Feline leukaemia virus outbreak in the endangered Iberian
lynx and the role of feeding stations: a cautionary tale
F. Palomares, J. V. Ló pez-Bao & A. Rodrı́guez
Department of Conservation Biology, Estación Biológica de Doñana (CSIC), Sevilla, Spain
Correspondence
Francisco Palomares, Department of Conservation Biology, Estación Biológica de Doñana (CSIC), Américo Vespucio s/n, Isla de la Cartuja, 41092
Sevilla, Spain.
Email: ffpaloma@ebd.csic.es
doi:10.1111/j.1469-1795.2010.00403.x
Lopez et al. (2009) reported a feline leukaemia virus (FeLV)
outbreak in the Iberian lynx Lynx pardinus, and speculated
on the potential negative role of feeding stations (FS)
installed for the supplementary feeding of the Donana lynx
population with domestic rabbits. Supplementary feeding
has proven to be useful in retaining Iberian lynx in areas
with extreme food scarcity where otherwise they would be
absent (Lopez-Bao, Rodrıguez & Palomares, 2008, 2009;
Lopez-Bao et al., 2010). Therefore, misunderstanding the
role of FS in the transmission of the FeLV might lead to
management recommendations regarding the use of FS,
with important conservation repercussions. Lopez et al.
(2009) assumed that all infected lynx belonged to the same
lynx subpopulation [Coto del Rey (CR)] within the Donana
metapopulation. This assumption was incorrect and led to
faulty inferences about the role of FS in FeLV transmission.
Here, we discuss the supposed pro-active role of FS in the
propagation of the FeLV outbreak, and the rationality of
the measures adopted to control the disease, we call attention to the lynx subpopulations that were involved, and how
their identification challenges inferences about the spread of
FeLV and we propose a plausible ecological scenario for
understanding the outbreak.
The FeLV outbreak likely began with the infection of an
adult male called Roman inhabiting the CR subpopulation
(Fig. 1). This male was the only FeLV-positive individual
detected out of 18 trapped lynx in November–December
2006 [10 in CR, five in Vera and three in Dehesa de GatoArrayan (DGA)]. All lynx known to be inhabiting CR and
Vera subpopulations, and three of seven in DGA subpopulation were trapped during that trapping campaign. Captured lynx were transferred from the trap to a transport cage
where they were anaesthetized for tagging, a health check
and collection of biological samples at the same laboratory,
which included ultrasonographical analysis (Goritz et al.,
2009), and electroejaculation of adult males (Ganan et al.,
2010). The individual that was handled 2.5 h after Roman
was an adult male called Uda from the DGA subpopulation.
Between 13 March and 8 May 2007 four lynx were found
dead (Roman, Uda, and two other adult males from CR).
All of them were FeLV viraemic. In April 2007, the control
programme reported by Lopez et al. (2009) began. Between
9 May and 1 August 2007, an additional eight individuals
were found to be FeLV positive, seven of which were
captured in CR and one in DGA (Fig. 1).
If FS had a relevant role in the transmission of feline
leukaemia, individuals sharing FS with Roman would be
expected to have a higher probability of infection than other
individuals. However, none of the other 11 lynx positive for
FeLV shared FS with Roman, and all three lynx that did
share FS were found to be FeLV negative (Fig. 1). The
Iberian lynx exhibits a territorial spatial organization, where
one adult male, one adult female and their offspring o1–2
years old exhibit a high overlap in their home ranges,
whereas little overlap exists between the home ranges of
adults of the same sex (Ferreras et al., 1997; Palomares et al.,
2001). Some males may share their home ranges with more
than one adult female. FS were primarily placed in the core
of lynx territories, in this way minimizing potential aggressive interactions between neighbouring lynx. Lynx visits to
FS were monitored by automatic photographic cameras to
identify the individuals that used the supplementary food,
and to record the frequency with which each individual
visited FS. Using independent methods, it was known that
all lynx living in territories containing FS were in this way
detected inside feeding enclosures; therefore, the probability
of an undetected individual using a feeding station was low
(Lopez-Bao et al. 2009). Out of 709 photographic records
from 15 different lynx that used nine FS in sites where
neighbouring territories were occupied, lynx entered a FS
placed in a neighbouring territory only on three occasions
(0.4%). Two of these records corresponded to visits at the
very beginning of FS operation, before any territory holder
used the enclosure. Once territory owners entered the FS,
this intruder did not visit it again. Outside of Roman’s
territory, four lynx that shared FS with infected individuals
F
Figure 1 Distribution of Iberian lynx Lynx pardinus tested against FeLV by López et al. (2009) during 2006 and 2007. Circles represent known male
or female territories (when males territories were not clearly identified), and a cluster of contacting circles represents one subpopulation within
the Doñ ana metapopulation. During 2006 and 2007, supplementary feeding stations were placed in territories represented by bold circles.
Numbers denote territories where at least one lynx was caught by López et al. (2009), and circles without numbers represent territories inhabited
by lynx where no individual was caught. M, Z2-year-old male; F, Z2-year-old female; m, about 15-month-old males; f, about 15-month-old
females; fc, female cub; mc, male cub; *lynx were FeLV positive; #an individual that arrived to Román’s territory after his death. Individuals that
were checked for FeLV infection during November and December 2006 are underlined.
were found to be FeLV negative. On the other hand, two
cubs that never used FS were infected. These data, in
combination, lend little support to the hypothesis that FS
had a deterministic role in the transmission of FeLV before
or during the outbreak.
The Iberian lynx often kills smaller carnivores (Palomares
& Caro, 1999). Because FeLV needs direct contact between
individuals to be transmitted (Barr & Bowman, 2006),
Roman could have acquired the virus while killing an
infected domestic cat (Meli et al., 2009). A possible way for
FeLV propagation through the lynx population could be
fights between adult males during the mating season (January–February; Palomares et al., 2005). During this season
adult males explore neighbouring territories searching for
females, which may result in aggressive encounters with
other males (Ferreras et al., 1997; Lopez-Bao, Rodrıguez &
Ales, 2008). Wounds exposed to the saliva of infected rivals
may be a mechanism of FeLV transmission. If this is the
case, one might expect that the probability of infection for
adult males in the neighbourhood of Roman’s territory
would be higher than that for non-neighbouring males.
Indeed, all neighbouring adult males of Roman were infected with the disease, whereas two out of five nonneighbouring adult males belonging to a different subpopulation (DGA) were also infected (Fig. 1). How did FeLV
reach the two adult males living in DGA? We cannot discard
the hypothesis that some undetected, infected dispersing
lynx from CR might have transmitted the virus to DGA
males, although this was not supported by intensive monitoring of CR lynx. Also, we cannot discard that any male from
DGA could get the virus after killing another domestic cat,
although sequencing of the envelope surface unit gene revealed a common origin for the FeLV found in all lynxes
(Meli et al., 2010). However, the most parsimonious explanation might be that the male Uda, handled soon after Roman,
was infected with FeLV through improper disinfection of the
equipment used for lynx immobilization and health checking,
while the other positive male in DGA received the virus later
on through mating fights with Uda. Adult females could
receive the virus while mating with infected males, and
juveniles could be infected through suckling and licking from
their infected mothers. The hypothesis that some virus transmission could have taken place during the intensive trapping
campaign of autumn 2006, when nine out of 12 positive lynx
detected by Lopez et al. (2009) were captured and handled,
cannot be discarded.
Finally, Lopez et al. (2009) suggested that a measure to
control the spread of the disease would be to provide just
one rabbit at a time in FS, in order to avoid different lynx
feeding on the same prey. No evidence exists in support of
this proposal. Lynx forage alone, and a rabbit represents a
‘ration prey’ (Delibes, 1980; Aldama, Beltran & Delibes,
1991). This is also the case in FS, in which only 9% of 2238
pictures there were more than one lynx recorded within a FS
(often adult females with their offspring), and we never
witnessed two lynx sharing a prey (41540 h of video
recording in FS examined). Therefore, we infer that the
probability that two or more lynx share a rabbit, in FS or
elsewhere, is very small (see also Aldama & Delibes, 1991),
of course excluding rabbits brought to the cubs by their
mothers, a behaviour that takes place with rabbits caught in
FS or elsewhere.
Despite the lack of clear evidence relating the use of FS with
the transmission of FeLV during the outbreak, a further issue
should be considered. Domestic rabbits consumed by lynx in
FS may have indirectly affected their resistance to FeLV and
subsequent secondary infections with other pathogens (Meli
et al., 2009). The domestic rabbits we supplied in FS were
treated with antibiotics to prevent generalized infections, which
may have entailed some health risks for lynx. Lemus & Blanco
(2009) found that vultures with circulating antibiotics showed
depressed cellular and humoral immune systems compared
with individuals without circulating antibiotics, which suggests
that ingestion of antibiotics may depress the immune system,
temporarily reducing their resistance to opportunistic pathogens. Therefore, exposure to antibiotics may have had a role in
the fatal FeLV outbreak among Donana lynx and should be
further investigated. The impoverished immunological and
genetic condition of the Donana lynx, resulting from high
inbreeding and low MHC genetic diversity (Johnson et al.,
2004; Jimenez et al., 2008; S. Roques, pers. comm.), might also
explain a potentially high vulnerability to diseases, even in the
absence of exposure to antibiotics.
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