Alien pathogens and parasites impacting native freshwater fish of southern Australia: a scientific and historical review Simon Kaminskas Murray–Darling Basin Authority, Canberra, Australia [email protected] Downloaded from http://meridian.allenpress.com/australian-zoologist/article-pdf/doi/10.7882/AZ.2020.039/2675961/10.7882_az.2020.039.pdf by guest on 26 September 2021 Native freshwater fish of Australia have a diverse but largely undescribed endemic pathogen and parasite fauna. However, due to long-shared evolutionary histories and virulence/transmissibility trade-offs, effects of these endemic pathogens and parasites appear to be subtle: significant impacts are rarely observed and epizootics have not been recorded. In contrast, a number of alien pathogens and parasites are now established across southern Australia, causing manifestly harmful effects to native fish species and known or suspected epizootics in native fish populations. Undetected and/or undescribed alien viral pathogens are also suspected of being present. Alien pathogens and parasites were introduced to Australia with imports of live alien fish or their fertilised eggs. A review of the scientific and historical evidence indicates that they have had, and continue to have, greater impacts on native fish species than previously realised—especially for freshwater species. This review also documents a previously unknown, Murray-Darling-Basin-wide epizootic of Murray cod Maccullochella peelii in 1929–30, which may have contributed to strong declines in the related eastern freshwater cod Maccullochella ikei. A serious Chilodonella epizootic of M. peelii in 1982 is also examined. In addition, a possible role for alien viruses of the family Iridoviridae (Ranavirus and Megalocytivirus) in the general decline of the critically endangered silver perch Bidyanus bidyanus, and the rapid collapse of two specific native fish populations—upper Murrumbidgee River B. bidyanus and Shoalhaven River Macquarie perch Macquaria australasica—is suggested. It is argued that the severity of the impact of the virulent alien oomycete Saprolegnia parasitica, both historical and present day, has been underestimated. Finally, action is recommended against emerging new pathogen and parasite threats, and the extreme risk current alien fish importations pose in introducing them. These will further threaten already stressed native fish populations in southern Australia, particularly across the Murray-Darling Basin. ABSTRACT Key words: alien fish, importation, stocking, alien parasites, alien pathogens, epizootics, Saprolegnia, Lernaea, Chilodonella, Iridoviridae, Ranavirus, Megalocytivirus, Sphaerothecum, Maccullochella, Gadopsis, Galaxias, Prototroctes, Macquaria, Bidyanus, Murray-Darling Basin DOI: https://doi.org/10.7882/AZ.2020.039 Introduction The spread and emergence of new, alien pathogens and salmon fluke Gyrodactylus salaris on naïve Norwegian parasites is receiving increasing attention as a threat Atlantic salmon Salmo salar stocks (Johnsen and to the world’s endemic freshwater faunas. Reports of Jensen 1988, 1991), and the multiple extinctions and emerging diseases in amphibians, fishes, crayfishes and declines in frog species around the world from chytrid even Copepoda have significantly increased in the fungus Batrachochytrium dendrobatidis (e.g. Skerrat et al. scientific literature in recent decades (Johnson and Paull 2007; Cheng et al. 2011). More recently, the formerly 2011; Roennfeldt 2013). New fungal and fungal-like widespread European sunbleak Leucaspius delineatus has pathogens are emerging in fish and are on the increase severely declined due to total spawning inhibition and globally (Gozlan et al. 2014). Importantly, various studies increased mortality caused by an alien fungal pathogen have shown the ornamental fish trade (Whittington and (rosette agent Sphaerothecum destruens) vectored by an Chong 2007; Peeler et al. 2011) and aquaculture (Johnson asymptomatic invasive alien fish (topmouth gudgeon and Paull 2011; Okamura and Feist 2011; Peeler et al. Pseudorasbora parva) (Gozlan et al. 2005). Sphaerothecum 2011) are the major vectors spreading these pathogens destruens is now having further devastating impacts on and parasites around the world. naïve endemic freshwater fish species across Eurasia as well as on sea bass Dicentrarchus labrax farming operations Notable impacts of alien pathogens and parasites in the Mediterranean Sea (Ercan et al. 2015). internationally include the near-extirpation of the European noble crayfish Astacus astacus by the alien These impacts are largely predicted by the scientific oomycete crayfish plague Aphanomyces astaci (Alderman literature. Endemic pathogens and parasites are an 1996), the catastrophic impact of the translocated Baltic expected component of any ecosystem, with extensive Australian 2020 Zoologist A Kaminskas linkages in foodwebs and roles in competitive and trophic peelii in 1929–30, which may also have contributed to interactions and species fitness (Marcogliese 2004; strong declines in the related eastern freshwater cod Hudson et al. 2006; Lymbery et al. 2010; Johnson and Maccullochella ikei, Paull 2011; Okamura and Feist 2011). Endemic pathogens and parasites generally lead to subtle sub-clinical chronic • highlight the future threat posed by alien pathogens and (i.e. long-term) infections that are tolerated by their parasites, which are currently entering Australia in large endemic fish hosts. This is a reflection of natural processes quantities with imported ornamental fish, and and a long evolutionary history between hosts and parasites (Okamura and Feist 2011). However, when alien • explore the role of historical evidence in understanding pathogens and parasites are introduced to new areas and and providing context to past declines of threatened Downloaded from http://meridian.allenpress.com/australian-zoologist/article-pdf/doi/10.7882/AZ.2020.039/2675961/10.7882_az.2020.039.pdf by guest on 26 September 2021 switch hosts to new, naïve species and populations (host- native freshwater fish and their current conservation switching), their effects are often severe to catastrophic. situation. Such impacts can generally be attributed to a lack of innate immunity in the new host compared with the original host (Peeler et al. 2011). Significantly, such severe Analysis effects are also exacerbated by the generalist ecological Of the alien pathogens and parasites presented in nature of most parasites and pathogens that succeed in Table 1, those of greatest concern and therefore establishing in new habitats (Dove 2000; Gozlan et al. considered for further analysis are: 2014). The ability of generalist pathogens and parasites to infect multiple hosts means there is no selective • viruses of the Iridoviridae family advantage to them in moderating their virulence and this feature often drives high virulence in susceptible and/or • the oomycetes Saprolegnia parasitica and Aphanomyces naïve hosts (Langdon 1990; Peeler et al. 2011; Gozlan et invadans al. 2014). • the ecto-parasitic protozoans Chilodonella hexasticha and The historical record and scientific literature clearly Ichthyophthirius multifiliis, and demonstrate that Australian freshwater systems and their naïve endemic fish faunas have been similarly impacted by • the non-protozoan parasites Lernaea cyprinacea and alien pathogens and parasites. Schyzocotyle acheilognathi. A summary of alien pathogens and parasites that are of EHNV and other members of the concern to native freshwater fish and have established Iridoviridae Family in southern Australia is provided at Table 1. These can be divided into five main groups: viruses, bacteria, Epizootic Haematopoietic Necrosis Virus (EHNV) is oomycetes, protozoans, and parasites (internal and a member of the Ranavirus genus and the Iridoviridae external). Known alien viruses affecting southern family, a family of viruses that infect invertebrates and Australian native fish in the wild currently only comprise non-homeothermic vertebrates. A number of ranaviruses the ranavirus Epizootic Haematopoietic Necrosis Virus affecting fish suddenly emerged between the mid-1980s (EHNV), vectored by alien redfin perch Perca fluviatilis and mid-1990s, proving to be severe pathogens of fish and possibly alien rainbow trout Oncorhynchus mykiss1 and capable of causing severe epizootics with high (see Table 1). However, other viruses listed in Table 1 are mortality rates (Whittington et al. 2010). EHNV was suspected of being present, and both ISKNV and VER isolated in 1985, and was the first ranavirus recorded have already entered Australian aquaculture facilities, to cause epizootic mortalities in fish, with Santee- causing severe mortalities (Clunie and Koehn 2001; Cooper Virus (SCV) and European Catfish Virus (ECV) Go and Whittington 2006). Other significant disease- following shortly after (Langdon et al. 1986; Whittington causing agents are the alien ecto-parasitic protozoans et al. 2010). EHNV and ECV are very closely related to and the virulent alien oomycetes (Table 1). each other, and closely related to the type species for the Ranavirus genus, Frog Virus 3 (FV–3), which was In undertaking this analytical review, this paper specifically isolated from the leopard frog Rana pipiens in North seeks to: America in the 1960s (Whittington et al. 2010). This indicates that EHNV probably had its origin in an • explore the role of alien pathogens and parasites in amphibian host (although iridoviruses are adept at host- historical declines