Density reduction, particularly culling (i.e. the widespread killing of hosts regardless of infection status), has been undertaken to reduce the incidence of rabies and therefore eliminate the disease on the basis that transmission is density-dependent. As previously discussed, the assumption of density dependence originates from the interpretation of cycles in wildlife rabies and thresholds for the invasion for foxes and dogs. However, the fact that culling has failed to achieve sustained control of rabies in wildlife and dogs (Kaplan, Goor & Tierkel 1954; Anderson et al. 1981; Macdonald & Voigt 1985; Anderson 1986; Beran & Frith 1988; WHO 2004; Windiyaningsih et al. 2004; Cleaveland et al. 2006) may be the best evidence that a simple relationship between disease incidence and host population density does not exist for rabies. We now discuss evidence from culling programmes (dogs and wildlife) followed by more limited evidence on sterilization campaigns.
Culling has been shown to be ineffective in controlling rabies in all host species. Rabies persisted in foxes in New York State despite ‘concentrated reduction campaigns’ following an outbreak in 1945, while simultaneous vaccination of dogs in the State eliminated rabies from this species (Friend 1968). Similarly, in Denmark in 1964, culling did not prevent rabies outbreaks in foxes; however, rabies did not occur where dogs in the same region had been vaccinated (Muller 1966, 1971). In response to a rabies outbreak in 1997, nearly 300 000 dogs, approximately half of the population estimated at the start of the outbreak, were culled in Flores, Indonesia over a period of 4 years. However, in 2004, rabies was still endemic although the total dog population was still considerably reduced (Windiyaningsih et al. 2004). Culling failed to control canine rabies in Korea (Lee et al. 2001) and Israel (Kaplan, Goor & Tierkel 1954), whereas subsequent vaccination in both countries controlled the disease.
Culling has been used to control ongoing outbreaks and to prevent the invasion of rabies in foxes. Declines in rabies cases have followed outbreaks irrespective of active culling (Bogel et al. 1974), with stochastic extinction expected (Anderson et al. 1981) particularly where disease-induced mortality is substantial (Bogel et al. 1974). Within a given area, culling might be expected to amplify these processes, increasing the probability of stochastic extinction regardless of density dependence. Indeed, rabies appeared to die-out in some areas where fox dens were gassed (Wandeler et al. 1974b). However, the limited data available are unclear regarding how culling interacts with disease-induced mortality during an epidemic and how it may change disease dynamics (Wandeler et al. 1974b). Other processes may also counter the effect of density reduction on disease incidence. Examples include social perturbations, as demonstrated in badger populations (Woodroofe et al. 2006a,b), and interactions between the level of culling, age structure (Bolzoni, Real & De Leo 2007) and demographic processes (Choisy & Rohani 2006).
Culling has also failed to prevent outbreaks of rabies in foxes in previously unaffected areas or the recurrence of the disease in areas where it had died-out, as observed in southern Denmark (Muller 1971). Where density-dependent transmission has been assumed, invasion thresholds are reported to vary and to be low (i.e. <1 fox km−2 in Europe and <0·4 foxes km−2 in Ontario). Thus, even if transmission were density-dependent, reductions in density to below an invasion threshold may not be achievable practically or be sustainable (Wandeler et al. 1974a; Anderson et al. 1981).
Culling has generally failed to eliminate outbreaks of rabies in dogs. In our review of the scaling of rabies transmission rates with density (in the previous sections), we have found no conclusive evidence to support either the frequency-dependent or density-dependent assumption for canine rabies. We are therefore unable to unequivocally conclude that the ineffectiveness of culling is because transmission is frequency-dependent. An alternative explanation is that reductions in densities to below invasion thresholds are not achievable practically. Canine rabies can circulate where densities are as low as 1·36 dogs km−2 (Hampson 2009), which is substantially lower than the densities reported for most free-roaming dog populations. Under the assumption of density-dependent contact rates, culling and vaccination should have similar impacts on disease incidence. Thus, given estimated values of R0 < 2, control should be achieved by culling at most half the population. Yet, in Flores, Indonesia, rabies persisted after this level of culling was achieved (Windiyaningsih et al. 2004). More generally, the stochastic persistence of canine rabies despite low attack rates and considerable density reduction is interesting irrespective of the mode of transmission.
The fact that rabies often persists despite culling may be a function of human factors. The continual translocation of dogs (some infected) with people (Beran & Frith 1988; Denduangboripant et al. 2005; Coetzee & Nel 2007; Kasempimolporn, Jitapunkul & Sitprija 2008; Zinsstag et al. 2009) may offset the selective removal of infectious and in-contact dogs and stochastic extinctions. Where culling occurs simultaneously, translocation may also offset any reductions in the incidence of rabies. In addition, translocation may be exacerbated in response to culling campaigns. For example, within a few days of a village-wide cull in Kelusa, Bali, where rabies had not occurred previously, two residents brought in unvaccinated, potentially infected puppies from outside the village to replace their culled, vaccinated adult dogs. As attack rates are typically very low, culling predominately removes healthy dogs, and some of these may be vaccinated and hence unlikely to become infected. Other compensatory mechanisms may also offset reductions in host density. These include concomitant reductions in mortality from reduced competition for food (although the actual intensity of competition in free-roaming dogs is unknown), reductions in the dumping of surplus puppies/unwanted dogs and improved care of dogs. To address these issues, we are currently investigating the effects of human behaviour in response to culling on dog population dynamics and disease transmission in Kelusa.
The ethics of culling healthy, free-roaming animals in conjunction with vaccination programmes are also debatable. Raccoons have been culled on Wolfe Island, Ontario, as a means to reduce the number of animals that needed to be trapped and vaccinated (Rosatte et al. 2007). The same justification may be extended to dogs, and a variable degree of culling of free-roaming dogs, historically regarded as ‘strays’, has often been undertaken alongside mass vaccination programs (Wells 1954; Cheuk 1969; Larghi et al. 1988; Ernst & Fabrega 1989). However, despite appearances, the vast majority of free-roaming dogs in most societies globally are owned (WHO & WSPA 1990; Cleaveland & Dye 1995; Butler & Bingham 2000; Windiyaningsih et al. 2004) and in reasonable health. Not only are these dogs more accessible to vaccination than commonly recognized, but culling healthy animals can result in unintended negative consequences on both animal welfare and disease control.
The use of immunological and chemical sterilization has been modelled for the control of rabies in wildlife and in dogs (Suppo et al. 2000; Smith & Cheeseman 2002; Carroll et al. 2010). However, only surgical sterilization has been used in dogs under field conditions. Sterilizations are usually carried out by nongovernmental organizations and local authorities, which aim to vaccinate and simultaneously sterilize at least 70% of the dog population (Totton 2009). Limited data suggest that these programs reduce the incidence of rabies and may stabilize or gradually reduce population density over time-scales of several years (Reece & Chawla 2006; Totton 2009; Totton et al. 2010). However, the respective impacts of vaccination and sterilizations have not been assessed. Reductions in population density may plausibly reduce the number of dogs that require vaccination, although timely reductions in density may be constrained by resources and population dynamics (Hemachudha 2005). As with culling, the demand for dogs by communities may result in an increase in dog importation where local supply has been reduced by sterilization. Thus, we are studying the effect of human behaviour in response to sterilization on dog population dynamics and disease transmission in Antiga, Bali.