Hostname: page-component-7c8c6479df-r7xzm Total loading time: 0 Render date: 2024-03-28T00:39:39.480Z Has data issue: false hasContentIssue false

Co-extinct and critically co-endangered species of parasitic lice, and conservation-induced extinction: should lice be reintroduced to their hosts?

Published online by Cambridge University Press:  22 August 2014

Lajos Rózsa*
Affiliation:
MTA-ELTE-MTM Ecology Research Group, Budapest, Pázmány Str. 1/c, H-1117Hungary
Zoltán Vas
Affiliation:
Hungarian Natural History Museum, Budapest, Hungary
*
(Corresponding author) E-mail lajos.rozsa@gmail.com
Rights & Permissions [Opens in a new window]

Abstract

The co-extinction of parasitic taxa and their host species is considered a common phenomenon in the current global extinction crisis. However, information about the conservation status of parasitic taxa is scarce. We present a global list of co-extinct and critically co-endangered parasitic lice (Phthiraptera), based on published data on their host-specificity and their hosts’ conservation status according to the IUCN Red List. We list six co-extinct and 40 (possibly 41) critically co-endangered species. Additionally, we recognize 2–4 species that went extinct as a result of conservation efforts to save their hosts. Conservationists should consider preserving host-specific lice as part of their efforts to save species.

Type
Short Communication
Copyright
Copyright © Fauna & Flora International 2014 

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.

References

Buckley, T.R., Palma, R.L., Johns, P.M., Gleeson, D.M., Heath, A.C.G., Hitchmough, R.A. & Stringer, I.A.N. (2012) The conservation status of small or less well known groups of New Zealand terrestrial invertebrates. New Zealand Entomologist, 35, 137143.CrossRefGoogle Scholar
Clayton, D.H. & Price, R.D. (1999) Taxonomy of New World Columbicola (Phthiraptera: Philopteridae) from the Columbiformes (Aves), with descriptions of five new species. Annals of the Entomological Society of America, 92, 675685.Google Scholar
Colwell, D.D., Otranto, D. & Stevens, J.R. (2009) Oestrid flies: eradication and extinction versus biodiversity. Trends in Parasitology, 25, 500504.Google Scholar
Dunn, R.R. (2009) Coextinction: anecdotes, models, and speculation. In Holocene Extinctions (ed. Turvey, S.T.), pp. 167180. Oxford University Press, Oxford, UK.CrossRefGoogle Scholar
Dunn, R.R., Harris, N.C., Colwell, R.K., Koh, L.P. & Sodhi, N.S. (2009) The sixth mass coextinction: are most endangered species parasites and mutualists? Proceedings of the Royal Society B: Biological Sciences, 276, 30373045.Google Scholar
Durden, L.A. & Keirans, J.E. (1996) Host–parasite coextinction and the plight of tick conservation. American Entomologist, 42, 8791.CrossRefGoogle Scholar
Durden, L.A. & Musser, G.G. (1994) The sucking lice (Insecta, Anoplura) of the world: a taxonomic checklist with records of mammalian hosts and geographical distributions. Bulletin of the American Museum of Natural History, 218, 190.Google Scholar
Emerson, K.C. (1964) Checklist of the Mallophaga of North America (north of Mexico). Part I. Suborder Ischnocera. Deseret Test Center, Dugway, USA.Google Scholar
Gompper, M.E. & Williams, E.S. (1998) Parasite conservation and the black-footed ferret recovery program. Conservation Biology, 12, 730732.Google Scholar
IUCN (2011) The IUCN Red List of Threatened Species v. 2011.2. Http://www.iucnredlist.org [accessed 10 January 2012].Google Scholar
Johnson, K.P., Kennedy, M. & McCracken, K.G. (2006) Reinterpreting the origins of flamingo lice: cospeciation or host switching? Biology Letters, 2, 275278.CrossRefGoogle ScholarPubMed
Koh, L.P., Dunn, R.D., Sodhi, N.S., Colwell, R.K., Proctor, H.C. & Smith, V.S. (2004) Species co-extinctions and the biodiversity crisis. Science, 305, 16321634.Google Scholar
Mey, E. (2003) On the development of animal louse systematics (Insecta, Phthiraptera) up to the present day. Rudolstädter Naturhistorische Schriften, 11, 115134.Google Scholar
Mey, E. (2004) Zur taxonomie, verbreitung und parasitophyletischer evidenz des Philopterus-komplexes (Insecta, Phthiraptera, Ischnocera). Ornithologischer Anzeiger, 43, 149203.Google Scholar
Mey, E. (2005) Psittacobrosus bechsteini: a new extinct chewing louse (Insecta, Phthiraptera, Amblycera) off the Cuban Macaw Ara tricolor (Psittaciiformes), with an annotated review of fossil and recently extinct animal lice. Anzeiger des Vereins Thüringer Ornithologen, 5, 201217.Google Scholar
Mey, E. (2010) The Pedicinus species (Insecta, Phthiraptera, Anoplura, Pedicinidae) on douc langurs (Pygathrix spp.). Vietnamese Journal of Primatology, 4, 5768.Google Scholar
Mihalca, A.D., Gherman, C.M. & Cozma, V. (2011) Coendangered hard-ticks: threatened or threatening? Parasites & Vectors, 4, 71.Google Scholar
Moir, M.L., Vesk, P.A., Brennan, K.E.C., Keith, D.A., Hughes, L. & McCarthy, M.A. (2010) Current constraints and future directions in estimating coextinction. Conservation Biology, 24, 682690.CrossRefGoogle ScholarPubMed
Moir, M.L., Vesk, P.A., Brennan, K.E.C., Keith, D.A., McCarthy, M.A. & Hughes, L. (2011) Identifying and managing threatened invertebrates through assessment of coextinction risk. Conservation Biology, 25, 787796.Google Scholar
Muñiz-Pereira, L.C., Vieira, F.M. & Luque, J.L. (2009) Checklist of helminth parasites of threatened vertebrate species from Brazil. Zootaxa, 2123, 145.CrossRefGoogle Scholar
Pérez, J.M. & Palma, R.L. (2001) A new species of Felicola (Phthiraptera: Trichodectidae) from the endangered Iberian lynx: another reason to ensure its survival. Biodiversity and Conservation, 10, 929937.CrossRefGoogle Scholar
Price, R.D., Clayton, D.H. & Adams, R.J. (2000) Pigeon lice down under: taxonomy of Australian Campanulotes (Phthiraptera: Philopteridae), with a description of C. durdeni n. sp. Journal of Parasitology, 86, 948950.Google ScholarPubMed
Price, R.D., Hellenthal, R.A., Palma, R.L., Johnson, K.P. & Clayton, D.H. (2003) The Chewing Lice: World Checklist and Biological Overview. Illinois Natural History Survey, Champaign, USA.Google Scholar
Reed, D.L., Light, J.E., Allen, J.M. & Kirchman, J.J. (2007) Pair of lice lost or parasites regained: the evolutionary history of anthropoid primate lice. BMC Biology, 5, 7.Google Scholar
Rózsa, L. (1992) Endangered parasite species. International Journal for Parasitology, 22, 265266.CrossRefGoogle ScholarPubMed
Saxena, A.K. & Agarwal, G.P. (1983) Review article: in vitro rearing of Mallophaga. Angewandte Parasitologie, 24, 178–86.Google Scholar
Stephenson, B.M., Gaskin, C.P., Griffiths, R., Jamieson, H., Baird, K.A., Palma, R.L. & Imber, M.J. (2008) The New Zealand storm-petrel (Pealeornis maoriana Mathews, 1932): first live capture and species assessment of an enigmatic seabird. Notornis, 55, 191206.Google Scholar
Stork, N.E. & Lyal, C.H.C. (1993) Extinction or ‘co-extinction’ rates? Nature, 366, 307.Google Scholar
Whiteman, N.K. & Parker, P.G. (2005) Using parasites to infer host population history: a new rationale for parasite conservation. Animal Conservation, 8, 175181.Google Scholar
Figure 0

Table 1 Species of lice that exclusively parasitize(d) Critically Endangered or Extinct birds or mammals, with their host species and conservation status.