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Paradigms for parasite conservation

dc.contributor.authorDougherty, Eric R.
dc.contributor.authorCarlson, Colin J.
dc.contributor.authorBueno, Veronica M.
dc.contributor.authorBurgio, Kevin R.
dc.contributor.authorCizauskas, Carrie A.
dc.contributor.authorClements, Christopher F.
dc.contributor.authorSeidel, Dana P.
dc.contributor.authorHarris, Nyeema C.
dc.date.accessioned2016-09-17T23:54:08Z
dc.date.available2017-11-01T15:31:29Zen
dc.date.issued2016-08
dc.identifier.citationDougherty, Eric R.; Carlson, Colin J.; Bueno, Veronica M.; Burgio, Kevin R.; Cizauskas, Carrie A.; Clements, Christopher F.; Seidel, Dana P.; Harris, Nyeema C. (2016). "Paradigms for parasite conservation." Conservation Biology 30(4): 724-733.
dc.identifier.issn0888-8892
dc.identifier.issn1523-1739
dc.identifier.urihttps://hdl.handle.net/2027.42/133571
dc.description.abstractParasitic species, which depend directly on host species for their survival, represent a major regulatory force in ecosystems and a significant component of Earth’s biodiversity. Yet the negative impacts of parasites observed at the host level have motivated a conservation paradigm of eradication, moving us farther from attainment of taxonomically unbiased conservation goals. Despite a growing body of literature highlighting the importance of parasite‐inclusive conservation, most parasite species remain understudied, underfunded, and underappreciated. We argue the protection of parasitic biodiversity requires a paradigm shift in the perception and valuation of their role as consumer species, similar to that of apex predators in the mid‐20th century. Beyond recognizing parasites as vital trophic regulators, existing tools available to conservation practitioners should explicitly account for the unique threats facing dependent species. We built upon concepts from epidemiology and economics (e.g., host‐density threshold and cost‐benefit analysis) to devise novel metrics of margin of error and minimum investment for parasite conservation. We define margin of error as the risk of accidental host extinction from misestimating equilibrium population sizes and predicted oscillations, while minimum investment represents the cost associated with conserving the additional hosts required to maintain viable parasite populations. This framework will aid in the identification of readily conserved parasites that present minimal health risks. To establish parasite conservation, we propose an extension of population viability analysis for host–parasite assemblages to assess extinction risk. In the direst cases, ex situ breeding programs for parasites should be evaluated to maximize success without undermining host protection. Though parasitic species pose a considerable conservation challenge, adaptations to conservation tools will help protect parasite biodiversity in the face of an uncertain environmental future.ResumenLas especies parásitas, aquellas que dependen directamente de las especies hospederas para sobrevivir, representan una gran fuerza regulatoria dentro de los ecosistemas y un componente significativo de la biodiversidad de la Tierra. Aún así, los impactos negativos de los parásitos que se han observado a nivel del hospedero han motivado un paradigma de conservación enfocado en la erradicación, lo que nos aleja cada vez más de alcanzar objetivos de conservación sin sesgos taxonómicos. A pesar de la creciente bibliografía que resalta la importancia de la conservación incluyente de los parásitos, la mayoría de este tipo de especies sigue siendo poco estudiada, mal financiada y poco valorada. Argumentamos que la protección de la diversidad parasitaria requiere de un cambio en el paradigma de la percepción y valoración de su papel como especies consumidoras, similar al de los depredadores primarios a mediados del siglo XX. Más allá de reconocer a los parásitos como reguladores tróficos vitales, las herramientas existentes disponibles para quienes practican la conservación deberían reconocer explícitamente las amenazas únicas que enfrentan las especies dependientes. Partimos de conceptos de epidemiología y economía (p. ej.: umbral de densidad de hospedero y análisis de costo‐beneficio) para diseñar medidas novedosas del margen de error y la inversión mínima para la conservación de parásitos. Definimos el margen de error como el riesgo de extinción accidental del hospedero a partir de una mala estimación del tamaño de poblaciones en equilibrio y de los pronósticos de oscilación, mientras que la inversión mínima representa el costo asociado a la conservación de los hospederos adicionales requeridos para mantener viables a las poblaciones de parásitos. Este marco de trabajo ayudará en la identificación de los parásitos conservados inmediatamente que presentan un riesgo sanitario mínimo. Para establecer la conservación de parásitos, proponemos una extensión del análisis de viabilidad poblacional para los conjuntos de hospedero‐parásito y así evaluar el riesgo de extinción. En los casos más urgentes, se deberían evaluar programas de crianza ex situ para maximizar el éxito sin debilitar la protección al hospedero. Aunque las especies parásitas presentan un reto considerable para la conservación, las adaptaciones de las herramientas de conservación ayudarán a proteger la diversidad de parásitos de frente a un futuro ambiental incierto.
dc.publisherSpringer
dc.publisherWiley Periodicals, Inc.
dc.subject.otherparasitología
dc.subject.otherredes alimentarias
dc.subject.othervaloración económica
dc.subject.otherdisease ecology
dc.subject.othereconomic valuation
dc.subject.otherex situ conservation
dc.subject.otherfood webs
dc.subject.otherparasitology
dc.subject.otherpopulation viability analysis
dc.subject.otheranálisis de viabilidad poblacional
dc.subject.otherconservación ex situ
dc.subject.otherecología de las enfermedades
dc.titleParadigms for parasite conservation
dc.typeArticleen_US
dc.rights.robotsIndexNoFollow
dc.subject.hlbsecondlevelEcology and Evolutionary Biology
dc.subject.hlbtoplevelScience
dc.description.peerreviewedPeer Reviewed
dc.description.bitstreamurlhttp://deepblue.lib.umich.edu/bitstream/2027.42/133571/1/cobi12634.pdf
dc.description.bitstreamurlhttp://deepblue.lib.umich.edu/bitstream/2027.42/133571/2/cobi12634_am.pdf
dc.identifier.doi10.1111/cobi.12634
dc.identifier.sourceConservation Biology
dc.identifier.citedreferenceLefevre T, Lebarbenchon C, Gauthier‐Clerc M, Misse D, Poulin R, Thomas F. 2009. The ecological significance of manipulative parasites. Trends in Ecology & Evolution 24: 41 – 48.
dc.identifier.citedreferenceStringer AP, Linklater W. 2014. Everything in moderation: principles of parasite control for wildlife conservation. BioScience 64: 932 – 937.
dc.identifier.citedreferenceSoulé M, Gilpin M, Conway W, Foose T. 1986. The millenium ark: How long a voyage, how many staterooms, how many passengers? Zoo Biology 5: 101 – 113.
dc.identifier.citedreferenceKamath PL, Turner WC, Kusters M, Getz WM. 2014. Parasite‐mediated selection drives an immunogenetic trade‐off in plains zebras ( Equus Quagga ). Proceedings of the Royal Society of London B: Biological Sciences 281 ( 1783 ): DOI:  10.1098/rspb.2014.0077.
dc.identifier.citedreferenceKellert SR, Black M, Rush CR, Bath AJ. 1996. Human culture and large carnivore conservation in north america. Conservation Biology 10: 977 – 990.
dc.identifier.citedreferenceKoh LP, Dunn RR, Sodhi NS, Colwell RK, Proctor HC, Smith VS. 2004. Species coextinctions and the biodiversity crisis. Science 305: 1632 – 1634.
dc.identifier.citedreferenceKoskella B, Lively CM. 2007. Advice of the rose: experimental coevolution of a trematode parasite and its snail host. Evolution 61: 152 – 159.
dc.identifier.citedreferenceKuris AM. 2012. The global burden of human parasites: Who and where are they? How are they transmitted? The Journal of Parasitology 98: 1056 – 1064.
dc.identifier.citedreferenceKuris AM, et al. 2008. Ecosystem energetic implications of parasite and free‐living biomass in three estuaries. Nature 454: 515 – 518.
dc.identifier.citedreferenceLafferty KD. 2014. Biodiversity loss and infectious diseases. Pages 73 – 89 in Verdade LM, Lyra‐Jorge MC, Piña CI, editors. Applied ecology and human dimensions in biological conservation. Springer, New York.
dc.identifier.citedreferenceLafferty KD, et al. 2008. Parasites in food webs: the ultimate missing links. Ecology Letters 11: 533 – 546.
dc.identifier.citedreferenceLafferty KD, Dobson AP, Kuris AM. 2006. Parasites dominate food web links. Proceedings of the National Academy of Sciences 103: 11211 – 11216.
dc.identifier.citedreferenceLafferty KD, Kuris A. 2014. Ecological consequences of host manipulation by parasites. Integrative and Comparative Biology 54: E117 – E117.
dc.identifier.citedreferenceStork NE, Lyal CH. 1993. Extinction or ‘co‐extinction’ rates? Nature 366: 307.
dc.identifier.citedreferenceMariner JC, House JA, Mebus CA, Sollod AE, Chibeu D, Jones BA, Roeder PL, Admassu B, van ’t Klooster GG. 2012. Rinderpest eradication: appropriate technology and social innovations. Science 337: 1309 – 1312.
dc.identifier.citedreferenceMech LD, Boitani L. 2010. Wolves: behavior, ecology, and conservation: behavior, ecology, and conservation. University of Chicago Press, Chicago.
dc.identifier.citedreferenceMessmer TA, Brunson MW, Reiter D, Hewitt DG. 1999. United States public attitudes regarding predators and their management to enhance avian recruitment. Wildlife Society Bulletin 27: 75 – 85.
dc.identifier.citedreferenceMougi A, Kondoh M. 2012. Diversity of interaction types and ecological community stability. Science 337: 349 – 351.
dc.identifier.citedreferenceMyers N, Mittermeier RA, Mittermeier CG, Da Fonseca GA, Kent J. 2000. Biodiversity hotspots for conservation priorities. Nature 403: 853 – 858.
dc.identifier.citedreferenceNunn CL, Altizer SM. 2005. The global mammal parasite database: an online resource for infectious disease records in wild primates. Evolutionary Anthropology: Issues, News, and Reviews 14: 1 – 2.
dc.identifier.citedreferencePérez JM, Sánchez I, Palma RL. 2013. The dilemma of conserving parasites: the case of Felicola (Lorisicola) isidoroi ( Phthiraptera: Trichodectidae) and its host, the endangered Iberian lynx ( Lynx pardinus ). Insect Conservation and Diversity 6: 680 – 686.
dc.identifier.citedreferencePizzi R. 2009. Veterinarians and taxonomic chauvinism: the dilemma of parasite conservation. Journal of Exotic Pet Medicine 18: 279 – 282.
dc.identifier.citedreferencePoulin R. 2010. Parasite manipulation of host behavior: an update and frequently asked questions. Advances in the Study of Behavior 41: 151 – 186.
dc.identifier.citedreferenceRay J, Redford KH, Steneck R, Berger J. 2013. Large carnivores and the conservation of biodiversity. Island Press, Washington, D.C.
dc.identifier.citedreferenceRohlf DJ. 1991. Six biological reasons why the endangered species act doesn’t work—and what to do about it. Conservation Biology 5: 273 – 282.
dc.identifier.citedreferenceRózsa L, Vas Z. 2015. Co‐extinct and critically co‐endangered species of parasitic lice, and conservation‐induced extinction: Should lice be reintroduced to their hosts? Oryx 49: 107 – 110.
dc.identifier.citedreferenceRudolf V, Lafferty KD. 2011. Stage structure alters how complexity affects stability of ecological networks. Ecology Letters 14: 75 – 79.
dc.identifier.citedreferenceSato T, Watanabe K, Kanaiwa M, Niizuma Y, Harada Y, Lafferty KD. 2011. Nematomorph parasites drive energy flow through a riparian ecosystem. Ecology 92: 201 – 207.
dc.identifier.citedreferenceSergio F, Caro T, Brown D, Clucas B, Hunter J, Ketchum J, McHugh K, Hiraldo F. 2008. Top predators as conservation tools: ecological rationale, assumptions, and efficacy. Annual Review of Ecology, Evolution, and Systematics 39: 1 – 19.
dc.identifier.citedreferenceSilverman AL, Qu LH, Blow J, Zitron IM, Gordon SC, Walker ED. 2001. Assessment of hepatitis B virus DNA and hepatitis C virus RNA in the common bedbug ( Cimex lectularius L.) and kissing bug ( Rodnius prolixus ). The American Journal of Gastroenterology 96: 2194 – 2198.
dc.identifier.citedreferenceSmith KF, Sax DF, Gaines SD, Guernier V, Guégan J. 2007. Globalization of human infectious disease. Ecology 88: 1903 – 1910.
dc.identifier.citedreferenceStrona G, Lafferty KD. 2012. FishPEST: an innovative software suite for fish parasitologists. Trends in Parasitology 28: 123.
dc.identifier.citedreferenceSummers RW, Elliott DE, Urban Jr JF, Thompson R, Weinstock JV. 2005. Trichuris suis therapy in Crohn’s disease. Gut 54: 87 – 90.
dc.identifier.citedreferenceWhite PC, Gregory KW, Lindley PJ, Richards G. 1997. Economic values of threatened mammals in britain: a case study of the otter Lutra lutra and the water vole Arvicola terrestris. Biological Conservation 82: 345 – 354.
dc.identifier.citedreferenceYazdanbakhsh M, Kremsner PG, van Ree R. 2002. Allergy, parasites, and the hygiene hypothesis. Science 296: 490 – 494.
dc.identifier.citedreferenceZhang J, Daszak P, Huang H, Yang G, Kilpatrick AM, Zhang S. 2008. Parasite threat to panda conservation. Ecohealth 5: 6 – 9.
dc.identifier.citedreferenceAiello C, Nussear K, Walde A, Esque T, Emblidge P, Sah P, Bansal S, Hudson P. 2014. Disease dynamics during wildlife translocations: disruptions to the host population and potential consequences for transmission in desert tortoise contact networks. Animal Conservation 17 ( S1 ): 27 – 39.
dc.identifier.citedreferenceAlmberg ES, Cross PC, Dobson AP, Smith DW, Hudson PJ. 2012. Parasite invasion following host reintroduction: a case study of Yellowstone’s wolves. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 367 ( 1604 ) DOI:  10.1098/rstb.2011.0369.
dc.identifier.citedreferenceAnderson RM, May RM. 1978. Regulation and stability of host‐parasite population interactions: I. Regulatory processes. The Journal of Animal Ecology 47: 219 – 247.
dc.identifier.citedreferenceBarrett S. 2004. Eradication versus control: the economics of global infectious disease policies. Bulletin of the World Health Organization 82: 683 – 688.
dc.identifier.citedreferenceBerger J, Wehausen JD. 1991. Consequences of a mammalian predator‐prey disequilibrium in the great basin desert. Conservation Biology 5: 244 – 248.
dc.identifier.citedreferenceBergstrom R, Harrington LM, Ramsey D. 2013. Balancing communities, economies, and the environment in the greater Yellowstone ecosystem. Journal of Rural and Community Development 8: 228 – 241.
dc.identifier.citedreferenceBoyce MS. 1992. Population viability analysis. Annual Review of Ecology and Systematics 23: 481 – 506.
dc.identifier.citedreferenceCaira J, Jensen K, Barbeau E. 2012. Global cestode database. Available from www.tapewormdb.uconn.edu (accessed July 2015).
dc.identifier.citedreferenceCallahan K, Bolton B, Hopkins DR, Ruiz‐Tiben E, Withers PC, Meagley K. 2013. Contributions of the guinea worm disease eradication campaign toward achievement of the millennium development goals. PLoS Neglected Tropical Diseases 7: e2160 DOI: 10.1371/journal.pntd.0002160.
dc.identifier.citedreferenceClayton DH, Price RD. 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: 675 – 685.
dc.identifier.citedreferenceCorn JL, Nettles VF. 2001. Health protocol for translocation of free‐ranging elk. Journal of Wildlife Diseases 37: 413 – 426.
dc.identifier.citedreferenceCostello MJ, May RM, Stork NE. 2013. Can we name Earth’s species before they go extinct? Science 339: 413 – 416.
dc.identifier.citedreferenceCunningham AA. 1996. Disease risks of wildlife translocations. Conservation Biology 10: 349 – 353.
dc.identifier.citedreferenceDennis B, Munholland PL, Scott JM. 1991. Estimation of growth and extinction parameters for endangered species. Ecological Monographs 61: 115 – 143.
dc.identifier.citedreferenceDeVault TL, Rhodes Jr OE, Shivik JA. 2003. Scavenging by vertebrates: behavioral, ecological, and evolutionary perspectives on an important energy transfer pathway in terrestrial ecosystems. Oikos 102: 225 – 234.
dc.identifier.citedreferenceDunn RR, Harris NC, Colwell RK, Koh LP, Sodhi NS. 2009. The sixth mass coextinction: Are most endangered species parasites and mutualists? Proceedings of the Royal Society of London B: Biological Sciences 276 ( 1670 ) DOI:  10.1098/rspb.2009.0413.
dc.identifier.citedreferenceFenton A, Perkins SE. 2010. Applying predator‐prey theory to modelling immune‐mediated, within‐host interspecific parasite interactions. Parasitology 137: 1027 – 1038.
dc.identifier.citedreferenceGerber LR, McCallum H, Lafferty KD, Sabo JL, Dobson A. 2005. Exposing extinction risk analysis to pathogens: Is disease just another form of density dependence? Ecological Applications 15: 1402 – 1414.
dc.identifier.citedreferenceGibson D, Bray R, Harris E. 2005. Host‐parasite database of the Natural History Museum, London. Available from http://www.nhm.ac.uk/host‐parasites/database (accessed July 2015).
dc.identifier.citedreferenceGómez A, Nichols E. 2013. Neglected wild life: parasitic biodiversity as a conservation target. International Journal for Parasitology: Parasites and Wildlife 2: 222 – 227.
dc.identifier.citedreferenceGompper ME, Williams ES. 1998. Parasite conservation and the black‐footed ferret recovery program. Conservation Biology 12: 730 – 732.
dc.identifier.citedreferenceHairston NG, Smith FE, Slobodkin LB. 1960. Community structure, population control, and competition. The American Naturalist 94: 421 – 425.
dc.identifier.citedreferenceHatcher MJ, Dick JT, Dunn AM. 2012. Diverse effects of parasites in ecosystems: linking interdependent processes. Frontiers in Ecology and the Environment 10: 186 – 194.
dc.identifier.citedreferenceIzdebska JN. 2006. Skin mites (acari: Demodecidae, psoroptidae, and sarcoptidae) of the european bison, bison bonasus. Biological Letters 43 ( 2 ): 169 – 174.
dc.identifier.citedreferenceJohnson PT, Preston DL, Hoverman JT, LaFonte BE. 2013. Host and parasite diversity jointly control disease risk in complex communities. Proceedings of the National Academy of Sciences 110: 16916 – 16921.
dc.identifier.citedreferenceJones L. 2015. What would happen if all the parasites disappeared? BBC, London. Available from http://www.bbc.com/earth/story/20150127‐what‐if‐all‐the‐pests‐vanished (accessed July 2015).
dc.identifier.citedreferenceJørgensen D. 2014. Conservation implications of parasite co‐reintroduction. Conservation Biology 29: 602 – 604.
dc.owningcollnameInterdisciplinary and Peer-Reviewed


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