Risky Business: Live Non-CITES Wildlife UK Imports and the Potential for Infectious Diseases

International wildlife trade is recognised as a major transmission pathway for the movement of pathogenic organisms around the world. The UK is an active consumer of non-native live wild animals and is therefore subject to the risks posed by pathogen pollution from imported wildlife. Here, we characterise a key yet overlooked portion of the UK wildlife import market. We evaluate the trade in live non-CITES (Convention on International Trade in Endangered Species) wild terrestrial animals entering the UK over a 5-year period using data reported by the Animal and Plant Health Agency (APHA). Between 2014 and 2018, over 48 million individual animals, across five taxonomic classes and 24 taxonomic orders, were imported into the UK from 90 countries across nine global regions. The largest volumes of wild animals were imported from North America and Asia, and most of the import records were from Europe and Africa. Excluding Columbiformes (pigeons) and Galliformes (‘game birds’), amphibians were the most imported taxonomic class (73%), followed by reptiles (17%), mammals (4%), birds (3%), and arachnids (<1%). The records described herein provide insight into the scope and scale of non-CITES listed wildlife imported in to the UK. We describe the potential for pathogen pollution from these vast and varied wildlife imports and highlight the potential threats they pose to public health. We also draw attention to the lack of detail in the UK wildlife import records, which limits its ability to help prevent and manage introduced infectious diseases. We recommend that improved record keeping and reporting could prove beneficial in this regard.

Did you wash your caving suit? Cavers’ role in the potential spread of Pseudogymnoascus destructans, the causative agent of White-Nose Disease

White-Nose Disease (WND) has killed millions of hibernating bats in the US and Canada. Its causative agent, the fungus Pseudogymnoascus destructans was introduced to North America, but is native to Europe and Asia, where it is not associated with mass mortality. Although it is nearly impossible to eradicate an emerging wildlife disease, research on P. destructans spread mechanisms can aid in prevention of new introductions and development of better environmental management strategies. It is of particular importance to quantify the potential role of people visiting caves (cavers, tourists, bat researchers, etc.) whom inadvertently move P. destructans spores between sites, and to limit spread, particularly to areas where the fungus is absent. In the course of two consecutive field seasons, samples were collected from the equipment before and after work in Bulgarian caves where P. destructans is present. Viable P. destructans spores were isolated from field equipment after nearly 100% of cave visits, irrespective of the season. Results from lab experiments show the pathogen’s spores can remain viable on pieces of contaminated caving equipment under room temperature for at least 25 days, with no significant reduction in germination rates. This is concerning evidence indicating the potential for movement of viable P. destructans spores across countries and continents. Results further demonstrated that any type of regular washing can successfully remove the majority of P. destructans spores from several fabric types. Brushing complemented by washing in a ‘washing machine’ was slightly more effective than brushing alone, while a washing temperature of 50°C was more effective than temperatures of 30 and 40°C. However, none of the methods herein tested fully removed P. destructans and hence they are not a substitute for decontamination. Since many cavers forgo washing equipment after surveys, and bat workers often visit several underground sites per day during monitoring activities without cleaning equipment in between sites, it is essential to raise awareness on this subject and introduce hygienic protocols for the prevention of pathogen pollution in underground sites.

Trade in wild anurans vectors the urodelan pathogen Batrachochytrium salamandrivorans into Europe

Pathogen pollution has caused dramatic losses of amphibian diversity on a global scale. The recently emerged chytrid fungus Batrachochytrium salamandrivorans (Bsal) has been hypothesized to have its origin in Asian urodelan populations, from which it may have been introduced to Europe through the trade in live urodelans. We here show that Bsal is present on wild small-webbed fire-bellied toads (Bombina microdeladigitora) from Vietnam and on representatives of the same species that have recently been imported in Germany. This finding suggests that the installment of measures to mitigate the Bsal threat through the amphibian trade should not be limited to urodeles, but should equally take anurans into account.

California mussels (Mytilus californianus) as sentinels for marine contamination with Sarcocystis neurona

SUMMARYSarcocystis neurona is a terrestrial parasite that can cause fatal encephalitis in the endangered Southern sea otter (Enhydra lutris nereis). To date, neither risk factors associated with marine contamination nor the route of S. neurona infection to marine mammals has been described. This study evaluated coastal S. neurona contamination using California mussels (Mytilus californianus) as sentinels for pathogen pollution. A field investigation was designed to test the hypotheses that (1) mussels can serve as sentinels for S. neurona contamination, and (2) S. neurona contamination in mussels would be highest during the rainy season and in mussels collected near freshwater. Initial validation of molecular assays through sporocyst spiking experiments revealed the ITS-1500 assay to be most sensitive for detection of S. neurona, consistently yielding parasite amplification at concentrations ⩾5 sporocysts/1 mL mussel haemolymph. Assays were then applied on 959 wild-caught mussels, with detection of S. neurona confirmed using sequence analysis in three mussels. Validated molecular assays for S. neurona detection in mussels provide a novel toolset for investigating marine contamination with this parasite, while confirmation of S. neurona in wild mussels suggests that uptake by invertebrates may serve as a route of transmission to susceptible marine animals.

Clinically healthy amphibians in captive collections and at pet fairs: A reservoir of Batrachochytrium dendrobatidis

Batrachochytrium dendrobatidis is the cause of the fungal disease chytridiomycosis, a potentially lethal skin disease of amphibians. Asymptomatically infected amphibians may pose a risk for environmental pathogen pollution. This study therefore assessed the role of healthy, captive amphibians as a reservoir of Batrachochytrium dendrobatidis. Samples were collected from captive amphibians in Belgium, the Netherlands, Germany and France (559 from anurans, 330 from urodelans and 4 from gymnophians) from private owners, zoos, and laboratories. In addition to which, 78 anurans from 19 living collections were sampled during a pet fair in the Netherlands. Nearly 3% of the captive amphibians were infected by B. dendrobatidis, and 13.6% of the collections yielded at least one positive result. At the fair, 7 out of 78 anurans, representing 2 collections were positive. None of the animals that tested positive showed any obvious health problems at the time of sampling. Our results demonstrate the potential of the amphibian pet trade as a vehicle for the spread of B. dendrobatidis.