Pooled samples and eDNA-based detection can facilitate the "clean trade" of aquatic animals.


Journal

Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288

Informations de publication

Date de publication:
24 06 2020
Historique:
received: 07 11 2019
accepted: 18 05 2020
entrez: 26 6 2020
pubmed: 26 6 2020
medline: 22 12 2020
Statut: epublish

Résumé

The regional and international trade of live animals facilitates the movement, spillover, and emergence of zoonotic and epizootic pathogens around the world. Detecting pathogens in trade is critical for preventing their continued movement and introduction, but screening a sufficient fraction to ensure rare infections are detected is simply infeasible for many taxa and settings because of the vast numbers of animals involved-hundreds of millions of live animals are imported into the U.S.A. alone every year. Batch processing pools of individual samples or using environmental DNA (eDNA)-the genetic material shed into an organism's environment-collected from whole consignments of animals may substantially reduce the time and cost associated with pathogen surveillance. Both approaches, however, lack a framework with which to determine sampling requirements and interpret results. Here I present formulae for pooled individual samples (e.g,. swabs) and eDNA samples collected from finite populations and discuss key assumptions and considerations for their use with a focus on detecting Batrachochytrium salamandrivorans, an emerging pathogen that threatens global salamander diversity. While empirical validation is key, these formulae illustrate the potential for eDNA-based detection in particular to reduce sample sizes and help bring clean trade into reach for a greater number of taxa, places, and contexts.

Identifiants

pubmed: 32581260
doi: 10.1038/s41598-020-66280-7
pii: 10.1038/s41598-020-66280-7
pmc: PMC7314758
doi:

Substances chimiques

DNA, Environmental 0

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

10280

Références

Daszak, P., Cunningham, A. A. & Hyatt, A. D. Emerging infectious diseases of wildlife—threats to biodiversity and human health. Sci 287, 443–449 (2000).
Cunningham, A., Daszak, P. & Rodriguez, J. Pathogen pollution: defining a parasitological threat to biodiversity conservation. J. Parasitol. 89, S78–S83 (2003).
Fèvre, E., Bronsvoort, B., Hamilton, K. & Cleaveland, S. Animal movements and the spread of infectious diseases. Trends Microbiol. 14, 125–131 (2006).
pubmed: 16460942 pmcid: 7119069
Rodgers, C., Mohan, C. & Peeler, E. The spread of pathogens through trade in aquatic animals and their products. Rev. Sci. Tech. - Off. Int. Epizoot 30, 241–256 (2011).
Travis, D., Watson, R. & Tauer, A. The spread of pathogens through trade in wildlife. Rev. Sci. Tech. - Off. Int. Epizoot 30, 219 (2011).
Smith, K. et al. Summarizing US wildlife trade with an eye toward assessing the risk of infectious disease introduction. EcoHealth 14, 29–39 (2017).
pubmed: 28176029 pmcid: 5357285
Can, Ö. E., D’Cruze, N. & Macdonald, D. W. Dealing in deadly pathogens taking stock of the legal trade in live wildlife and potential risks to human health. Glob. Ecol. Conserv 17, e00515 (2017).
Karesh, W. B., Cook, R. A., Bennett, E. L. & Newcomb, J. Wildlife trade and global disease emergence. Emerg. Infect. Dis. 11, 1000 (2005).
pubmed: 16022772 pmcid: 3371803
Smith, K. F. et al. Reducing the risks of the wildlife trade. Sci 324, 594–595 (2009).
Karesh, W. & Machalaba, C. (eds.). The unregulated and informal trade in wildlife: implications for biodiversity and health. (OIE (World Organisation for Animal Health), Paris, France, 2012).
Perrings, C., Levin, S. & Daszak, P. The economics of infectious disease, trade and pandemic risk. EcoHealth (2018).
Peeler, E. & Feist, S. Human intervention in freshwater ecosystems drives disease emergence. Freshw. Biol 56, 705–716 (2011).
Cunningham, A. A., Daszak, P. & Wood, J. L. N. One health, emerging infectious diseases and wildlife: two decades of progress. Phil. Trans. R. Soc. Lond. B Biol. Sci 372, 20160167 (2017).
Whittington, R. & Chong, R. Global trade in ornamental fish from an Australian perspective: the case for revised import risk analysis and management strategies. Prev. Vet. Med. 81, 92–116 (2007).
pubmed: 17485126
Costard, S. et al. African swine fever: how can global spread be prevented? Phil. Trans. R. Soc. Lond. B Biol. Sci 364, 2683–2696 (2009).
Martel, A. et al. Integral chain management of wildlife diseases. Conserv. Lett (2020).
Kuiken, T. et al. Pathogen surveillance in animals. Sci 309, 1680–1681 (2005).
Langwig, K. et al. Context-dependent conservation responses to emerging wildlife diseases. Front. Ecol. Evol 13, 195–202 (2015).
Voyles, J. et al. Moving beyond too little, too late: Managing emerging infectious diseases in wild populations requires international policy and partnerships. EcoHealth 12, 404–407 (2015).
pubmed: 25287279
Hood, Y., Sadler, J., Poldy, J., Starkey, C. & Robinson, A. Biosecurity system reforms and the development of a risk-based surveillance and pathway analysis system for ornamental fish imported into Australia. Prev Vet Med 167, 159–168 (2019).
pubmed: 30587454
Dorfman, R. The detection of defective members of large populations. Ann. Math. Stat 14, 436–440 (1943).
Venette, R. C., Moon, R. D. & Hutchison, W. D. Strategies and statistics of sampling for rare individuals. Annu. Rev. Entomol. 47, 143–174 (2002).
pubmed: 11729072
Sabino-Pinto, J. et al. Detectability vs. time and costs in pooled DNA extraction of cutaneous swabs: a study on the amphibian chytrid fungi. Amphib. https://doi.org/10.1163/15685381-20181011 (2018).
doi: 10.1163/15685381-20181011
Theobald, C. & Davie, A. Group testing, the pooled hypergeometric distribution, and estimating the number of defectives in small populations. Comm. Stat.-Theor. Methods 43, 3019–3026 (2014).
Bass, D., Stentiford, G., Littlewood, D. & Hartikainen, H. Diverse applications of environmental DNA methods in parasitology. Trends Parasitol. 31, 499–513 (2015).
pubmed: 26433253
Brunner, J. L. et al. Ranavirus infection dynamics and shedding in American bullfrogs: consequences for spread and detection in trade. Dis. Aquat. Organ 135, 135–150 (2019).
pubmed: 31392966
Hyman, O. & Collins, J. Evaluation of a filtration-based method for detecting Batrachochytrium dendrobatidis in natural bodies of water. Dis. Aquat. Organ 97, 185–195 (2012).
pubmed: 22422089
Hall, E., Crespi, E., Goldberg, C. & Brunner, J. Evaluating environmental DNA-based quantification of ranavirus infection in wood frog populations. Mol. Ecol. Resour. 16, 423–433 (2016).
pubmed: 26308150
Mosher, B. A. et al. Design- and model-based recommendations for detecting and quantifying an amphibian pathogen in environmental samples. Ecol. Evol 7, 10952–10962 (2017).
pubmed: 29299272 pmcid: 5743658
Sato, M. O. et al. Usefulness of environmental DNA for detecting Schistosoma mansoni occurrence sites in Madagascar. Int. J. Infect. Dis. 76, 130–136 (2018).
pubmed: 30201503
Egan, S. et al. Rapid molecular detection of invasive species in ballast and harbor water by integrating environmental DNA and light transmission spectroscopy. Environ. Sci. Technol. 49, 4113–4121 (2015).
pubmed: 25686279
Collins, R. A., Armstrong, K. F., Holyoake, A. J. & Keeling, S. Something in the water: biosecurity monitoring of ornamental fish imports using environmental DNA. Biol. Invasions 15, 1209–1215 (2013).
Kolby, J. et al. First evidence of amphibian chytrid fungus (Batrachochytrium dendrobatidis) and ranavirus in Hong Kong amphibian trade. PLoS One 9, e90750 (2014).
pubmed: 24599268 pmcid: 3944218
Trujillo-González, A., Edmunds, R. C., Becker, J. A. & Hutson, K. S. Parasite detection in the ornamental fish trade using environmental DNA. Sci. Rep. 9 (2019).
Schmidt, B. R., Kéry, M., Ursenbacher, S., Hyman, O. J. & Collins, J. P. Site occupancy models in the analysis of environmental DNA presence/absence surveys: a case study of an emerging amphibian pathogen. Methods Ecol. Evol 4, 646–653 (2013).
Scheele, B. C. et al. Amphibian fungal panzootic causes catastrophic and ongoing loss of biodiversity. Sci 363, 1459–1463 (2019).
Vredenburg, V. et al. Prevalence of Batrachochytrium dendrobatidis in Xenopus collected in Africa (1871–2000) and in California (2001–2010). PLoS One 8, e63791 (2013).
pubmed: 23691097 pmcid: 3655066
Mazzoni, R. et al. Emerging pathogen of wild amphibians in frogs (Rana catesbeiana) farmed for international trade. Emerg. Infect. Dis. 9, 995–998 (2003).
pubmed: 12967500 pmcid: 3020601
Schloegel, L. et al. Magnitude of the U.S. trade in amphibians and presence of Batrachochytrium dendrobatidis and ranavirus infection in imported North American bullfrogs (Rana catesbeiana). Biol. Conserv. 142, 1420–1426 (2009).
Van Rooij, P. et al. Clinically healthy amphibians in captive collections and at pet fairs: A reservoir of Batrachochytrium dendrobatidis. Amphib 32, 419–423 (2011).
Wombwell, E. et al. Detection of Batrachochytrium dendrobatidis in amphibians imported into the UK for the pet trade. EcoHealth 13, 456–466 (2016).
pubmed: 27317049
Fisher, M. & Garner, T. The relationship between the introduction of Batrachochytrium dendrobatidis, the international trade in amphibians and introduced amphibian species. Fungal Biol. Rev. 21, 2–9 (2007).
O’Hanlon, S. J. et al. Recent Asian origin of chytrid fungi causing global amphibian declines. Sci 360, 621–627 (2018).
Martel, A. et al. Batrachochytrium salamandrivorans sp. nov. causes lethal chytridiomycosis in amphibians. Proc. Nat. Acad. Sci 110, 15325–15329 (2013).
pubmed: 24003137
Spitzen-van der Sluijs, A. et al. Rapid enigmatic decline drives the fire salamander (Salamandra salamandra) to the edge of extinction in the Netherlands. Amphib 34, 233–239 (2013).
Martel, A. et al. Recent introduction of a chytrid fungus endangers Western Palearctic salamanders. Sci 346, 630–631 (2014).
Stegen, G. et al. Drivers of salamander extirpation mediated by Batrachochytrium salamandrivorans. Nat 544, 353–356 (2017).
Laking, A., Ngo, H., Pasmans, F., Martel, A. & Nguyen, T. Batrachochytrium salamandrivorans is the predominant chytrid fungus in Vietnamese salamanders. Sci. Rep 7, 44443 (2017).
pubmed: 28287614 pmcid: 5347381
Nguyen, T. T., Nguyen, T. V., Ziegler, T., Pasmans, F. & Martel, A. Trade in wild anurans vectors the urodelan pathogen Batrachochytrium salamandrivorans into. Europe. Amphib 38, 554–556 (2017).
Yuan, Z. et al. Widespread occurrence of an emerging fungal pathogen in heavily traded Chinese urodelan species. Conserv. Lett 11, e12436 (2018).
Baláz, V. et al. First survey of pathogenic fungus Batrachochytrium salamandrivorans in wild and captive amphibians in the Czech Republic. Salamandra 54, 87–91 (2018).
Gimeno, A., Meikl, M., Pitt, A., Winkler, M. & Berninger, U.-G. Testing of Fire Salamanders around Salzburg for Batrachochytrium salamandrivorans within a school project. eco.mont 7, 72–76 (2015).
Parrott, J. et al. Survey of pathogenic chytrid fungi (Batrachochytrium dendrobatidis and B. salamandrivorans) in salamanders from three mountain ranges in Europe and the Americas. EcoHealth 14, 296–302 (2017).
pubmed: 27709310
Cunningham, A. A. et al. Apparent absence of Batrachochytrium salamandrivorans in wild urodeles in the United Kingdom. Sci. Rep. 9 (2019).
Sabino-Pinto, J. et al. First detection of the emerging fungal pathogen Batrachochytrium salamandrivorans in Germany. Amphib 36, 411–416 (2015).
Fitzpatrick, L. D., Pasmans, F., Martel, A. & Cunningham, A. A. Epidemiological tracing of Batrachochytrium salamandrivorans identifies widespread infection and associated mortalities in private amphibian collections. Sci. Rep 8, 443 (2018).
Sabino-Pinto, J., Veith, M., Vences, M. & Steinfartz, S. Asymptomatic infection of the fungal pathogen Batrachochytrium salamandrivorans in captivity. Sci. Rep. 8, https://doi.org/10.1038/s41598-018-30240-z (2018).
Govindarajulu, P., Matthews, E. & Ovaska, K. Swabbing for Batrachochytrium salamandrivorans on wild rough-skinned newts (Taricha granulosa) and pettraded amphibians on southern Vancouver Island, British Columbia, Canada. Herpetol. Rev 48, 564–568 (2017).
Klocke, B. et al. Batrachochytrium salamandrivorans not detected in U.S. survey of pet salamanders. Sci. Rep 7, 13132 (2017).
pubmed: 29030586 pmcid: 5640657
Harris, R. et al. A North American strategic plan to control invasions of the lethal salamander pathogen Batrachochytrium salamandrivorans. Tech. Rep., North American Bsal Task Force (2019).
Grant, E. H. C. et al. Salamander chytrid fungus (Batrachochytrium salamandrivorans) in the United States—developing research, monitoring, and management strategies. Tech. Rep., U.S. Geological Survey (2016).
Richgels, K., Russell, R., Adams, M., White, C. & Grant, E. Spatial variation in risk and consequence of Batrachochytrium salamandrivorans introduction in the USA. R. Soc. Open Sci 3, 150616 (2016).
pubmed: 26998331 pmcid: 4785982
Yap, T., Nguyen, N., Serr, M., Shepack, A. & Vredenburg, V. Batrachochytrium salamandrivorans and the risk of a second amphibian pandemic. EcoHealth 14, 851–864 (2017).
pubmed: 29147975
U.S. Fish and Wildlife Service. Listing salamanders as injurious due to risk of salamander chytrid fungus (January 12, 2016). https://www.fws.gov/injuriouswildlife/salamanders.html (2016).
Canada Border Services Agency. Environment and Climate Change Canada (ECCC)’s import restrictions on salamanders. Customs Notice 17-17. https://www.cbsa-asfc.gc.ca/publications/cn-ad/cn17-17-eng.html (2018).
Hance, J. Will trade bans stop a deadly salamander plague from invading the US? Mongabay https://news.mongabay.com/2018/10/can–trade–bans–stop–a–deadly–salamander–plague–from–invading–the–us/ (2018).
More, S. et al. Risk of survival, establishment and spread of Batrachochytrium salamandrivorans (Bsal) in the EU. EFSA J 16, 2581 (2018).
Watts, A., Olson, D., Harris, R. & Mandica, M. The deadly amphibian Bsal disease: How science-management partnerships are forestalling amphibian biodiversity losses. Tech. Rep., US Department of Agriculture, Forest Service, Pacific Northwest Research Station., Portland, OR, USA (2019).
Blooi, M. et al. Duplex real-time PCR for rapid simultaneous detection of Batrachochytrium dendrobatidis and Batrachochytrium salamandrivorans in amphibian samples. J. Clin. Microbiol. 51, 4173–4177 (2013).
pubmed: 24108616 pmcid: 3838082
European Union. Commission Implementing Decision (EU) 2018/320 of 28 February 2018 on certain animal health protection measures for intra-union trade in salamanders and the introduction into the union of such animals in relation to the fungus Batrachochytrium salamandrivorans. Off. J. Eur. Union 61, 18–33 (2018).
Altmann, M. C. G. & Kolby, J. E. Trends in US imports of amphibians in light of the potential spread of chytrid fungus, (Bd), and implications for conservation. J. Int. Wildl. Law Pol 20, 226–252 (2018).
Peel, A., Hartley, M. & Cunningham, A. Qualitative risk analysis of introducing Batrachochytrium dendrobatidis to the UK through the importation of live amphibians. Dis. Aquat. Organ 98, 95–112 (2012).
pubmed: 22436458
Trujillo-González, A., Becker, J., Huerlimann, R., Saunders, R. & Hutson, K. Can environmental dna be used for aquatic biosecurity in the aquarium fish trade. Biol. Invasions 22, 1011–1025 (2020).
Laurin, E. et al. To pool or not to pool? guidelines for pooling samples for use in surveillance testing of infectious diseases in aquatic animals. J. Fish Dis 42, 1471–1491 (2019).
pubmed: 31637760
Johnson, S. et al. The impact of pooling samples on surveillance sensitivity for the megalocytivirus Infectious spleen and kidney necrosis virus. Transbound Emerg. Dis 00, 1–11 (2019).
Rimmer, A. et al. Detection of dwarf gourami iridovirus (Infectious spleen and kidney necrosis virus) in populations of ornamental fish prior to and after importation into Australia, with the first evidence of infection in domestically farmed platy (Xiphophorus maculatus). Prev. Vet. Med. 122, 181–194 (2015).
pubmed: 26452601
Shin, J., Bataille, A., Kosch, T. & Waldman, B. Swabbing often fails to detect amphibian chytridiomycosis under conditions of low infection load. PLoS One 9, e111091 (2014).
pubmed: 25333363 pmcid: 4205094
Goldberg, C. S. et al. Critical considerations for the application of environmental DNA methods to detect aquatic species. Methods Ecol. Evol 7, 1299–1307 (2016).
Goldberg, C., Strickler, K. & Fremier, A. Degradation and dispersion limit environmental DNA detection of rare amphibians in wetlands: Increasing efficacy of sampling designs. Sci. Total. Environ. 633, 695–703 (2018).
pubmed: 29602110
Hyatt, A. et al. Diagnostic assays and sampling protocols for the detection of Batrachochytrium dendrobatidis. Dis Aquat Organ 73, 175–192 (2007).
pubmed: 17330737
Cameron, A. R. & Baldock, F. C. A new probability formula for surveys to substantiate freedom from disease. Prev. Vet. Med. 34, 1–17 (1998).
pubmed: 9541947
Teunis, P. & Havelaar, A. The beta Poisson dose-response model is not a single-hit model. Risk Analysis 20, 513–520 (2000).
pubmed: 11051074
Stokdyk, J. P., Firnstahl, A., Spencer, S. K., Burch, T. R. & Borchardt, M. A. Determining the 95% limit of detection for waterborne pathogen analyses from primary concentration to qPCR. Water Res 96, 105–113 (2016).
pubmed: 27023926
Johnson, A. & Brunner, J. Persistence of an amphibian ranavirus in aquatic communities. Dis. Aquat. Organ 111, 129–138 (2014).
pubmed: 25266900
Klymus, K. E., Richter, C. A., Chapman, D. C. & Paukert, C. Quantification of eDNA shedding rates from invasive bighead carp Hypophthalmichthys nobilis and silver carp Hypophthalmichthys molitrix. Biol. Conserv. 183, 77–84 (2015).
Strickler, K. M., Fremier, A. K. & Goldberg, C. S. Quantifying effects of UV-B, temperature, and pH on eDNA degradation in aquatic microcosms. Biol. Conserv. 183, 85–92 (2015).
Lucas, A., Scholz, I., Boehme, R., Jasson, S. & Maechler, M. gmp: Multiple Precision Arithmetic R package version 0.5–13.5 (2019).

Auteurs

Jesse L Brunner (JL)

Washington State University, School of Biological Sciences, Pullman, WA, 99164, USA. jesse.brunner@wsu.edu.

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