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Feline leukaemia virus outbreak in the endangered Iberian lynx and the role of feeding stations: a cautionary tale


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Feline leukaemia virus outbreak in the endangered Iberian lynx and the role of feeding stations: a cautionary tale


F. Palomares, J. V. Lo´ pez-Bao & A. Rodr´ıguez
Department of Conservation Biology, Estacio´ n Biolo´ gica de Don˜ ana (CSIC), Sevilla, Spain

Correspondence

Francisco Palomares, Department of Conservation Biology, Estacio´ n Biolo´ gica de Don˜ ana (CSIC), Ame´ rico 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 atten- tion 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 Gato- Arrayan (DGA)]. All lynx known to be inhabiting CR and Vera subpopulations, and three of seven in DGA subpopu- lation were trapped during that trapping campaign. Cap- tured 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 aggres- sive 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


Figure 1 Distribution of Iberian lynx Lynx pardinus tested against FeLV by Lo´ pez 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 Don˜ 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 Lo´ pez 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 Roma´ n’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 (Ja- nuary–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 in- fected with the disease, whereas two out of five non- neighbouring adult males belonging to a different subpopu- lation (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 monitor- ing 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 re- vealed a common origin for the FeLV found in all lynxes (Meli et al., 2010). However, the most parsimonious explana- tion 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 trans- mission 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 patho- gens. 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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