Assessment of the risk to Norwegian biodiversity from import and keeping of crustaceans in freshwater aquaria

Introduction The Norwegian Scientific Committee for Food and Environment (VKM) was requested by the Norwegian Environment Agency to assess the risk of negative impacts to biodiversity in Norway resulting from import of crustacean decapods for keeping in freshwater aquariums. VKM was asked to 1) list species of crayfish, crabs and shrimps that are currently kept in freshwater aquaria in Norway, and species that are likely to be kept in freshwater aquaria in Norway within the next 10 years, 2) assess the ability of the species to survive under Norwegian conditions and cause impacts on ecosystems and other species, and 3) state the potential negative effects on the biological diversity of diseases caused by pathogens, regulated under the Norwegian Food Act.Methods The risk assessment, without focus on pathogens, was performed in two steps. First, we used a pre-screening toolkit to identify species of crayfish, crabs and shrimps with potential to become invasive in freshwater habitats in Norway. Each species was given an invasiveness score based on 55 questions on biogeography, ecology, and climate change. In a second step, a full risk assessment, including the potential impacts of pathogens, was conducted on those species receiving the highest invasiveness score. This assessment included questions on the organism’s probability of entry and pathways of entry, establishment and spread, potential impacts on biodiversity, and how climate change scenarios might affect the assessment. Likelyhood and confidence was assessed for each question. In conclusion, each species was designated as either low-, moderate-, or high risk. Many crustacean decapod species are confirmed or suspected carriers of pathogens that can cause mass mortality among native crustaceans. The risk posed by crustaceans as carriers of pathogens may be independent of the environmental risk that they pose through ecological interactions. Therefore, the four crustacean disease pathogens that are regulated under the Norwegian Food Act, were assessed separately. These include Aphanomyces astaci causing crayfish plague, white spot syndrome virus (WSSV) causing white spot disease, Taura syndrome virus (TSV) causing Taura syndrome, and yellow head virus genotype 1 (YHV1) causing yellow head disease. The assessments comprised questions on the pathogen’s probability of entry (as a hitchhiker organism with imported crustaceans), pathways of entry, establishment and spread, and potential impact on crustacean biodiversity. Likelihood and confidence were assessed for each question. In conclusion, each pathogen was designated as either low-, moderate-, or high risk.In a third step, we categorized the likelihood that a crustacean species introduces a pathogen associated with a high- or moderate risk into: I) known chronic carriers, II) suspected chronic carriers, III) suspected situational carrier, IV) possible pathogen transmitters, and V) no direct or circumstantial evidence for carrier status or pathogen transmission in the genus.Results Based on information from the Norwegian Pet Trade Association, the project group listed 112 taxa (mainly species and some genera) of freshwater crayfish, crabs and shrimps that are relevant for trade in Norway. These included 38 crayfish taxa, 28 crab taxa, and 45 shrimp taxa. In addition, one marine crab was included. Sixteen species of crayfish, four species of shrimps, and two species of crabs underwent a full ecological risk assessment. The probabilities of entry both into the aquarium trade in Norway, and potentially further into Norwegian nature, were based on the prevalence of the species in the aquarium trade in Norway. We assumed that all species were equally likely to escape captivity or to be released. The four pathogens regulated under the Norwegian Food Act are either known or potential hazards to biodiversity in Norway. A. astaci is already present in Norway. It is regarded among the greatest threats to European freshwater crayfish, including noble crayfish (Astacus astacus). American freshwater crayfish are either known or suspected chronic carriers of A. astaci, while several crayfish species from other continents, as well as some species of crab and shrimp, may be situational carriers. WSSV is a "non-exotic" list 2 disease. All decapods can be infected by the virus. WSSV is primarily a problem in shrimp farming in Asia, but has spread to America and more recently to Australia. WSSV can cause 100% mortality in noble crayfish at water temperatures above 20 °C. Both TSV and YHV1 are "exotic" list 1 diseases. These can infect and cause high mortality in a limited range of saltwater shrimps. There is no evidence that TSV and YHV1 pose a risk to freshwater crayfish in the Nordic climate, nor is introduction likely through aquarium trade in freshwater crustaceans. Several other pathogens that cause crustacean dirsease are listed by the World Organization for Animal Health (OIE). These were briefly assessed, but not fully risk assessed.Conclusions VKM concluded that the risk of negative impacts on biodiversity caused by ecological interactions following import and private keeping of crayfish is high for Faxonius virilis, Faxonius spp., Procambarus clarkii, P. virginalis, and Pacifastacus leniusculus. These species can displace native crayfish, reduce the abundance of aquatic plants, and cause cascading effects that negatively influence invertebrates, fish, and birds. They can likely establish in Norwegian nature under the current climate conditions. The risk of negative consequences is moderate (with medium confidence) for the crayfish Cambarellus patzcuarensis, Procambarus alleni, Creaserinus fodiens, Cambarellus montezumae, Cherax monticola, Cherax tenuimanus, Faxonius neglectus. Perconon gibbesi of the crabs and Neocaridina davidi and Macrobrachium rosenbergii of the shrimps were associated with a moderate risk with medium confidence. Species associated with medium risk are omnivorous keystone species that will have at least moderate ecological impact on littoral freshwater ecosystems (medium confidence) if established in dense populations. None of the species associated with medium risk are likely to establish today. However, climate change will increase the risk for establishment and resulting ecological impact. The risk for negative impacts caused by the crayfish plague pathogen Aphanomyces astaci is high with high confidence. Crayfish plague can cause up to 100% mortality, and has already eradicated several noble crayfish populations in Norway. For WSSV, the risk for negative impact is moderate with high confidence. The risks associated with TSV and YHV1 are assessed as low for Norwegian crustacean biodiversity. According to the risk assessment of pathogens and the categorization of crustacean species based on their likelihood of being carriers of A. astaci and WSSV, 25 and 13 species of crayfish are associated with a high and medium risk, respectively. Four and 25 species of crabs are associated with a medium and low risk, respectively, and 14 and 31 species of shrimps are associated with medium and low risk, respectively. Notably, all species in the named genera should be regarded as belonging to the given risk category. OIE and general literature provide information of known crustacean diseases along with known susceptible crustacean hosts. However, there is a lack of information regarding carrier status of known and unknown disease pathogens for many exotic crustaceans. In this perspective, all exotic crustaceans should be regarded as potentially infected with a known or unknown pathogen. In order to reduce the risk of spreading diseases, eggs and living or dead animals should under no circumstances be disposed of in nature. The same applies for aquarium water or any material, such as gravel or ornamental plants, that have been in contact with the animals or water in the aquarium. The current permit requirement exemption for import of freshwater organisms that can only survive at temperatures above 5 °C provides no protection against the introduction, establishment, and spread of accompanying pathogens that could cause mass mortality in Norwegian crustacean populations. Finally, we can never predict how, or from which host species, a new disease might emerge. Many pandemics and plagues result from cross-continental pathogen-host jumps often facilitated by human transport, trade, introduction, release, or escape of alien species and associated alien pathogens.