predator inter-
actions, mesopredator release and biodiversity
conservation. Ecology Letters, 12: 982–998.
Rodríguez, A., Calzada, J., 2015. Lynx pardinus:
The IUCN Red List of Threatened Species 2015:
e.T12520A50655794.
Roemer, G. W., Gompper, M. E., Van Valkenburgh,
B., 2009. The ecological role of the mammalian
mesocarnivore. BioScience, 59: 165–173.
Roper, T. J., 1994. The European badger (Meles
meles): food specialist or generalist? Journal of
Zoology, 234: 437–452.
Schmidt, K., 2008. Behavioural and spatial adaptation
of the Eurasian lynx to a decline in prey availability.
Acta Theriologica, 53: 1–16.
Simón, M. A., Gil–Sánchez, J. M., Ruiz, G., Garrote,
G., Mccain, E. B., FernÁndez, L., López–Parra,
M., Rojas, E., Arenas–Rojas, R., Rey, T. D., 2012.
Reverse of the decline of the endangered Iberian
lynx. Conservation Biology, 26: 731–736.
Sogbohossou, E. A., Kassa, B. D., Waltert, M.,
Khorozyan, I., 2018. Spatio–temporal niche parti-
tioning between the African lion (Panthera leo leo)
and spotted hyena (Crocuta crocuta) in western
African savannas. European Journal of Wildlife
Research, 64: 1.
Tannerfeldt, M., Elmhagen, B., Angerbjörn, A., 2002.
Exclusion by interference competition? The rela-
tionship between red and arctic foxes. Oecologia,
132: 213–220.
Terborgh, J., 2001. Ecological meltdown in predator–
free forest fragments. Science, 294: 1923–1926.
Thompson, J. N., 1988. Variation in interspecic
interactions. Annual review of ecology and sys-
tematics, 19: 65–87.
Valverde, J. A., 1963. Información sobre el lince en
España. Ministerio de Agricultura. Dirección Ge-
neral de Montes, Caza y Pesca Fluvial. Servicio
Nacional de Pesca Fluvial y Caza.
Van Der Meer, J., Ens, B. J., 1997. Models of inter-
ference and their consequences for the spatial
distribution of ideal and free predators. Journal of
Animal Ecology, 66(6): 846–858, doi: 10.2307/6000
Villafuerte, R., Gortázar, C., Angulo, E., Cabezas,
S., Millán, J., Buenestado, F., 2000. Situación del
conejo y la perdiz en Andalucía. Evaluación de las
medidas de su gestión. Technical report, Junta de
Andalucía, Sevilla. [In Spanish].
Villafuerte, R., Lazo, A., Moreno, S., 1997. Inuence
of food abundance and quality on rabbit uctua-
tions: conservation and management implications
in Doñana National Park (SW Spain). Rev. Ecol.
(Terre Vie), 52: 345–356.
Virgós, E., Mangas, J. G., Blanco–Aguiar, J. A.,
Garrote, G., Almagro, N., Viso, R. P., 2004. Food
habits of European badgers (Meles meles) along an
altitudinal gradient of Mediterranean environments:
a eld test of the earthworm specialization hypoth-
esis. Canadian Journal of Zoology, 82: 41–51.
Virgós, E., Travaini, A., 2005. Relationship between
small–game hunting and carnivore diversity in cen-
tral Spain. Biodiversity & Conservation, 14: 3475.
Voigt, D. R., Earle, B. D., 1983. Avoidance of coyotes
by red fox families. The Journal of Wildlife Man-
agement, 47: 852–857.
Wikenros, C., Ståhlberg, S., Sand, H., 2014. Feeding
under high risk of intraguild predation: vigilance
patterns of two medium–sized generalist predators.
Journal of Mammalogy, 95: 862–870.
