Parasite threats from the ornamental fish trade

Trujillo-González, Alejandro (2018) Parasite threats from the ornamental fish trade. PhD thesis, James Cook University.

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The ornamental fish trade is an important commodity sector that involves the capture or farming of fish species for their aesthetic value. Since the 1960s, technological advances have enabled multiple countries to trade numerous ornamental fish species globally. As such, the ornamental fish trade is a pathway for the introduction of exotic fish species and their associated parasites and pathogens into endemic environments, with the potential for detrimental effects on biodiversity, ecosystems, industries, and their dependent local communities.

Governments can establish quarantine measures to detect, prevent and mitigate the risks of introducing exotic parasites and pathogens. For example, Australia has established import requirements for ornamental fish species based on risk assessments undertaken by the Australian government Department of Agriculture and Water Resources (DAWR). However, Australian risk assessments largely focus on parasites and pathogens of global significance in food fish production (i.e., salmonids and prawns). As such, established biosecurity requirements for the import of ornamental fish to Australia (DAWR 2018), focus on pathogenic bacteria (e.g., Aeromonas salmonicida (Lehmann and Neumann, 1896)) and viruses (e.g., spring viraemia of carp virus (SVCV)) known to impact aquaculture, while a much broader parasite fauna of ornamental fishes remains to be assessed. The aim of this thesis was to address three specific gaps of knowledge of the ornamental trade. First, I examined limitations in data collation of t ornamental fish imported to Australia (Chapter 2). Second, I examined the diversity of parasite fauna infecting traded marine and freshwater ornamental fish species (Chapter 3 and 4), and; third, I evaluated the validity of cutting-edge molecular methods to detect parasites infecting imported ornamental fishes at border control (Chapters 5 and 6).

Accurate data that describes the supply and demand of the global ornamental trade is essential for the development of comprehensive biosecurity protocols to protect endemic ecosystems and natural resources from introduced pathogens and parasites. To quantify the species diversity and volume of ornamental fishes imported to Australia, I examined publicly available data of aquarium fish imports to Australia between 2010-2016, collated and curated by DAWR (Chapter 2). I found that DAWR provides publicly available records of imported ornamental fish species ascribed to categories that offered limited resolution regarding the specific species identity. Taxonomically sound evaluation of Australian aquarium imports would be useful to understand the importance of the Australian aquarium trade in the translocation of potentially hazardous parasites and pathogens, and aid international conservation policies.

Following, I surveyed freshwater and marine ornamental fish populations imported from Asia (i.e., Singapore, Malaysia, Thailand and Sri Lanka) to Australia for the presence of protozoan (Chapter 3) and metazoan parasites (Chapter 4). Fish were received following veterinary certification by exporting countries declaring no clinical signs of pests or diseases, and visual inspection by Australian Quarantine Services. Fish necropsies revealed a diverse array of parasite species, including 18 putative types of myxozoans (e.g. Ceratomyxa, Kudoa and Myxobolus spp.), and 14 parasitic monogenean species (e.g. Dactylogyrus, Gyrodactylus, Urocleidoides, and Trianchoratus spp.). One of the major findings was that goldfish, Carassius auratus Linnaeus, 1758, which are the most frequently traded freshwater fish species world-wide, exhibited high parasite diversity (Chapter 3 and 4). Subsequently, I conducted an exhaustive review of the history of the goldfish trade and parasite richness to provide insight into how the international trade of this species may have facilitated parasite co-introduction and co-invasion (Chapter 5). I found that more than 113 parasite species infect goldfish in their native range, of which 26 species were likely co-introduced with the international trade of goldfish (or other cyprinids). These included harmful, generalist parasite species in freshwater aquaculture fishes such as Ichthyophthirius multifiliis Fouquet, 1876, Lernaea cyprinacea Linnaeus, 1758, and Schyzocotyle acheilognathi (Yamaguti, 1934). It is concluded that the goldfish trade likely continues to facilitate the introduction and invasion of exotic parasites on a global scale.

It is clear that pre-export health requirements for the importation of ornamental fish species into Australia are not being met (Chapters 3-5), and that cryptic parasites are not detected during visual inspections at border control. Thus, inspection prior to exportation and at border control must account for the highly cryptic nature of parasites and pathogens and consider alternatives to current pre-export conditions and visual inspections at border control. For this reason, I proposed screening fish transport water for the presence of parasite environmental DNA (eDNA) as a detection method for enhanced biosecurity (Chapter 6). I examined water samples from 11 target populations (cyprinids susceptible to Dactylogyrus spp. infections) and seven non-target fish populations (non-cyprinids, not susceptible to Dactylogyrus spp. infections) imported from southeast Asia to Australia for the presence of eDNA from five Dactylogyrus species (Monogenea: Dactylogyridae) using novel species-specific quantitative PCR (qPCR) assays. Dactylogyrus spp. eDNA was detected in all targeted fish populations, showing that eDNA presents a considerable advantage over visual inspections and parasitological necropsies. However, Dactylogyrus spp. eDNA was also detected in water from non-cyprinid fish populations that are not susceptible to and were not infected by Dactylogyrus parasites, highlighting the risk of false positive detections associated with contaminated water sources used to transport ornamental fish species. Environmental DNA screening for parasite DNA offers a highly sensitive and non-invasive detection tool during pre-export monitoring of ornamental species and could aid quarantine officers to triage high-risk ornamental fish exports based on eDNA detection of parasite DNA in the exporting country. Nonetheless, quarantine officers should be vigilant in the limitations posed by contaminated water sources if eDNA screening methods are used at border control.

Parasite eDNA detection in water samples from non-cyprinid fish populations in Chapter 5 suggested the possibility of false positive detections by eDNA screening. For this reason, I tested the reliability of eDNA screening methods by qPCR for biosecurity purposes in an experimental system simulating the export process (Chapter 7). Experimentally infected live fish (i.e., the monogenean Neobenedenia girellae (Hargis, 1955) infecting Lates calcarifer (Bloch, 1790)) were used to detect parasite eDNA in water samples, simulating the export process from packaging to delivery over a 48 h period. The consignments included 'infected fish', 'treated fish', and 'contaminated water' (containing dead parasites) delivered by 'exporting companies'. Quantitative PCR tests were inaccurate when detecting eDNA collected from low parasite intensities (mean intensity ± S.D. = 6.80 ± 4.78 parasites/fish). Quantitative PCR tests detected parasite eDNA in 50% of infected fish indicating a high plausibility of false negative detections because of low eDNA concentrations in water samples. Furthermore, parasite eDNA was detected in70% of non-infected fish in contaminated water samples, indicating the possibility of false positive detection of DNA from dead parasites present in the water. Environmental DNA screening methods, while more sensitive than current biosecurity protocols, are limited for accurate and reliable use where differentiation between live parasite infections and dead, non-viable parasites in the water is paramount.

This thesis highlights the limitations of the DAWR current data collation framework to accurately examine aquarium fish import data and determined that a large diversity of protozoan and metazoan parasites are not detected at border control. Import conditions for ornamental species are not being met by exporting companies. While eDNA screening methods offer a potential tool for the detection of cryptic pathogens, the limitations of this technique need to be considered for development as a detection tool to demonstrate freedom from parasite infection in the ornamental fish trade.

Item ID: 64533
Item Type: Thesis (PhD)
Keywords: aquaculture, aquarium trade, biosecurity, border control, Carassius auratus, cointroduction, coinvasion, data curation, ectoparasites, eDNA, environmental DNA, fish, import, infection, invasive parasites, life cycle, molecular genetics, monogenea, ornamental fish, ornamental trade, parasite cultures, parasites, policy, qPCR, quarantine, species translocation, transboundary animal disease
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Copyright Information: Copyright © 2018 Alejandro Trujillo-González.
Additional Information:

Five publications arising from this thesis are stored in ResearchOnline@JCU, at the time of processing. Please see the Related URLs. The publications are:

Chapter 2: Trujillo-Gonzalez, Alejandro, and Militz, Thane A. (2019) Taxonomically constrained reporting framework limits biodiversity data for aquarium fish imports to Australia. Wildlife Research, 46 (4). pp. 355-363.

Chapter 3: Hutson, Kate, Brazenor, Alexander, Vaughan, David, and Trujillo Gonzalez, Alejandro (2018) Monogenean parasite cultures: current techniques and recent advances. In: Rollinson, D., and Stothard, J.R., (eds.) Advances in Parasitology. Advances in Parasitology, 99 . Elsevier, London, UK, pp. 61-91.

Chapter 4: Trujillo-Gonzalez, Alejandro, Becker, Joy A., and Hutson, Kate S. (2018) Parasite dispersal from the ornamental goldfish trade. In: Rollinson, D., and Stothard, J.R., (eds.) Advances in Parasitology. Elsevier, London, UK, pp. 239-281.

Chapter 5: Trujillo-González, Alejandro, Edmunds, R. C., Becker, J. A., and Hutson, K. S. (2019) Parasite detection in the ornamental fish trade using environmental DNA. Scientific Reports, 9. 5173.

Chapter 6: Trujillo-González, A., Becker, J.A., Huerlimann, R., Saunders, R.J., and Hutson, K.S. (2020) Can environmental DNA be used for aquatic biosecurity in the aquarium fish trade? Biological Invasions, 22. pp. 1011-1025.

Date Deposited: 05 Oct 2020 23:57
FoR Codes: 07 AGRICULTURAL AND VETERINARY SCIENCES > 0704 Fisheries Sciences > 070404 Fish Pests and Diseases @ 33%
05 ENVIRONMENTAL SCIENCES > 0501 Ecological Applications > 050103 Invasive Species Ecology @ 34%
06 BIOLOGICAL SCIENCES > 0604 Genetics > 060499 Genetics not elsewhere classified @ 33%
SEO Codes: 83 ANIMAL PRODUCTION AND ANIMAL PRIMARY PRODUCTS > 8301 Fisheries - Aquaculture > 830102 Aquaculture Fin Fish (excl. Tuna) @ 50%
96 ENVIRONMENT > 9604 Control of Pests, Diseases and Exotic Species > 960401 Border Biosecurity (incl. Quarantine and Inspection) @ 50%
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