Managing the risk of wildlife disease introduction: pathway-level biosecurity for preventing the introduction of alien ranaviruses

Summary Alien species are key vectors for the spread of globally emerging diseases, and these emerging diseases have proven to be devastating for amphibian populations world-wide. Border and post-border biosecurity activities are pivotal for preventing the introduction of new diseases, but their effectiveness has seldom been assessed. We developed and populated a model to describe transport pathways into Australia, and the biosecurity activities implemented to manage these pathways. We evaluated the capacity of Australian border and post-border biosecurity activities, frequently considered one of the best quarantine inspection services in the world, to prevent the introduction of alien ranaviruses via the unintentional transport of alien amphibians into six Australian States. High transport pressures, measured by the number of international airline passengers and ships arriving in each State, resulted in increasing total numbers of alien stowaway amphibians. Post-border detection of alien amphibians was variable across States and increased with the full-time equivalent employees devoted to post-border biosecurity in each State. The baseline probabilities of introduction, without biosecurity activities, for at least one infected amphibian into any State were very low (≤0·07 in all cases), January 2004–December 2012. The implementation of biosecurity activities reduced these introduction probabilities further, with reductions of up to 50% for some States. Synthesis and applications. We have demonstrated the efficacy of biosecurity activities in reducing the introduction risk of new diseases being transported unintentionally alongside alien amphibians. Critically, we found that not all alien amphibians had to be detected to reduce risks appreciably. We advocate the widespread adoption of border and post-border biosecurity activities to manage the risks posed by alien amphibians (and other stowaway species) as vectors of emergent diseases. We support the robust design of biosecurity activities by providing a framework to evaluate the likely outcomes of case-specific biosecurity arrangements.

[1]  R. Weir,et al.  Pathology of a Bohle-like virus infection in two Australian frog species (Litoria splendida and Litoria caerulea). , 2015, Journal of comparative pathology.

[2]  R. Speare,et al.  Priorities for management of chytridiomycosis in Australia: saving frogs from extinction , 2016, Wildlife Research.

[3]  F. Pasmans,et al.  Batrachochytrium salamandrivorans: The North American Response and a Call for Action , 2015, PLoS pathogens.

[4]  B. Bolker,et al.  Context‐dependent conservation responses to emerging wildlife diseases , 2015 .

[5]  Christina M. Romagosa,et al.  Integrating invasion and disease in the risk assessment of live bird trade , 2014, Diversity & distributions.

[6]  A. Tweedie,et al.  Incursions of Cyprinid herpesvirus 2 in goldfish populations in Australia despite quarantine practices , 2014 .

[7]  R. Whittington,et al.  Global trade in ornamental fish from an Australian perspective: the case for revised import risk analysis and management strategies. , 2007, Preventive veterinary medicine.

[8]  Emily H. Chan,et al.  Global capacity for emerging infectious disease detection , 2010, Proceedings of the National Academy of Sciences.

[9]  Samuel B. Fey,et al.  Recent shifts in the occurrence, cause, and magnitude of animal mass mortality events , 2015, Proceedings of the National Academy of Sciences.

[10]  T. Waltzek,et al.  Ranaviruses: Not Just for Frogs , 2014, PLoS pathogens.

[11]  Nicholas D. Preston,et al.  Global biogeography of human infectious diseases , 2015, Proceedings of the National Academy of Sciences.

[12]  T. Waltzek,et al.  Transmission of Ranavirus between Ectothermic Vertebrate Hosts , 2014, PloS one.

[13]  J. Ross,et al.  Integrative Analysis of the Physical Transport Network into Australia , 2016, PloS one.

[14]  Wolfgang Nentwig,et al.  Crossing Frontiers in Tackling Pathways of Biological Invasions , 2015 .

[15]  Dean Wilson,et al.  Surveillance, Risk and Preemption on the Australian Border , 2002 .

[16]  Rhys A. Farrer,et al.  Recent introduction of a chytrid fungus endangers Western Palearctic salamanders , 2014, Science.

[17]  N. Moody,et al.  Isolation and characterisation of a novel Bohle-like virus from two frog species in the Darwin rural area, Australia. , 2012, Diseases of Aquatic Organisms.

[18]  Kristine M. Smith,et al.  First Evidence of Amphibian Chytrid Fungus (Batrachochytrium dendrobatidis) and Ranavirus in Hong Kong Amphibian Trade , 2014, PloS one.

[19]  K. Murray,et al.  History and recent progress on chytridiomycosis in amphibians , 2016 .

[20]  P. Hulme,et al.  Invasive species challenge the global response to emerging diseases. , 2014, Trends in parasitology.

[21]  A. Gould,et al.  FIRST IDENTIFICATION OF A RANAVIRUS FROM GREEN PYTHONS (CHONDROPYTHON VIRIDIS) , 2002, Journal of wildlife diseases.

[22]  Stephen R. Carpenter,et al.  Scenario Planning: a Tool for Conservation in an Uncertain World , 2003, Conservation Biology.

[23]  J. Hoverman,et al.  Reliability of non-lethal surveillance methods for detecting ranavirus infection. , 2012, Diseases of aquatic organisms.

[24]  A. K. Davis,et al.  Cryptic infection of a broad taxonomic and geographic diversity of tadpoles by Perkinsea protists , 2015, Proceedings of the National Academy of Sciences.