Gompper & Williams (Reference Gompper and Williams1998) proposed that a species of Trichodectid louse specific to the black-footed ferret Mustela nigripes had gone extinct during a captive-breeding programme to save the host, and consequently this parasite has become an iconic species that exemplifies the need for parasite conservation. However, the claim that this louse is a separate species from the weasel louse Neotrichodectes minutus (Emerson, Reference Emerson1964) has never been confirmed. Thus parasite conservationists’ iconic species has never been described as a species.
In another erroneous example of co-extinction the louse Columbicola extinctus was believed to have gone extinct together with its only known host species, the passenger pigeon Ectopistes migratorius, until genetic analysis showed that the louse was conspecific with those parasitizing an extant species of pigeon (Clayton & Price, Reference Clayton and Price1999). Moreover, Campanulotes defectus, once also thought to be specific to the passenger pigeon, was shown to be a misidentification of an extant louse species (Price et al., Reference Price, Clayton and Adams2000) hosted by the common bronzewing Phaps chalcoptera.
These problems highlight the need to develop reliable taxonomical knowledge about threatened and extinct parasites. Although the co-extinction of host-specific dependent taxa (mutualists and parasites) and their hosts is known to be a feature of the ongoing wave of global extinctions (Stork & Lyal, Reference Stork and Lyal1993; Koh et al., Reference Koh, Dunn, Sodhi, Colwell, Proctor and Smith2004; Dunn et al., Reference Dunn, Harris, Colwell, Koh and Sodhi2009), the magnitude of this threat is difficult to assess. Published lists of threatened animal parasites only cover ixodid ticks (Durden & Keirans, Reference Durden and Keirans1996; Mihalca et al., Reference Mihalca, Gherman and Cozma2011), oestrid flies (Colwell et al., Reference Colwell, Otranto and Stevens2009), helminths of Brazilian vertebrates (Muñiz-Pereira et al., Reference Muñiz-Pereira, Vieira and Luque2009) and New Zealand mites and lice (Buckley et al., Reference Buckley, Palma, Johns, Gleeson, Heath, Hitchmough and Stringer2012). Our aim here is to provide a critical overview of the conservation status of parasitic lice.
Firstly, we document the louse species that are known or suspected to have gone extinct in conservation efforts to save the host species. Secondly, we define lice specific to Critically Endangered hosts as critically co-endangered parasites. We list critically co-endangered and co-extinct species on the basis of known host associations (Durden & Musser, Reference Durden and Musser1994; Price et al., Reference Price, Hellenthal, Palma, Johnson and Clayton2003; Mey, Reference Mey2004, Reference Mey2005, Reference Mey2010; Stephenson et al., Reference Stephenson, Gaskin, Griffiths, Jamieson, Baird, Palma and Imber2008) and whether the host is categorized as Extinct, Extinct in the Wild, or Critically Endangered on the IUCN Red List (IUCN, 2011). We do not list lice specific to Endangered or Vulnerable hosts because of the reduced threat of conservation-induced extinction in their case.
During the captive-breeding and release programme to save the California condor Gymnogyps californianus the louse Colpocephalum californici, which was specific to this host, went extinct, probably as a result of veterinary delousing routines (Dunn, Reference Dunn and Turvey2009).
Similarly, Rallicola (Aptericola) pilgrimi went extinct when its host, the little spotted kiwi Apteryx owenii, was translocated to predator-free islands to ensure its survival (Buckley et al., Reference Buckley, Palma, Johns, Gleeson, Heath, Hitchmough and Stringer2012).
We have no information about the fate of Rallicola (Rallicola) guami, a louse species known only from the Guam rail Gallirallus owstoni. Given that this host is extinct in the wild and only captive-bred stocks exist, it is likely that the parasite is extinct.
The status of Linognathus petasmatus is unknown, given the uncertainties about its host specificity. It may have been specific to the scimitar-horned oryx Oryx dammah and gone extinct as a result of conservation efforts to save this host in captivity or it may be specific to the addax Addax nasomaculatus and critically co-endangered.
The IUCN Red List (IUCN, 2011) includes only one Critically Endangered species of lice and the criteria for selecting this particular species are not known. We considerably expand this list by naming six co-extinct and 40 (possibly 41) critically co-endangered species of parasitic lice (Table 1), based on the IUCN Red List status of host species.
Table 1 Species of lice that exclusively parasitize(d) Critically Endangered or Extinct birds or mammals, with their host species and conservation status.
* Based on IUCN status of host species
There are several reasons why conservationists should care about threatened parasites. They not only constitute a large proportion of global biodiversity but also exert selective pressures to increase host diversity (Rózsa, Reference Rózsa1992), and therefore harbouring a unique parasitic fauna can increase the conservation value of the host (Pérez & Palma, Reference Pérez and Palma2001). Furthermore, parasites carry phylogenetic and population genetic information about the evolutionary past of their hosts (Whiteman & Parker, Reference Whiteman and Parker2005; Johnson et al., Reference Johnson, Kennedy and McCracken2006). On the other hand, the preservation of parasite species that pose considerable medical or veterinary threats would not be widely accepted.
Not all parasites are equally important. For example, the critically co-endangered gorilla louse Pthirus gorillae is of particular value because it is closely related to the human pubic louse Pthirus pubis (Reed et al., Reference Reed, Light, Allen and Kirchman2007) thus its loss would deprive us of a unique possibility to study the evolution and ecology of a human pathogen.
In several cases the IUCN categorization of birds or mammals as Critically Endangered appears to be an understatement. Hosts such as the Jamaica petrel Pterodroma caribbaea, New Caledonian rail Gallirallus lafresnayanus and Guadalupe storm-petrel Oceanodroma macrodactyla probably went globally extinct long ago. Consequently our list probably underestimates the number of co-extinct and critically co-endangered species. Further sources of uncertainty are the arbitrary nature of the species concept in the case of lice (Mey, Reference Mey2003) and the limited information available regarding host specificity (Moir et al., Reference Moir, Vesk, Brennan, Keith, Hughes and McCarthy2010, Reference Moir, Vesk, Brennan, Keith, McCarthy and Hughes2011).
Conservationists should consider preserving host-specific lice as part of their efforts to save birds or mammals ex situ. An obvious method is to establish in vitro cultures, which are relatively easy and cheap to maintain (Saxena & Agarwal, Reference Saxena and Agarwal1983). This would open the possibility for reintroduction of infested hosts. The potential costs and benefits of reintroducing infested vs non-infested animals are open to debate. As far as we are aware no practical work has been carried out to conserve any species of louse.
Biographical sketches
Lajos Rózsa's primary research interest is the interaction between animals (including humans) and their pathogens. Zoltán Vas is studying the interaction between birds and their parasites, with a particular emphasis on evolution, ecology and conservation.
