Journal of Threatened Taxa |
www.threatenedtaxa.org | 17 February 2020 | 12(2): 15221–15228
ISSN 0974-7907 (Online) | ISSN 0974-7893
(Print)
doi: https://doi.org/10.11609/jott.4829.12.2.15221-15228
#4829 | Received 16 January 2019 | Final
received 05 June 2019 | Finally accepted 09 October 2019
Breaking barriers: Iberian Lynx Lynx pardinus Temminck, 1827 (Mammalia: Carnivora: Felidae) colonizing
Olive groves
Germán Garrote
1, José Francisco Bueno 2, Manuel Ruiz 3, Santiago
de Lillo 4, José Manuel Martin 5, Manuel Moral 6
& Miguel Angel Simón 7
1,2,3,4,5,6 Agencia
de Medio Ambiente y Agua de Andalucía, c/ Johan
Gutenberg s/n, Isla de la Cartuja, 41092, Seville,
Spain.
7 Consejería
de Medio Ambiente de la Junta de Andalucía, c/ Doctor
Eduardo García-Triviño López, 15. 23009, Jaén, Spain.
1 gergarrote@gmail.com
(corresponding author), 2 jfrancisco.bueno@juntadeandalucia.es, 3
manuel.ruiz@juntadeandalucia.es,
4 santiago.lillo@juntadeandalucia.es,
5 jmanuel.martin@juntadeandalucia.es, 6 mmoral@agenciamedioambienteyagua.es,
7 miguelsimon03@gmail.com
Editor: Angie Appel,
Wild Cat Network, Bad Marienberg, Germany. Date of publication: 17 February
2020 (online & print)
Citation: Garrote,
G., J.F. Bueno, M. Ruiz, S. de Lillo, J.M. Martin, M. Moral & M.A. Simón (2020). Breaking barriers: Iberian Lynx Lynx pardinus Temminck, 1827 (Mammalia: Carnivora: Felidae) colonizing
Olive groves. Journal of Threatened Taxa 12(2): 15221–15228. https://doi.org/10.11609/jott.4829.12.2.15221-15228
Copyright: © Garrote et al. 2020. Creative Commons Attribution
4.0 International License. JoTT allows unrestricted use, reproduction, and
distribution of this article in any medium by providing adequate credit to the
author(s) and the source of publication.
Funding: LIFE Project 10NAT/ES/570.
Competing interests: The authors
declare no competing interests.
Author details: Dr. Germán Garrote has been working in research and
conservation of the Iberian Lynx since 2000. José
Francisco Bueno, Manuel Ruiz, Santiago de Lillo, José Manuel Martin and Manuel Moral are field assistants of
the Iberian Lynx conservation program of the Agencia
de Medio Ambiente y Agua de Andalucía, Spain. Miguel Ángel Simón
was the director of this program for 20 years and is now retired.
Author contribution: Germán Garrote designed the
study, conducted the field surveys, compiled the data and wrote this
manuscript. Bueno, Ruiz, Lillo, Martin and Moral conducted the field
surveys. M.A.SImon wrote this manuscript.
Acknowledgements: The study was supported by the
LIFE Project 10NAT/ES/570 “Recovery of the historical distribution of the
Iberian Lynx (Lynx pardinus) in Spain and
Portugal”.
Abstract: In recent years, the Andújar-Cardeña Iberian Lynx Lynx
pardinus population has grown both in number and
in occupied surface area. This feline
has spread into areas surrounding existing population nuclei and occupied new
habitats including human-dominated areas and tree crops. Here we describe this colonization process
and the evolution of the Iberian Lynx populations in the Olive Olea europaea groves that surround typical Lynx scrub
habitats in Andújar-Cardeña. Our findings were obtained through
radio-tracking, camera trapping and European Rabbit Oryctolagus
cuniculus monitoring. Two colonized
areas—Zocueca and Marmolejo-Montoro—were
identified in which Olive cultivation is predominant. Since 2011, a total of 45 and 50 different
individuals have been detected in Zocueca and Marmolejo-Montoro, respectively. At present, 19 individuals are known to live
in Zocueca and 29 in Marmolejo-Montoro. The main cause of mortality is
road-kills. Our results suggest that the
Iberian Lynx is capable of colonizing human-modified areas such as agricultural
land provided that they can support high-density Rabbit populations and the
causes of non-natural mortality are minimized.
Keywords: Agricultural land, camera
trapping, human-dominated habitat, radio telemetry, Sierra Morena.
Resumen: En los últimos años,
la población de lince ibérico de Andújar-Cardeña
ha crecido tanto en número como en superficie ocupada. Este felino se ha
extendido a áreas que rodean
los núcleos de población existentes y ha ocupado nuevos hábitats, incluyendo áreas
dominadas por humanos y cultivos arbóreos. En este trabajo se describe este proceso de colonización y la evolución de las poblaciones de
lince ibérico en los olivares Olea
europaea que rodean sus hábitats típicos de matorral mediterráneo en Andújar-Cardeña. Nuestros hallazgos se obtuvieron mediante radioseguimiento, fototrampeo y seguimiento de la población de conejos. Se identificaron dos áreas colonizadas, Zocueca
y Marmolejo-Montoro, en las
que predomina el cultivo del olivo.
Desde 2011, se han detectado
un total de 45 y 50 individuos
diferentes en Zocueca y Marmolejo-Montoro, respectivamente.
En la actualidad, se sabe
que 19 individuos viven en Zocueca y 29 en Marmolejo-Montoro. La
principal causa de mortalidad son
los atropellos. Nuestros
resultados sugieren que el lince ibérico es capaz de colonizar áreas modificadas por humanos, como tierras agrícolas, siempre que existan poblaciones de conejos de alta densidad y se minimicen las causas de la mortalidad
no natural.
Introduction
The global expansion of human activities has
had profound consequences for wildlife (Gaynor et al. 2018). Human-induced
habitat degradation and loss, prey depletion and poaching are widely recognized
as the main threats to carnivores (Karanth et al.
2004; Groenendijk et al. 2015; Wolf & Ripple
2016), causing widespread declines in their populations (Carter & Rosas
1997; Lodé et al. 2001; Ripple et al. 2014). Nevertheless, in recent decades a certain
stabilization or even increase in the abundance of some carnivore populations
has taken place owing foremost to protective legislation, greater public
concern and a variety of policies that encourage co-existence between humans
and carnivores (Recharte & Bodmer
2010; Chapron et al. 2014). Some carnivore species can now settle in and
use human-altered landscapes if there are no human activities that act as
impediments (Dellinger et al. 2013; Garrote et al. 2013). Thus, understanding and then managing
carnivore responses to landscape heterogeneity and to the human-driven changes
occurring therein are now two main priorities in ecological research and
applied conservation techniques (Fahrig et al. 2011).
The Iberian Lynx Lynx
pardinus is an Iberian endemic specialist
predator whose staple prey is the European Rabbit Oryctolagus
cuniculus (Fedriani et al. 1999; Gil-Sánchez et
al. 2006). Its populations dropped
dramatically in the 20th century (Gil-Sánchez & McCain 2011) to
the point that at the beginning of the 21st century, less than 100
Lynx were estimated to remain in just two isolated populations in eastern
Sierra Morena and Doñana (Simón et al. 2012; Guzmán
et al. 2004). This decline was
attributed to the combined effects of habitat destruction and fragmentation,
declines in European Rabbit abundance, and hunting and/or poaching (Guzman et
al. 2004; Rodríguez & Delibes 2004).
As a result, the species was listed as Critically Endangered in 2002
(Cat Specialist Group 2002). Since then,
the Iberian Lynx population increased significantly in size due to measures carried
out as part of conservation projects (Simón et al. 2012) designed to increase
the carrying capacity of occupied habitats by enhancing European Rabbit
populations, reducing known causes of mortality, and creating new populations
through reintroductions (Simón et al. 2012).
These actions succeeded in population recovery, so that the Iberian Lynx
was downlisted to Endangered in 2015 (Rodríguez &
Calzada 2015).
By 2017, the minimun number of Iberian Lynx
detected in the wild was estimated at 589 individuals (Simón 2018). Specifically, the population in Andújar-Cardeña rose from 79 individuals in an area of
153km2 in 2004 to 195 individuals detected in 520km2 in
2017. During the period of 13 years, the
Lynx has spread to areas surrounding its main remnant population nuclei that
contain apparently suboptimal habitats such as humanized areas and tree crops
(Garrote et al. 2013, 2016).
On the southeastern edge of the range of the Andújar-Cardeña Lynx population, the Mediterranean
scrubland borders vast swathes of intensively cultivated Olive Olea europaea groves.
The first Lynx to establish territories here were detected in 2012, and
the first breeding attempt in this type of habitat was recorded in 2013
(Garrote et al. 2015). Thereafter, more
Lynx began to occupy this area and a new Lynx subpopulation was established 8km
to the south of the main population in an area dominated by Olive groves. Below, we describe the colonization process
and evolution of the Iberian Lynx populations that now thrive in these new
habitats.
Study areas
Andújar-Cardeña in eastern Spain’s Sierra Morena (Figure 1) is an area with low
mountains covered by well-preserved Mediterranean forests and scrublands where
most of the land is occupied by large hunting reserves. It is located between Guadalmellato
(25km to the west) and Guarrizas (30km to the east),
where Iberian Lynx were reintroduced since 2010. By 2017, the minimum number of individuals
detected in Guadalmellato and Guarrizas
were 82 and 85 individuals, respectively (Simón 2018). On the southern to southeastern edge of Andujar-Cardeña, the Mediterranean scrubland borders two
large areas of intensive Olive cultivation consisting of old trees set in
parallel lines, Marmolejo-Montoro and Zocueca. Due to the
intensive management of these groves, few patches of shrubs or meadows still exist,
the only exceptions to this uniformity being small rocky outcrops that cannot
be managed, scattered stands of Mastic Tree Pistacia
lentiscus and Holly Oak Quercus coccifera, and narrow (< 2m) gullies lined with
Giant Cane Arundo donax
and young White Poplar Populus alba. To the south of both areas flows the
Guadalquivir River, which is surrounded by a gallery forest consisting mainly
of White Poplar.
Materials and
Methods
Our findings were obtained as part of the
Iberian Lynx population-monitoring program carried out within the framework of
the Iberian Lynx Life Project (see Simón 2012; Simón et al. 2012). This monitoring program employs
radio-tracking, camera trapping and Rabbit population monitoring. Radio-tagged Lynxes were captured using double-entrance,
electro-welded mesh box traps (2×0.5×0.5 m) baited with Rabbits where Lynx were
trapped and then fitted with VHF radio collars (Wagener Collar, Brenaerham, Germany).
The VHF radio-tracking routine consisted of obtaining 1–5 locations by
triangulation each week. We used the
Locate extension of the QGIS 2.2.0 (QGIS Development Team, 2014) program to
obtain locations from the field data.
Camera traps were deployed across the entire Iberian Lynx distribution
area (Gil-Sánchez et al. 2011). During
the year, signs of Lynx presence like tracks and excrements were searched for
in the known distribution area and in its periphery. When such signs were detected in a new area,
camera traps were installed to confirm the species’ presence and to attempt to
identify the individuals present. In this way, we were able to identify the
areas into which the species was expanding, which were then incorporated into
the annual population-monitoring program.
We designed a camera trapping grid system each year, with a mean
distance between cameras of 1.36±1.03 km.
Surveys lasted from June to July until October to November to maximize
detection of kittens. The camera
stations were kept active for a period of two to five months, depending on
efficiency and redundancy of captures.
Cameras were baited with Lynx urine or with live bait, either Rabbits or
Rock Pigeons Columba livia in wire cages
inaccessible by Lynxes. Each camera trap
was visited once a week allowing to download pictures, to replenish urine or
batteries and to care for live bait. Due
to high levels of human frequentation and unrestricted access, only Lynx urine
was used as bait in the Olive groves to avoid camera theft. Two camera trap models were used in this
study: Moultrie M880 and Covert II Assasin. Lynxes were individually identified on the
basis of their spot pattern (Garrote et al. 2011). Fecundity was assessed yearly by camera
trapping through counting the number of kittens that accompanied each adult
female after the breeding season. Therefore,
our measure of fecundity is in regards to the number of kittens per territorial
female detected during the period of post-weaning dependence (Monterroso et al. 2016).
We identified a Lynx as territorial if the individual had breeding
status, determined through detection of kittens, and/or if the camera trapping
results or radiotracking data supported a non-overlapping surface (Gil-Sánchez
et al. 2011). The information obtained
from the camera traps and radio-tracking enabled us to delimit the species’
annual area of presence in a grid of 1x1 km2.
European Rabbit populations were monitored
using latrine counts (> 20 pellets in a circle with an area > 30cm2)
along transects. Latrine counts are an
indirect method that is frequently used to estimate relative Rabbit abundance
over large areas (Virgós et al. 2003), which is
calculated as a kilometric abundance index (KAI) of latrines. The complete Iberian Lynx distribution area
was divided into 2.5×2.5 km2 squares. Latrine counts were carried out along 4.5–7
km transects in each square. Sampling
was conducted once a year in June and July at the end of the Rabbits’ breeding
season (June–July) when the populations reached their greatest density (Beltrán 1991).
Results
Two areas dominated by Olive cultivation were
identified as having been colonised by Iberian
Lynx. The first, Zocueca,
is located on the southeastern edge of the main population (Figure 1). A total of 56 camera traps were installed in
this area from 2011 to 2017, yielding a sampling effort of 2,017 trap
nights. A total of 46 different
individuals were identified throughout the study period. The first Lynx was detected in 2011. In 2017, a minimum of 19 individuals were
detected in an area of 53km2 (Table 1).
The second area, Marmolejo-Montoro,
lies 8km to the south-west of the main Andújar-Cardeña
Lynx population. The first two Lynx were sighted and radio-detected here in
2013; one was a radio-collared individual from the main Andújar-Cardeña
population (Table 1). A total of 58
camera traps were installed in this area from 2013 to 2017, yielding a sampling
effort of 7,474 trap nights. A total of
50 different individuals were identified throughout the study period. In 2017, a minimum of 29 individuals had been
detected in an area of 82km².
Nine Lynx with radio-collars were monitored
in Zocueca and seven in Marmolejo-Montoro. Of these 16 individuals, seven were captured
and radio-marked in Olive groves in the study area; 10 were individuals that
had been marked in other areas and had dispersed into the study area. These Lynx originated from the Andújar-Cardeña population (n=4), and from the individuals
reintroduced into Guarrizas (n=3) and Guadalmellato (n=3) (Figure 1). One of the Lynx radio-marked in Marmolejo-Montoro established itself in Zocueca.
Rabbit abundances in the two areas are
similar, with an annual average of 20.92+-3.59 latrines/km in Zocueca (years 2013–2017) and 21.84+-8.90 latrines/km in Marmolejo-Montoro (years 2014–2017).
A total of 11 Lynx breeding attempts were
detected in Zocueca and 13 in Marmolejo-Montoro. Average fecundity was 1.46±0.70 and 1.68±0.69
kittens/year/territorial female in Zocueca and Marmolejo-Montoro, respectively.
In all, 22 Lynx deaths were reported (Table
2), with road accidents being the most frequent cause of death in both
populations (63%). Disease was the
second commonest cause of death (18%): of the four known cases, one was a
five-year-old territorial female that died of tuberculosis; and the other three
were old animals that had lost their territories and had wandered into this
area.
Discussion
Our results show that the Iberian Lynx has
colonized the Olive groves that border the Mediterranean scrub habitats in the
mountains of Andújar and Cardeña. When the Lynx’s range was at its smallest and
restricted to just Doñana and Andújar,
the research showed that its preferred habitat was found to be Mediterranean
shrublands (Palomares et al. 2000; Fernández et al.
2006). Specifically, Lynx showed a
preference for areas with shrub cover of over 35%, rocky outcrops and high
densities of European Rabbits (Palomares et al. 2000;
Palomares 2001; Fernández et al. 2006), whereas
arable areas and woody crops were identified as unsuitable habitats (Palomares 2001; Fernández et al. 2006). Nevertheless, our findings suggest that the
ecology of the Iberian Lynx is more plastic than originally thought, and that
it is able to use habitats including agricultural areas that were deemed
unsuitable (Palomares et al. 2000). Although some patches of scrub must be
present in the chosen agricultural areas, research shows that the Iberian Lynx
can establish territories and even reproduce in areas with only 2% shrub cover
as long as suitable Rabbit densities exist (Garrote et al. 2016).
The presence of this feline is dependent on
Rabbit abundance, which directly affects its demography and, above all, its
breeding rates (Monterroso et al. 2016). The appearance in 2011 of a new variant of
the Rabbit Haemorrhagic Disease Virus (RHDV2), also
known as Lagovirus europaeus
GI.2 (hereafter GI.2; Le Pendu et al. 2017) in
European Rabbit populations led to a decline of 60–70% in Rabbit populations in
Andújar-Cardeña, which was followed by a fall of
45.5% in Lynx breeding rates from 1.36±0.12 kittens/year/territorial female
before GI.2 to 0.13±0.07 (2011–2013; Monterroso et
al. 2016). Emergency management actions
implemented to alleviate the effects of GI.2 (i.e., Rabbit restocking
operations and the setting up of supplementary feeding stations) prompted a
significant increase in Lynx fecundity (2012–2017: 0.82±0.19
kittens/year/territorial female, unpublished data). Pre-GI.2 fecundity values, however, have not
yet been restored. In the Olive groves
where Rabbit abundance was three times higher than in Andújar-Cardeña
(07.13±0.62 latrines/km; unpublished data), Lynx fecundity reached 1.46±0.70
and 1.68±0.69 kittens/year/territorial female in Zocueca
and Marmolejo-Montoro, respectively. These values are higher than the fecundity
detected in the Andújar-Cardeña Lynx population
during the same period and similar to values during the pre-GI.2 period. Evidently, Lynx breeding rates are not
impeded by the use of Olive grove habitat.
The recovery of the Iberian Lynx population
in Andújar-Cardeña was due to two main factors: (i) the carrying capacity of the habitat was increased by
improving Rabbit populations and (ii) non-natural mortality was reduced (Simón
et al. 2012; López et al. 2014). In the
most remote areas where the impact of human presence is minimal, the main
strategy employed was the reinforcement of Rabbit populations. In more peripheral areas, where Rabbit
populations are strong enough to sustain the territorial Lynx’s, the emphasis
was put on reducing non-natural mortality via an anti-poaching program, the
identification of road black-spots and educational activities. As a consequence of these conservation
efforts, Lynx mortality (compared to figures from the 1980s and 1990s) has
decreased significantly, not only in Andújar-Cardeña
but throughout its whole range (Simón et al. 2012; Lopez et al. 2014). The highest abundance (n = 202 individuals)
and density (0.72 individuals/km2) of the Lynx population in Andujar-Cardeña was reached between 2010 and 2011. This coincides with the completion of the
conservation efforts to increase the carrying capacity of the Lynx. It was also during this time that the first
Lynx was detected in the Olive groves.
Almost simultaneously, the appearance of the aforementioned GI.2 caused
a significant decline in Rabbit populations in areas of historical presence,
reaching minimum densities in 2013 (Monterroso et al.
2016). Therefore, the process of
colonization of Olive groves by the Lynx could be due to the search for new
territories due to intraspecific competition, conditioned by demographic
pressure, and subsequently exacerbated by the reduction in the carrying
capacity of the medium due to the drastic decline of food. It is after the settlement of the first Lynx
native to Andujar-Cardeña, when dispersing Lynx of the
neighboring Guarrizas and Guadalmellato
populations were detected.
It has become obvious that the Iberian Lynx
can colonize areas such as Olive groves that have been altered by human
activities, provided that good Rabbit populations exist and that mortality
rates are kept to acceptable levels (López-Parra et al. 2012; Garrote et al.
2013; López et al. 2014). The
colonization of these areas improved connectivity between Lynx populations in Andújar-Cardeña, Guarrizas and Guadalmellato, and stimulated a continuous exchange of
individuals. Today, these populations
can be considered a single metapopulation.
The vast areas of agricultural land surrounding traditional Lynx
habitats were always regarded as unsuitable and obstructing the species’
expansion. Nevertheless, the historical
absence of the Lynx in these areas could in fact be more closely tied to
human-induced mortality than to any lack of habitat resources (Corsi et al. 1999; Gastón et al. 2016). Given the scarcity of European Rabbits in
most Iberian habitats (Delibes-Mateos et al. 2014),
agricultural areas with small patches of scrub could become the most
Rabbit-rich habitat in the Lynx’s range (Calvete et
al. 2004). Therefore, management should
be orientated towards allowing small shrubby patches to be conserved in Olive
groves and other agricultural areas.
Likewise, vigorous actions must be implemented to reduce non-natural
mortality, which would notably increase the useful surface available for
Iberian Lynx.
Table 1. Results of the Iberian
Lynx population-monitoring in our study area.
|
|
2011 |
2012 |
2013 |
2014 |
2015 |
2016 |
2017 |
|
ZOCUECA |
|
|
|
|
|
|
|
|
Individuals |
1 |
4 |
12 |
11 |
10 |
14 |
19 |
|
Breeding females |
0 |
0 |
2 |
3 |
3 |
4 |
4 |
|
Breeding events |
0 |
0 |
1 |
2 |
1 |
3 |
4 |
|
Kittens |
0 |
0 |
2 |
5 |
2 |
6 |
10 |
|
Kittens/breeding females |
0 |
0 |
1 |
1.7 |
0.7 |
1.5 |
2.5 |
|
Surface |
2 |
12 |
27 |
47 |
44 |
54 |
53 |
|
Rabbit abundance |
- |
- |
22.5 |
18.8 |
18.9 |
26.2 |
19.5 |
|
Radio-tagged individuals |
0 |
1 |
2 |
3 |
5 |
4 |
5 |
|
Camera-trap stations (trap
nights) |
2 (62) |
2 (175) |
5 (225) |
5 (246) |
20 (433) |
11 (446) |
11 (430) |
|
MARMOLEJO-MONTORO |
|
|
|
|
|
|
|
|
Individuals |
|
|
2 |
9 |
24 |
28 |
29 |
|
Breeding females |
|
|
0 |
2 |
5 |
5 |
6 |
|
Breeding events |
|
|
0 |
1 |
5 |
3 |
4 |
|
Kittens |
|
|
0 |
2 |
13 |
9 |
8 |
|
Kittens/breeding females |
|
|
0 |
1.0 |
2.6 |
1.8 |
1 |
|
Dead |
|
|
0 |
0 |
0 |
3 |
2 |
|
Surface |
|
|
8 |
19 |
73 |
85 |
82 |
|
Rabbit abundance |
|
|
- |
9.1 |
29.6 |
25.4 |
23.2 |
|
Radio-tagged individuals |
|
|
1 |
1 |
1 |
6 |
6 |
|
Camera-trap stations (trap
nights) |
|
|
- |
11 (1068) |
14 (1146) |
16 (2289) |
17 (2971) |
Table 2. Cause-specific mortality
detected in the Zocueca and Marmolejo-Montoro
Iberian Lynx populations in the period 2011–2017.
|
|
Zocueca |
Marmolejo-Montoro |
|
Road-kill |
10 |
4 |
|
Poaching |
1 |
0 |
|
Disease |
4 |
0 |
|
Fight |
2 |
0 |
|
Total |
17 |
5 |
For
figure & images - - click here
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