More than just invisible inhabitants: parasites are important but neglected components of the biodiversity

Carlos Frederico Duarte Rocha Helena Godoy Bergallo Emerson Brum Bittencourt About the authors

Biodiversity is crucial to humanity, and its value (such as equilibrating ecosystem function, ethics, aesthetics, and economic worth) has become increasingly more perceptible to humans, since it became clear that loss of biodiversity has had detrimental effects on many fundamental ecosystem services. In response to the loss of biodiversity resulting from human activities, a number of strategies have been developed to help preserve species. Checklists of endangered species are especially relevant to biodiversity conservation, since they identify entities that are at high risk of extinction. Based on them, appropriate measures to mitigate extinction risks can be taken. However, while highlighting a portion of the total biodiversity, in parti cular threatened species, these lists may underestimate the true number of species at risk. There are three principal reasons for this - (i) our limited knowledge of the actual number of species on the planet (Joppa et al. 2010Joppa L, Roberts DL, Pimm SL (2010) How many species of flowering plants are there? Proceedings of the Royal Society B 278: doi: 10.1098/rspb.2010.1004
https://doi.org/10.1098/rspb.2010.1004...
, Mora et al. 2011Mora C, Tittensor DP, Adl S, Simpson AGB (2011) Worm B How Many Species Are There on Earth and in the Ocean? PLOS Biology 9: doi: 10.1371/journal.pbio.1001127
https://doi.org/10.1371/journal.pbio.100...
), (ii) our limited knowledge of the real risk of extinction of most species, and (iii) some groups of species are systematically overlooked. Parasites are a prime example of the third case. Not only they tend to have cryptic habits, but also they are often on the receiving end of prejudices due to their habits. Nevertheless, parasites play an important role at individual, population and ecosystem levels (Wood & Johnson 2015Wood CL, Johnson PTJ (2015) A world without parasites: exploring the hidden ecology of infection. Frontiers in Ecology and the Environment 13: 425-434.), such as affecting the immunity of hosts and the dynamics of their populations, altering the composition of ecological communities, and modifying trophic interactions, including predation rates and nutrient cycling. These processes have complex effects, both direct and indirect, which may include co-extinctions, the long-term implications of which are not yet completely understood (Strona 2015Strona G (2015) Past, present and future of host-parasite co-extinctions. International Journal for Parasitology. International Journal for Parasitology: Parasites and Wildlife 4: 431-441. doi: 10.1016/j.ijppaw.2015.08.007
https://doi.org/10.1016/j.ijppaw.2015.08...
).

As the number of parasite species outnumbers non-parasites, they constitute a large portion of the total biodiversity (Windsor 1995Windsor DA (1995) Equal rights for parasites. Conservation Biology 9: 1-2., 1998Windsor DA (1998) Most of species on Earth are parasites. International Journal for Parasitology 28: 1939-1941.). However, the final number of parasite species can only be ascertained after all hosts have been accounted for (Windsor 1998Windsor DA (1998) Most of species on Earth are parasites. International Journal for Parasitology 28: 1939-1941.). Despite representing a considerable proportion of the species diversity of some groups of taxa (Dobson et al. 2008Dobson A, Lafferty KD, Kuris AM, Hechinger RF, Jetz W (2008) Homage to Linnaeus: How many parasites? How many hosts? Proceedings of the National Academy of Sciences 105: 11482-11489., Justine et al. 2012Justine JL, Beveridge I, Boxshall GA, Bray RA, Miller TL, Moravec F, Trilles JP, Whittington ID (2012) An annotated list of fish parasites (Isopoda, Copepoda, Monogenea, Digenea, Cestoda, Nematoda) collected from Snappers and Bream (Lutjanidae, Nemipteridae, Caesionidae) in New Caledonia confirms high parasite biodiversity on coral reef fish. Aquatic Biosystems 8: 22. doi: 10.1186/2046-9063-8-22
https://doi.org/10.1186/2046-9063-8-22...
), parasites have been largely ignored by conservationists (Dougherty et al. 2015Dougherty ER, Carlson CJ, Bueno VM, Burgio, KR, Cizauskas CA, Clements CF, Seidel DP, Harris NC (2015) Paradigms for parasite conservation. Conservation Biology. doi: 10.1111/cobi.12634
https://doi.org/10.1111/cobi.12634...
). Justine et al. (2012Justine JL, Beveridge I, Boxshall GA, Bray RA, Miller TL, Moravec F, Trilles JP, Whittington ID (2012) An annotated list of fish parasites (Isopoda, Copepoda, Monogenea, Digenea, Cestoda, Nematoda) collected from Snappers and Bream (Lutjanidae, Nemipteridae, Caesionidae) in New Caledonia confirms high parasite biodiversity on coral reef fish. Aquatic Biosystems 8: 22. doi: 10.1186/2046-9063-8-22
https://doi.org/10.1186/2046-9063-8-22...
), for example, estimated that the parasite species of coral reef fish were ten times more numerous than their hosts. Parasites are not passive inhabitants of other species, they are part of a dynamic system based on the interaction of selection pressures exerted by one species on another. The loss of one species resulting from the extinction of another, that is, a co-extinction (a term coined by Stork & Lyal 1993Stork NE, Lyal CHC (1993) Extinction or "co-extinction" rates? Nature 366: 307.), needs to be taken into consideration when making estimates of extinction rates (Koh et al. 2004Koh LP, Dunn RR, Sodhi NS, Colwell RK, Proctor HC, Smith V (2004) Species Coextinctions and the Biodiversity Crisis. Science 305: 1632-1634.). In most cases, lists of threatened species include the hosts, but fail to mention their parasites (their often invisible inhabitants). Many parasite species have coevolved with a specific host, and can only complete their life cycle in the presence of this host (Windsor 1995Windsor DA (1995) Equal rights for parasites. Conservation Biology 9: 1-2., McCoy et al. 2001Mccoy KD, Boulinier T, Tirard C, Michalakis Y (2001) Host specifiity of a generalist parasite: genetic evidence of sympatric host races in the seabird tick Ixodes uriae. Journal of Evolutionary Biology 14: 395-405., Bittencourt & Rocha 2003Bittencourt EB, Rocha CFD (2003) Host-ectoparasite Specificity in a Small Mammal Community in an Area of Atlantic Rain Forest (Ilha Grande, RJ), Southeastern Brazil. Memórias do Instituto Oswaldo Cruz 98: 793-798., Martins-Hata no et al. 2002Martins-Hatano F, Gettinger D, Bergallo HG (2002) Ecology and host specificity of laelapine mites (Acari: Laelapidae) of small mammals in an Atlantic Forest area of Brazil. Journal of Parasitology 88: 36-40., Krasnov et al. 2004Krasnov BR, Mouillot D, Shenbrot GI, Khokhlova IS, Poulin R (2004) Geographical variation in host specificity of fleas (Siphonaptera) parasitic on small mammals: the influence of phylogeny and local environmental conditions. Ecography 27: 787-797., Pedersena et al. 2005Pedersena AB, Altizerb S, Possc M, Cunninghamd AA, Nunn CL (2005) Patterns of host specificity and transmission among parasites of wild primates. International Journal of Parasitology 35: 647-657.). In these cases, if the host is a threatened species, the parasites that have co-evolved with it (or affiliated species, sensu Koh et al. 2004Koh LP, Dunn RR, Sodhi NS, Colwell RK, Proctor HC, Smith V (2004) Species Coextinctions and the Biodiversity Crisis. Science 305: 1632-1634.) will also be under the verge of extinction, which increases the overall challenges for species conservation (Dougherty et al. 2015Dougherty ER, Carlson CJ, Bueno VM, Burgio, KR, Cizauskas CA, Clements CF, Seidel DP, Harris NC (2015) Paradigms for parasite conservation. Conservation Biology. doi: 10.1111/cobi.12634
https://doi.org/10.1111/cobi.12634...
). While large numbers of parasite species appear to be threatened, only their host species are listed as such (Koh et al. 2004Koh LP, Dunn RR, Sodhi NS, Colwell RK, Proctor HC, Smith V (2004) Species Coextinctions and the Biodiversity Crisis. Science 305: 1632-1634.).

Taking mammals as an example, 5,506 species (out of a total of 47,761 worldwide) are listed in some category of threat in the IUCN Red Data List (IUCN 2015IUCN (2015) The IUCN Red List of Threatened Species. Cambridge, International Union for Conservation of Nature, available on line at: Cambridge, International Union for Conservation of Nature, available on line at: http://www.iucnredlist.org./details/9621/0 to Haematopinus oliveri and /details/9621/0 to Haematopinus oliveri and http://www.iucnredlist.org./details/21172/0 to Porcula salvania [Acessed: 30/04/2016]
http://www.iucnredlist.org./details/9621...
). Mammals host a wide spectrum of parasites, including micro- and macroparasites, and endo- or ectoparasites (Anderson 1990Anderson TJC (1990) Blood Parasites of Mammals from Papua New Guinea. Journal of Wildlife Disease 26: 291-294., Bittencourt & Rocha 2002Bittencourt EB, Rocha CFD (2002) Spatial Use of Rodents (Rodentia: Mammalia) Host Body Surface by Ectoparasites. Brazilian Journal of Biology 62: 419-425.). In most cases, a mammal will host a considerable diversity of parasites, occupying different compartments of its body, both externally (Bittencourt & Rocha 2002Bittencourt EB, Rocha CFD (2002) Spatial Use of Rodents (Rodentia: Mammalia) Host Body Surface by Ectoparasites. Brazilian Journal of Biology 62: 419-425.) and internally (Holmes 1973Holmes JC (1973) Site selection by parasitic helminths: interspecific interactions, site segregation, and their importance to the development of helminth communities. Canadian Journal of Zoology 51: 333-347.), and it is easy to imagine the vast diversity of parasite species - both known and as yet unsubscribed - that may be associated with the world's mammalian fauna. Considering all other types of organisms that may potentially host at least one type of parasite, an impressive portion of the world's total biodiversity may be found in or on host species (Koh et al. 2004Koh LP, Dunn RR, Sodhi NS, Colwell RK, Proctor HC, Smith V (2004) Species Coextinctions and the Biodiversity Crisis. Science 305: 1632-1634.). Despite this, parasite species tend to be overlooked in checklists of threatened fauna, even though virtually all species probably harbor parasites. The IUCN Red Data List includes only one parasite species, which is classified as critically endangered (CR): the louse Haematopinus oliveri Mishra & Singh, 1978 (Insecta: Phthiraptera: Haematopinidae), which is associated with the critically endangered pygmy hog Porcula salvania Hodgson, 1847 (Mammalia: Suidae), from Nepal and Bhutan, and which has a surviving population of only a few hundred individuals (IUCN 2015IUCN (2015) The IUCN Red List of Threatened Species. Cambridge, International Union for Conservation of Nature, available on line at: Cambridge, International Union for Conservation of Nature, available on line at: http://www.iucnredlist.org./details/9621/0 to Haematopinus oliveri and /details/9621/0 to Haematopinus oliveri and http://www.iucnredlist.org./details/21172/0 to Porcula salvania [Acessed: 30/04/2016]
http://www.iucnredlist.org./details/9621...
).

This provokes a number of questions. Why are parasites overlooked in the evaluation of species at risk, for example, and why are they so rarely included in lists of threatened species? The answers are numerous, and include the fact that (i) parasites are a less visible portion of the biodiversity since they are invariably very small; (ii) parasites are less well studied in comparison with their hosts, hindering reliable inferences on their conservation status (parasites have been studied traditionally by physicians and veterinarians, but only in the context of their target species - humans and domesticated animals) or their importance to the ecosystem; (iii) parasites are not charismatic and are associated with negative judgments because of their parasitic habits; (iv) parasites are often the agents of diseases that encourage their eradication rather than their protection (in this case, it is impor tant to consider the relatively recent concept of global health, which has been favored increasingly over the past decade, and promotes health and wellbeing through the prevention of risks and the mitigation of calamities), and finally (v) there may be an implicit assumption that the parasite will only be endangered if its host is endangered. Given all these considerations, it may appear as though ensuring the survival of the host will also ensure the survival of the parasite, at no extra cost. This is, however, not always true. Pollution, climate change, and shifts in the conditions for the transmission of parasites, as well as the development of resistance to other parasites or specific diseases, may require parasite-specific conservation measures. Overall, the primary reason for the exclusion of certain parasites from biodiversity lists may simply be man's narrow, stratified, and anthropocentric view of nature. As proposed by Dougherty et al. (2015Dougherty ER, Carlson CJ, Bueno VM, Burgio, KR, Cizauskas CA, Clements CF, Seidel DP, Harris NC (2015) Paradigms for parasite conservation. Conservation Biology. doi: 10.1111/cobi.12634
https://doi.org/10.1111/cobi.12634...
), the effective protection of parasite biodiversity will require a paradigm shift with regard to the perception and va luation of the role of these organisms in the ecosystem.

We conclude that a considerable portion of the total biodiversity - parasites - is widely ignored by conservationists, despite the fact that many species may be threatened by extinction due to their specific adaptations to their hosts, especially when these hosts are also endangered. The negligible numbers of parasites found on checklists of endangered species indicates that this group of organisms has been largely neglected by the researchers who compile these lists, whether on regional, national or global levels (IUCN). This is yet another example of how we may be losing a large number of species without even knowing that they exist, or understanding their extinction risk. The importance of parasites in nature emphasizes the need for a more mutualistic approach to the development of conservation strategies, especially when enumerating and evaluating the threatened fauna.

ACKNOWLEDGMENTS

This study was supported by research grants from the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq processes 472287/2012-5 and 302974/2015-6 to CFDR and 307781/2014-3 to HGB) and from Fundação Carlos Chagas Filho de Amparo à Pesquisa do Estado do Rio de Janeiro through "Cientistas do Nosso Estado" Program to C.F.D. Rocha (FAPERJ process E-26/102.765/2012 and E-26/202.920/2015) and to HGB (FAPERJ process E-26.103.016.2011 and E-26 201.267/2014).

LITERATURE CITED

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Publication Dates

  • Publication in this collection
    2016

History

  • Received
    04 Dec 2015
  • Reviewed
    07 Feb 2016
  • Accepted
    16 Mar 2016
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