Alien pathogens and parasites impacting native freshwater of southern : 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 of Australia have a diverse but largely undescribed endemic pathogen and parasite . 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 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 . 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 peelii in 1929–30, which may have contributed to strong declines in the related 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 ) in the general decline of the critically endangered silver perch bidyanus, and the rapid collapse of two specific native fish populations—upper Murrumbidgee B. bidyanus and australasica—is suggested. It is argued that the severity of the impact of the virulent alien oomycete 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, , Chilodonella, Iridoviridae, Ranavirus, Megalocytivirus, Sphaerothecum, Maccullochella, , , , 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 . Reports of Jensen 1988, 1991), and the multiple extinctions and emerging diseases in , , crayfishes and declines in 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 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 (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 , 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 (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 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 and the Iridoviridae external). Known alien viruses affecting southern family, a family of viruses that infect and Australian native fish in the wild currently only comprise non-homeothermic . 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 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 host (although iridoviruses are adept at host- historical declines and extirpations of specific native fish switching between fish and amphibians) and is an alien populations and consider if this role is more significant pathogen likely spread by the importation of alien fish, than commonly realised, amphibians or for the pet trade (Whittington et al. 2010). In terms of its entry to Australia however, alien • document a previously unknown, Murray-Darling- Gambusia Gambusia holbrooki remains the major suspect Basin-wide epizootic of Maccullochella (Langdon 1989). 1 Formerly Salmo gairdneri Australian B Zoologist 2020 Native fish pathogens

TABLE 1. Alien pathogens and parasites known or suspected to cause manifest harm or epizootic events in native fish freshwater of southern Australia (including the Murray-Darling Basin). Scientific name Common name Known or probable alien fish Known or probable wild Key references vectors impacts VIRUS Family Iridoviridae, Epizootic gambusia (Gambusia Declines of silver perch Langdon and Humphrey 1987; Ranavirus Haematopoietic holbrooki)—initially?; (), Macquarie Langdon et al. 1988; Langdon Genus Macquaria australasica et al. Necrosis Virus (EHNV) redfin perch (Perca fluviatilis); perch ( ), 1989; Whittington 2010; galaxias species (Galaxias spp.). Becker et al. 2013 rainbow trout (Oncorhynchus

mykiss). 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 Family Iridoviridae, Dwarf Gourami Uncertain; capable of using Uncertain but may be Go and Whittington 2006; Go et al. Genus Iridovirus/Infectious multiple fish species. involved in unexplained rapid 2006; Go 2015 Megalocytivirus Spleen and Kidney population crashes of silver Necrosis Virus (ISKNV) perch (Bidyanus bidyanus) and and strains and Macquarie perch (Macquaria variants thereof; other australasica). Megalocytivirus species Family Nodaviridae, Viral Encephalopathy and Other than native Uncertain if present in the Clunie and Koehn 2001 Lates calcarifer Genus Retinopathy (VER) ( ), uncertain; wild. Betanodavirus presumed to be an alien pathogen. BACTERIA Aeromonas Ulcer Disease goldfish (Carassius auratus); Uncertain. Clunie and Koehn 2001; Read salmonicida nova et al. et al. (GUD) (Cyprinus carpio); 2007; Rowland 2007; Rowland 2009 brown trout (Salmo trutta); rainbow trout (Oncorhynchus mykiss). Flavobacterium1 Columnaris carp (Cyprinus carpio); Uncertain; possible cause Clunie and Koehn 2001; Read columnare et al. et al. goldfish (Carassius auratus); of 1929–30 Murray cod 2007; Rowland (Maccullochella peelii) epizootic. 2007; Rowland 2009; Declercq brown trout (Salmo trutta); et al. 2013 rainbow trout (Oncorhynchus mykiss); other species; illegally released aquarium fish. Flavobacterium sp. ‘fin rot’ carp (Cyprinus carpio); Uncertain. Clunie and Koehn 2001; Read et al. et al. Vibrio sp. goldfish (Carassius auratus); 2007; Rowland 2007; Rowland 2009; Declercq Pseudomonas sp. brown trout (Salmo trutta); et al. 2013 Aeromonas sp. rainbow trout (Oncorhynchus mykiss); other species; illegally released aquarium fish. OOMYCETE Saprolegnia water mould, cotton brown trout (Salmo trutta); Probable cause of large-scale Puckridge et al. 1989; Rowland parasitica mould, ‘fungus’ rainbow trout (Oncorhynchus late-1800s epizootics of and Ingram 1991; Cadwallader Saprolegnia mykiss Australian grayling (Prototroctes 1996; van West 2006; Phillips other ). maraena et al. et al. species ) and lesser epizootics 2007; Rowland of cod species (Maccullochella 2007; Rowland 2009; Gozlan spp.), Macquarie perch et al. 2014 (Macquaria australasica) and blackfish species (Gadopsis spp.). Regular cause of bony herring ( erebi) epizootics since at least the 1940s. Almost certain to be a pathogen of poorly handled caught-and-released Murray cod (Maccullochella peelii), and of Murray cod mats in the wild. Possible cause of 1929– 30 Murray cod epizootic. 1 Formerly Flexibacter

Australian 2020 Zoologist C Kaminskas

Scientific name Common name Known or probable alien fish Known or probable wild Key references vectors impacts Aphanomyces Epizootic Ulcerative Uncertain; capable of using Epizootics in estuarine species Clunie and Koehn 2001; Read invadans Disease (EUS), red-spot multiple fish species; Darling in estuaries of northern NSW et al. 2007; Rowland et al. disease River epizootics may have and southern . 2007; Rowland 2009; Boys et been initiated by movement Recent large-scale epizootics al. 2012; Gozlan et al. 2014; of infected native silver of freshwater native fish Kamilya and Baruah 2014 perch (Bidyanus bidyanus) for species in the . aquaculture.

Chilodonella Chilodonella carp (Cyprinus carpio); Regular epizootics of Murray Rowland and Ingram 1991; 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 hexasticha Maccullochella peelii goldfish (Carassius auratus); cod ( ) and Clunie and Koehn 2001; Read catfish (Tandanus tandanus), et al. 2007; Rowland et al. brown trout (Salmo trutta); most notably in the upper 2007; Rowland 2009; Trueman rainbow trout (Oncorhynchus system in 2011 mykiss); 1982. Hatchery epizootics, and suspected wild epizootics, other species; of (Maccullochella illegally released aquarium fish. macquariensis) and eastern freshwater cod (Maccullochella ikei). Ichthyophthirius Ich, white-spot carp (Cyprinus carpio); Has almost certainly caused Rowland and Ingram 1991; multifiliis goldfish (Carassius auratus); historical and modern Clunie and Koehn 2001; Read epizootics, though poorly et al. 2007; Rowland et al. brown trout (Salmo trutta); documented. 2007; Rowland 2009 rainbow trout (Oncorhynchus mykiss); other species; illegally released aquarium fish. Ichthyobo necator Ichthyobo Uncertain; capable of using Uncertain. Rowland and Ingram 1991; spp. Tetrahymena multiple alien fish species; Clunie and Koehn 2001; Read illegally released aquarium fish. et al. 2007; Rowland et al. Trichodina spp. Trichodina 2007; Rowland 2009 PARASITES (Non-Protozoan) Schyzocotyle Asian fish tapeworm carp (Cyprinus carpio); Uncertain, but causes regular Scott and Grizzle 1979; Dove 2 acheilognathi Carassius auratus epizootics in western carp et al. 1997; Dove 1998; Dove goldfish ( ); Hypseleotris (Platyhelminth) gudgeon ( and Fletcher 2000; Lintermans Gambusia Gambusia holbrooki; klungzingeri) in Lake Burley- 2007 many other species. Griffin, ACT. Lernaea cyprinacea anchor worm () carp (Cyprinus carpio); possibly Causes severe infestations and Grabda 1963; Khalifa and Post Carassius auratus (Copepoda) goldfish ( ); serious physiological harm and 1976; Rowland and Ingram illegally released aquarium fish. stress to diverse native fish 1991; Goodwin 1999; Clunie species. and Koehn 2001; Bond 2004; Piasecki et al. 2004; Lymbery et al. 2010 Ergasilus spp. gill lice (copepod) carp (Cyprinus carpio); possibly Uncertain. Rowland and Ingram 1991; goldfish (Carassius auratus); Clunie and Koehn 2001; Read (Copepoda) et al. et al. illegally released aquarium fish. 2007; Rowland 2007; Rowland 2009

2 Formerly Bothriocephalus acheilognathi

EHNV has a number of effects on infected fish, but the 1984 as G. holbrooki were first imported into Australia in key effect is severe necrosis of the haematopoietic or 1925 and were widely released in south-eastern Australia blood cell producing organs (kidney, liver and spleen), in the 1930s in a misguided attempt to control mosquitoes with subsequent haemorrhaging causing death (Langdon (White and Pyke 2011)). and Humphrey 1987). EHNV was first isolated from dead alien Perca fluviatilis that had been collected from Langdon (1989) conducted sensitivity trials with EHNV several Victorian water bodies in 1984 (Langdon et al. isolates from alien Perca fluviatilis and found P. fluviatilis 1986). However, unexplained spring-time kills of alien to be the most susceptible fish species to EHNV, and P. fluviatilis had been noted in some Victorian waterways as the primary vector. Bath-exposed Macquaria australasica early as 1972 (Langdon and Humphrey 1987), suggesting recorded 100% mortality (n = 10, 10) and bath-exposed EHNV’s origins significantly pre-date 1984. (Indeed, if Bidyanus bidyanus recorded significant mortalities ranging G. holbrooki were the means of EHNV’s introduction to between 30–66% (n = 10, 10, 6). Langdon (1989) Australia, EHNV’s presence must significantly pre-date speculated that EHNV may have been a factor in the Australian D Zoologist 2020 Native fish pathogens decline of M. australasica, B. bidyanus and Galaxias spp. in Burrinjuck Reservoir provides an accurate sequential recent decades. Alien Oncorhynchus mykiss were found to fit with historical evidence including the first record of be mildly susceptible, and capable of carrying EHNV virus alien P. fluviatilis from the in the asymptomatically. Studies recorded EHNV in a number Australian Capital Territory (ACT) (Lintermans 2000, of hatcheries propagating O. mykiss in the 1980s and 2002). An analysis of the Canberra Times newspaper 1990s (e.g. Langdon et al. 1988; Whittington et al. 1994; reports for Burrinjuck Reservoir reveals abundant Whittington et al. 1999). Thus, any stockings or releases B. bidyanus catches up to and including 1986: of O. mykiss fingerlings from these hatcheries into the wild—authorised or unauthorised—may have vectored ‘Burrinjuck now has a huge population of silver perch …’

EHNV into wild habitats in south-eastern Australia, (CT 1985) 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 particularly in the 1980s and early 1990s when awareness of EHNV was lower. Langdon (1989) experimentally ‘… many holiday makers are catching so many silver and infected further M. australasica with EHNV isolates from that it looks as if this is going to be one of the O. mykiss, with a mortality rate of 80% (n = 10) proving dam’s best seasons for these species.’ (CT 1986a) this transmission pathway is possible. ‘… silver perch are the most common fish this week.’ (CT In contrast to Langdon (1989), a more recent, larger- 1986b) scale study demonstrated only modest EHNV mortality in bath-exposed M. australasica (28%) (n = 135), but ‘… silver perch are as numerous as ever …’ (CT 1986c) substantial mortalities (40%) in bath-exposed B. bidyanus (n = 107) (Becker et al. 2013). This suggests the However, few catches of B. bidyanus are mentioned in impact of EHNV on wild M. australasica stocks may the Canberra Times fishing reports in 1987, and almost have been overestimated, while the impact of EHNV none were reported in 1988. They disappeared from on wild B. bidyanus stocks may have been seriously fishing reports completely after 1988, with the exception underestimated. Indeed, EHNV or a similar Iridoviridae of one brief mention in 1995 (CT 1995). This timeline pathogen (i.e. Ranavirus or Megalocytivirus) is strongly also fits neatly with monitoring data upstream from the suspected of involvement in the rapid decline and collapse short-lived Casuarina Sands (Table 2), which of some wild B. bidyanus populations in the 1980s (TSSC trapped B. bidyanus individuals as they made their annual 2012) and may be involved in their dramatic Murray- summer upstream migration up the Murrumbidgee River, Darling-Basin-wide decline at that time. This larger-scale a renowned local event (Pratt 1979; TSSC 2012). study also demonstrated that EHNV primarily affects juvenile fish, with less than 1% of older M. australasica, It is argued that this approximately two year switch from and less than 4% of >100 mm B. bidyanus affected emphasised abundance to effective localised extinction of (Becker et al. 2013). B. bidyanus is simply too rapid to be the consequence of a typical species decline due to more ecological reasons Whittington et al. (2010) reported that EHNV, while such degradation, alien fish competition, over- sporadically found in other parts of the Murray-Darling harvesting, etc. This conclusion is further supported by Basin, now appears to be endemic (i.e. permanently the species’ biology—namely a typical 7+ year life-span established in the epidemiological sense) in the upper and maximum age of 17+ years in Murray–Darling Murrumbidgee River. It is noteworthy that the sudden waterways (Mallen-Cooper and Stuart 2003; Tonkin rapid collapse of the strong B. bidyanus population in the et al. 2019). Such a pattern of rapid transition from upper Murrumbidgee River and Burrinjuck Reservoir in abundance to localised extinction does however have the late 1980s coincides with the general encroachment all the hallmarks of a naïve fish population struck by a of alien P. fluviatilis and EHNV, as well as alien Cyprinus virulent alien pathogen. Although it is acknowledged carpio, into the upper Murrumbidgee catchment that such a pattern may fit other potential causes such as (Lintermans 2000, 2002). a major water quality or pollution event, none of sufficient magnitude are recorded or known from this time period. EHNV was recorded from the downstream tributary impoundment of in 1986, but from Finally, Pratt provides an intriguing oral history where Burrinjuck Reservoir in 1990 (Whittington et al. 1996). he describes dead and dying B. bidyanus specimens from However, use of 1986 as an entry date for EHNV into Burrinjuck Reservoir and the Murrumbidgee River below

TABLE 2. Bidyanus bidyanus catches in a trap in the Murrumbidgee River at Casuarina Sands, Australian Capital Territory, 1981–91 (Lintermans 2000, 2002). The blank cells indicate zero captures during a drought which impeded movement.

Australian 2020 Zoologist E Kaminskas it with EHNV-like symptoms (Trueman 2011). The date with excellent native riparian vegetation, excellent nominated for this event by Pratt however—1967—is too spawning substrates and substantial unregulated natural early to be congruous with the timeline above. The date perennial flows (Figure 1). The decline of this important nominated by Pratt for alien P. fluviatilis entering Lake insurance population of Murray-Darling M. australasica Burley-Griffin and the upper Murrumbidgee River above can perhaps only be attributable to a pathogen of some Burrinjuck Reservoir, i.e. late 1960s, is also too early to be kind; the most likely candidate is introduction of alien congruous with the timeline above or with other accounts EHNV as a result of alien O. mykiss stockings. Langdon of these events (e.g. Lintermans 2000, 2002). However (1989) demonstrated that such a transmission pathway if some aspects of Pratt’s recollection of the B. bidyanus is possible, Whittington et al. (1999) recorded EHNV in

mortality event are accurate, it may be reflecting an an O. mykiss farm in the upper Shoalhaven catchment, 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 earlier outbreak of EHNV or of similar but undetected/ and Becker et al. (2013) demonstrated that EHNV was undescribed alien ranaviruses or related megalocytiviruses. a pathogen of juvenile M. australasica with negligible mortality of older M. australasica. Sampling by Lintermans Another rapid and so far unexplained collapse of a native (2008) indicated a population comprised of a few large fish population that strongly suggests involvement of surviving adults, that were clearly spawning, but with EHNV or another alien viral pathogen of the Iridoviridae negligible recruitment of juvenile M. australasica— family, involves Macquaria australasica of the Shoalhaven consistent with a scenario of elevated juvenile mortality River Basin. This genetically distinct population arguably via EHNV. Finally, the author explored the Mongarlowe warranted description as a distinct species (Faulks et al. River in the lower boundaries of 2010; Faulks et al. 2011). It was, by all anecdotal accounts in the mid-late 1990s and observed shoals of similarly- and department reports, present and abundant in the sized alien O. mykiss in the stream, which were strongly remote and undisturbed inflowing tributary Kangaroo River suggestive of the stream receiving stockings of alien (Figure 1) and in Tallowa Dam (flooded 1979) in the 1980s O. mykiss, either authorised or unauthorised. Given an and early 1990s. After the invasion of illegally released absence of effective control on the purchase of fingerlings alien Cyprinus carpio, and the commencement of stocking of alien trout species (O. mykiss and Salmo trutta) in of hatchery-bred Macquaria novemaculeata Australia, if any unauthorised stockings of O. mykiss (endemic to this system before the dam), also in the 1990s, occurred in this stream in the past, it is possible that this M. australasica population underwent a precipitous and fingerlings were used from the EHNV-infected farm rapid decline to extinction. By 1998 none could be sampled occurring in the same catchment. despite extensive efforts (Faulks et al. 2011). Neither the invasion of alien C. carpio, nor the re-established presence An examination of the scientific literature confirms that the of formerly endemic and sympatric M. novemaculeata seem presence of undescribed and/or undetected alien viruses in sufficient to explain this rapid extinction, but both of these Australian freshwaters is far from speculative and is in fact processes offer ample opportunity for vectoring alien viral inevitable. Whittington and Chong (2007) highlight the pathogens into Tallowa Dam and the Kangaroo River, with vast number of pathogen-harbouring alien fish imported subsequent effects on a naïve native fish population. into Australia annually, and the serious inadequacies of quarantine and disease surveillance measures applied Finally, any discussion of alien EHNV or other alien to these imports. Metagenomics/next-generation genetic ranaviruses/megalocytiviruses potentially causing sequencing reveal the vast diversity of undescribed viruses collapses of M. australasica populations would be remiss in fish species (e.g. Mungang’andu 2016; Nkili-Meyong et not to touch on the situation. The al. 2017). Geoghegan et al. (2018) document 12 potential Mongarlowe River is a tributary of the Shoalhaven River undescribed viruses from four species of fish purchased system, in turn noteworthy for hosting an EHNV outbreak from a market, and suggest their results support on an alien O. mykiss farm in the 1990s (Whittington et an emerging view that fish harbour a large and mostly al. 1999). The Mongarlowe River received at least one uncharacterised virome. Only recently, Mordecai et al. translocation of Murray-Darling M. australasica from (2019) discovered several novel viruses in endangered the Murrumbidgee River in the late 1800s (Sydney Mail Oncorhynchus spp. salmon populations in Canada. 1876; Goulburn Evening Penny Post 1897), and these established a thriving population in its middle and lower The Iridoviridae family of viruses is of significant concern, reaches. This M. australasica population was still thriving particularly the genera Ranavirus and Megalocytivirus. in 1969, as documented by accounts Ranaviruses are an emerging class of fish pathogen with (e.g. Pratt 1971). However, as documented by Lintermans a track record of causing severe epizootics with heavy (2008), the population has declined severely and is now mortalities in fish (Whittington et al. 2010). The genus effectively vestigial with minimal recruitment; its long Ranavirus has already yielded EHNV in Australia. Future term persistence is doubtful. threats lie in the genus Megalocytivirus, with species such as Dwarf Gourami Iridovirus (DGIV), effectively This is a decline that simply does not make sense. The synonymous with Infectious Spleen and Kidney Necrosis Mongarlowe River, over the period of this decline (i.e. Virus (ISKNV), spread by asymptomatic alien dwarf 1969–2008), has provided superb M. australasica habitat gouramis Colisa lalia. In 2013, an outbreak of this virus Australian F Zoologist 2020 Native fish pathogens

1. 2. 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

3. 4.

5. 6.

FIGURE 1. (1) Upper Murrumbidgee River near Burrinjuck Reservoir—core range of former silver perch Bidyanus bidyanus population (S. Kaminskas). (2) Bidyanus bidyanus (G. Schmida). (3) Kangaroo River—former habitat of Shoalhaven Macquarie perch Macquaria australasica (B. Stewart). (4) Shoalhaven Macquaria australasica (K. Pitman). (5) Mongarlowe River—habitat of a population of Murray-Darling Macquaria australasica that has suffered severe declines (‘Grahamec’, Wikimedia Commons). (6) Murray-Darling Macquaria australasica (J. Tait). caused a 90% mortality rate of Maccullochella peelii et al. 2006). Research has also shown that a number of co-cultured at an aquaculture facility—a stark indication megalocytiviruses can affect both marine and freshwater of its possible effects in the wild. Further research showed fish and are a great potential threat to Australian native the virus could spread between the two species through fish, including catadromous species (Go 2015). the water, and had a 90%+ mortality rate for M. peelii (Go and Whittington 2006). It was further demonstrated The Iridoviridae family potentially presents an that DGIV/ISKNV was present in 22% of alien gouramis indirect threat to native fishes. The recently described Colisa and Trichogaster spp. in retail shops in Sydney (Go Iridescent Virus (ZoopIIVHR) Australian 2020 Zoologist G Kaminskas was first recovered from south-eastern Australia and historical epizootics in Australia, supports its role as a demonstrates the capacity of some Iridoviridae to primary pathogen of fish. strongly affect invertebrates. It chiefly affects and cladocerans, which are important food sources for Research by Sandoval-Sierra et al. (2014) suggests the fish larvae, to the point where zooplankton communities situation with alien Saprolegnia spp. introductions may and presumably fish recruitment are strongly affected be even more complex than originally suspected. Their (Roennfeldt 2013). Facilitated by a shift in thermal results from alien salmonid culture systems in Chile regime due to climate change, ZoopIIVHR is regularly suggest multiple alien Saprolegnia species can be involved, reducing a formerly dominant copepod with a key role with each species having a different level of virulence and

in fish recruitment to vestigial levels in the Hopkins preferentially targeting different life history stages. In their 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 River estuary, western (Newton 1996; Newton results, S. parasitica preferentially targeted adult salmonids. and Mitchell 1999; Roennfeldt 2013; DoEE 2018). However, based on current knowledge S. parasitica remains While ZoopIIVHR is thought to be an endemic species the Saprolegnia species of greatest virulence and greatest (Roennfeldt pers. comm. 2019), it cautions that the concern to Australia’s southern native freshwater fishes, introduction of similar but alien Iridoviridae could have and is the focus of this analysis. severe consequences on local zooplankton communities and fish recruitment. Trophic Ecology

The Oomycete Saprolegnia parasitica Saprolegnia species are generally considered saprophytic Saprolegnia parasitica is arguably the most serious alien fish organisms that only secondarily and opportunistically infect pathogen introduced to Australian freshwaters. Multiple fish with surface wounds. There has been considerable lines of evidence suggest it has caused more serious historical debate as to whether S. parasitica can act as a large-scale epizootics/fish mortalities than any other alien primary pathogen and infect fish without pre-existing pathogen, albeit many of them in historical times. wounds or injuries. However, it has long been recognised that some species or strains of Saprolegnia—usually identified Description and as Saprolegnia parasitica—are highly virulent and can attack fish directly, often when low water temperatures reduce the S. parasitica and congeners are eukaryotic organisms that effectiveness of fish immune systems (winter saprolegniosis) have a filamentous growth habit and are coenocytic in (van West 2006; Phillips et al. 2007). nature, i.e. nuclear divisions occur without accompanying cell divisions. They produce broad aseptate (partition- Natural Distribution Versus Human-Assisted Dispersal less) hyphae that in turn form branching multi-nucleate mycelia. These organisms are referred to as Oomycetes or Sampling indicates Saprolegnia spp. have a world-wide ‘water moulds’ and are placed in the Oomycota Phylum distribution (van West pers. comm. 2011), and thus and the Saprolegniaceae Order (Bruno et al. 2011; were probably always present in some form in freshwater Gozlan et al. 2014). Morphologically and trophically they systems of the world. However, the world-wide pattern of resemble fungi and indeed for much of the 1900s they were sudden onset of severe, repeating S. parasitica epizootics in considered as fungal species. However there are subtle aquaculture operations and wild fish populations suggests differences, including cellulosic rather than chitinous cell S. parasitica has been spread to many areas where it was walls, and they are now considered to be taxonomically previously absent, via international movement of infected distinct and to be basal members of a marine algal lineage salmonid individuals and eggs. (i.e. heterokonts/stramenopiles) (Bruno et al. 2011; van Den Berg et al. 2013; Gozlan et al. 2014). Pathogenic Activity

S. parasitica is an extremely complex, highly virulent Motile flagellated unicellular zoospores, typically pathogen with great phenotypic and physiological secondary zoospores, seek out and encyst on the surface plasticity and predominantly asexual reproduction of a host fish. After germinating, S. parasitica hyphae (Diéguez-Uribeondo et al. 2007). The species is wholly grow through the dermal and epidermal tissues of the asexual when acting as a fish pathogen and many isolates fish, seeking nutrition. Evidence suggests S. parasitica from infected fish fail to produce sexual stages when uses proteolytic enzymes to break down fish tissues to cultured in vitro (Bruno et al. 2011). This phenotypic aid nutrition-seeking (Bruno et al. 2011). The hyphae plasticity and asexual reproduction—in a taxa where take the form of visible grey-white cottony growths sexual reproductive structures have been the main on the body surfaces and the gill surfaces, and cause basis for species differentiation—has long dogged cellular necrosis and severe damage to dermal and the taxonomy of Saprolegnia species. There has been epidermal surface tissues. In wild fish populations, considerable debate about the validity of S. parasitica as S. parasitica infections are tenacious once established a species (e.g. Hughes 1994). However, genetic studies and generally lead to fatal haemodilution (loss of now support S. parasitica as a valid species (Diéguez- blood, solutes and osmotic regulation). In aquaculture Uribeondo et al. 2007) and diverse evidence, including settings, S. parasitica infections are very difficult to Australian H Zoologist 2020 Native fish pathogens treat, requiring careful, frequent additions of powerful of S. parasitica which was introduced to Tasmania chemicals that have only limited effectiveness against through importation, propagation and stocking of alien the organism (van West 2006; Phillips et al. 2007; Read salmonids (Atlantic salmon Salmo salar and brown et al. 2007; Rowland et al. 2007). trout Salmo trutta) (Saville-Kent 1887; Cadwallader 1996) (Figure 2). Tasmania—The Original Outbreaks The Inspector of William Saville-Kent makes In the late 1800s, mass fish kills of Australian grayling clear that Saprolegnia was a problem in the Salmon Ponds, Prototroctes maraena occurred in Tasmanian , an alien salmonid hatchery on the Plenty River near

with the dead fish recorded as being covered in Hobart, Tasmania, from the moment the alien salmonid 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 characteristic woolly growths. This is strongly indicative eggs arrived in 1864:

FIGURE 2. Timeline for alien Saprolegnia parasitica colonisation of south-eastern Australia. Australian 2020 Zoologist I Kaminskas

‘… in fact, ever since artificial breeding operations have Colonisation of the Mainland been conducted there [Salmon Ponds], a greater or less number of the breeding fish have been attacked by this Movements of the vectoring alien trout species (Salmo trutta parasitic phase of the fungus, Saprolegnia, and many fish and Oncorhynchus mykiss) from Tasmania to the mainland have died.’ (Saville-Kent 1887) inevitably transferred alien S. parasitica to the mainland. In the state of Victoria, severe epizootics strongly indicative Saville-Kent also records the catastrophic impact of of S. parasitica were recorded in Gadopsis marmoratus in Saprolegnia on Tasmanian P. maraena populations: the southern coastal La Trobe and Gellibrand rivers in 1919–20, and in M. australasica in Lake Eildon (Murray-

‘… some 17 or 18 years ago [1869 or 1870] an epidemic, Darling Basin) in 1937. Also in 1937 S. parasitica (identified 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 apparently and most probably identical with the fungus as ‘Saprolegnia ferox’) was identified in the Ballarat alien disease of the British salmon rivers, broke out among the fish trout (Salmo trutta) hatchery after decades of unexplained of this colony, popularly known as the fresh water herring fish kills by pathogens, and innumerable releases of progeny or mullet, Prototroctes maraena, … This fact is from it into the wild (Appendices 1 and 2). recorded in Mr. R. M. Johnston’s excellent catalogue of the fishes of Tasmania, and has been attested to me by many In the state of (NSW), early kills residents. The fish at this particular period are stated to have involving substantial numbers of Macquaria australasica been seen floating down the rivers in thousands, covered and the cod species Maccullochella peelii and Maccullochella more or less extensively with a cottony fungoid growth. macquariensis2 were recorded in the Canberra/Queanbeyan So virulent and exhaustive was this epidemic that many, region of the Murray-Darling Basin in 1895–96. This was more especially of the southern rivers, were more or less only a mere 7–8 years after alien trout species introductions completely denuded of their stock of this species and have commenced in the region (1888), with fish sourced from so remained up to the present date.’ (Saville-Kent 1887) the Ballarat hatchery (Queanbeyan Observer 1905), and the causative agent actually identified as ‘Saprolegnia Other accounts corroborate Saville-Kent’s observations in ferax’. A similar outbreak is recorded in 1908. Meanwhile, terms of general timing and description of symptoms and regular Prototroctes maraena kills in nearby eastern coastal support alien salmonid introductions and stockings as the rivers are reported in 1906 (Appendix 1). means of spread of this pathogen, e.g.: Subsequently, there appears to be a pattern of steady ‘In northern Tasmania every river teemed with beautiful colonisation of mainland waterways by S. parasitica, driven grayling (otherwise called freshwater herring) … [which] by widespread stocking of alien trout species (O. mykiss also abounded in the south … Nearly 50 years ago brown and S. trutta). S. parasitica was reported as an intractable trout were introduced to Tasmania, and strange to say, pathogen of M. peelii eggs, larvae and adults in experimental the freshwater herring disappeared on a wholesale scale. field hatcheries in the upper Murrumbidgee River in the … Over 30 years ago [<1885] an epidemic broke out 1930s (Dakin and Kesteven 1938) and in M. peelii eggs in among the graylings, and they floated dead down the river the mid- in 1949–50 (Cadwallader 1977); it in countless numbers. It was the same both north and remains an intractable pathogen of M. peelii in hatchery south, in regions far separated …’ (Register 1915) settings to this day (Cadwallader and Gooley 1981; Rowland 1988; Rowland and Ingram 1991). Similarly, S. parasitica and was a regular killer of Nematalosa erebi in the lower Murray River by the 1940s and remains so to this day ‘In about 1868, the herring were smitten by an epidemic (Puckridge et al. 1989) (Figure 2). Puckridge et al. (1989) caused by a fungus, and they suddenly became scarce examined ongoing regular winter infection of wild N. erebi in, and almost disappeared from many rivers in which with S. parasitica in the lower Murray River, and stated that they were formerly abundant. In some places, it is said, ‘Fishermen in the region have noticed fungal infections [in bony thousands of dead fish were seen floating down the rivers, bream] in late winter or early spring since at least the 1940s’ and the fins, eyes, and gill covers being invested with a fungoid that ‘The cyst coat architecture of ... isolates from the Australian growth.’ (Examiner 1931) bony bream is similar to that found in Saprolegnia parasitica from British and Japanese salmonids’. Accounts involving Gadopsis marmoratus also emerge: Effects

‘Mr. G. Russell writes from Longford, Tasmania, on S. parasitica is today recorded as an endemic seasonal March 6 … Blackfish have almost entirely disappeared pathogen of golden galaxias Galaxias auratus from the largest of our , a fungoid disease in Lakes Crescent and Sorrell in Tasmania, an being the cause about three seasons since [~1896]. 2 Historically Murray cod Maccullochella peelii and trout cod Maccullochella I myself saw the fish dead in hundreds floating on the macquariensis co-habited many southern Murray–Darling Basin streams, water.’ (Australasian 1899) particularly in upland reaches. Anglers were highly variable in their ability to distinguish the two species. Therefore, in some locations, historical references to ‘cod’ are likely to involve both species. Australian J Zoologist 2020 Native fish pathogens endemic freshwater fish listed as ‘Endangered’ under Summation Commonwealth legislation. Characteristically striking in winter, the pathogen causes severe and presumably In their entirety, these accounts and studies suggest fatal saprolegniosis with a frequency of occurrence as S. parasitica has had severe effects and is now ubiquitous great as 40% in monthly fish samples (Hardie et al. in most or all of south-eastern Australia. It is noteworthy 2007). Undoubtedly introduced by the numerous alien that severe epizootics do not seem to occur with this trout (S. trutta) stockings that these waterways have alien pathogen today. However, this may be an artefact received historically, this interesting record represents of undersampling, with continuing effects hard to study another stepping-stone in the colonisation of Tasmanian or quantify. Gozlan et al. (2014) for example outline the

freshwater systems by alien S. parasitica. difficulties of studying the effects of fungal and fungal- 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 like organisms in fish in extensive, often-turbid river Tasmanian populations of Prototroctes maraena arguably systems. In any case, the effects of past epizootics on the never recovered their described original high abundance of some native fish species persist to after epizootics due to S. parasitica. Today they are a this day. Similarly, key questions remain regarding the sporadically sampled species and listed as ‘Protected’ and effect of S. parasitica on wild fish that have experienced ‘Vulnerable’ under various Tasmanian laws and ‘Vulnerable’ angler handling or environmental stress, and on eggs and under Commonwealth legislation (Backhouse et al. 2008). egg mats of native freshwater fishes in the wild.

Alien-trout-vectored S. parasitica must also be considered The 1929–30 Maccullochella peelii epizootic a strong suspect in the otherwise unsatisfactorily The most remarkable aspect of the 1929–30 Maccullochella explained extinction of the closely related New Zealand peelii epizootic is that it was forgotten. The author has grayling Prototroctes oxyrhynchus in the early 1900s never seen nor heard reference to this epizootic in (McDowall 1976; but see Lee and Perry 2019). The scientific, management or popular literature or discussion; fanatical zeal with which alien trout species (O. mykiss consequently, it was a surprise to find details of such a and S. trutta) were stocked in both Australia and serious and widespread fish epizootic in the Australian New Zealand, even in the most remote and unsuitable National Library’s TROVE Archive (see Appendix 2). waterways (e.g. Tilzey 1977; Cadwallader 1996), would (Trueman (2011) makes general reference to several have been a very effective way to rapidly disperse a kills contained within this event, but not in an epizootic virulent alien pathogen such as S. parasitica over large context.) This epizootic was severe in terms of the number islands, including into otherwise remote and largely of M. peelii killed, and remarkable for its geographic undisturbed areas. The process of ‘polyplanetism’ or extent. Kills commenced in June 1929 and continued Repeated Zoospore Emergence (RZE) in S. parasitica, well into 1930. They were reported from Darling River where secondary zoospores undergo repeated cycles headwater tributaries, the Darling River proper, the of encystment and relatively synchronous zoospore Murray River and its effluents from its upper reaches in release, may have made S. parasitica particularly suited Albury, NSW to its lowest reaches in , and to this form of dispersal (Uribeondo et al. 1994; van the major tributary , Victoria (Appendix West 2006). S. parasitica readily achieves four cycles 2). An account of this epizootic from the east-flowing of encystment and zoospore release in vitro, and up to Clarence River in the same time period, affecting the six cycles (Uribeondo et al. 1994). This is suggested to closely related eastern freshwater cod Maccullochella ikei, be an adaptation by S. parasitica to a parasitic lifestyle, is also significant. It is well known that along with heavy allowing zoospores multiple opportunities to find hosts , two catastrophic events struck M. ikei in as swimming spores, and multiple opportunities to the early 1900s, playing key roles in reducing it from an wait out unfavourable conditions as encysted spores abundant species to a rare and imperilled species (TSSC (Uribeondo et al. 1994; van West 2006). Recent research 2015). These events were severe widespread tin- has confirmed other long-suspected parasitic adaptations pollution in the 1930s and catchment-wide bushfires by S. parasitica, namely specialised long hooked hairs on and ash fish kills in 1936 (TSSC 2015). The 1929–30 secondary cysts for superior adhesion to hosts (Rezinciuc epizootic may represent another, hitherto unrecognised et al. 2018) and chemical mechanisms for suppression of catastrophic event for the species, on the eve of the host immune responses (Belmonte et al. 2014). decade where the other two would fall.

S. parasitica infections of Bidyanus bidyanus in winter Given the severity of the M. peelii epizootic, it is worth in aquaculture ponds (winter saprolegniosis) emerged speculating as to which alien pathogen may have caused as a serious problem in Australia in the 1990s (Read et it. Unfortunately, the available descriptions of symptoms al. 2007; Rowland et al. 2007; Rowland 2009). While of the dying fish are inconclusive. The primary suspect in aquaculture settings, this indicates the range of remains the virulent alien oomycete Saprolegnia parasitica, S. parasitica in Australia is still expanding, with the despite the lack of mention of the characteristic ‘cotton attendant risk of spilling this pathogen back to wild wool’ growths. (However gill inflammation is mentioned.) habitats (Johnson and Paull 2011; Okamura and Feist The capacity for S. parasitica to cause significant epizootics 2011; Peeler et al. 2011). in native fish species, including M. peelii, has already been Australian 2020 Zoologist K Kaminskas outlined. The 1929–30 epizootic also fits the expected A. invadans was first recorded in Australia in 1972 in geographic and temporal spread of the virulent alien estuarine fishes near Bundaberg, Queensland (QLD), oomycete S. parasitica throughout the Murray-Darling and has since spread through much of coastal NSW as Basin (and coastal systems)—striking in lower reaches well as the Northern Territory and Western Australia. several decades after regular stocking of vectoring alien In 2008 and 2010, A. invadans was recorded in native trout species (O. mykiss and S. trutta) had established both freshwater fish (Maccullochella peelii, Macquaria ambigua, alien host and alien pathogen in the upper reaches of these Nematalosa erebi, unicolor) in the Murray- river systems. Records show that by the 1940s this alien Darling Basin (Darling River). The severity of ulceration pathogen had become endemic in the lower reaches of the in the 2010 outbreak suggests native fish species are very

Murray River, causing annual fish kills of Nematalosa erebi susceptible to infection by A. invadans (Boys et al. 2012). 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 (Puckridge et al. 1989); the 1929–30 epizootic involving M. Given the rapid and continuing spread of A. invadans peelii may have been its first advance into the middle and since first being recorded in Japan in 1971, and its broad lower Murray system. There is scant evidence to support host range and virulence, A. invadans is likely to become or contradict 1929–30 as an entry date for S. parasitica into an increasingly serious pathogen of native freshwater and the Clarence River system, but the uppermost reaches of estuarine fishes in Australia as well as globally (Kamilya the system had invariably received a number of stockings and Baruah 2014). of alien trout species by this time. It is also noteworthy that even today, curious observations can be made in this system The Protozoans Chilodonella hexasticha and of wild M. ikei individuals with minor Saprolegnia infections Ichthyophthirius multifiliis around the dorsal spines (author’s pers. obs.). Chilodonella hexasticha and Ichthyophthirius multifiliis are Columnaris Flavobacterium columnare may also be considered ecto-parasitic protozoans that infect the surface tissues as a candidate for the 1929–30 M. peelii epizootic. As a and gills of fish. They are rapidly reproducing, virulent pathogen of fish it is somewhat similar to S. parasitica, in that parasites that frequently cause mass mortalities of fish it infects the skin surface and gills and causes skin lesions in aquaculture operations around the world, including and ulcers and gill necrosis (Declercq et al. 2013). Fin Bidyanus bidyanus operations in Australia. Both organisms infection and erosion is an additional symptom. Mortality have caused a number of recorded kills of Australian can be caused by gill damage leading to respiratory and native freshwater fish in the wild (Rowland and Ingram circulatory failure and internal haemorrhage, loss of osmotic 1991; Fishing World 2011). regulation, or secondary bacterial infections (Declercq et al. 2013). An argument in favour of F. columnare is that the A kill of Maccullochella peelii in the upper reaches of the epizootic continued through warming water temperatures Macquarie River (Bathurst to ) and its into spring and summer; F. columnare is well-known for its tributaries and Crudine Creek by Chilodonella liking of warmer water temperatures and its capacity to hexasticha is noteworthy for its severity and long-term cause epizootics in warm-water fishes (Declercq et al. 2013). impacts. It commenced in May–June 1982 (Schaerf pers. comm. 2020) and continued into August 1982, and was The Oomycete Aphanomyces invadans confirmed by NSW Fisheries Department staff to be Aphanomyces invadans, also known as Epizootic Ulcerative caused by C. hexasticha (Rowland and Ingram 1991). Very Syndrome (EUS) or ‘red-spot disease’, is another virulent low flows and very cold water temperatures appear to oomycete in the same family as Saprolegnia parasitica have suppressed the immune systems of affected native (Saprolegniaceae). As a fish pathogen A. invadans has fish and pre-disposed them to this epizootic. Numerous striking similarities to S. parasitica including asexual dead and dying M. peelii, as well as catfish Tandanus reproduction, spore encystment and mode of pathogenic tandanus were observed in the streams (Rowland and activity, although A. invadans penetrates through to and Ingram 1991; Schaerf pers. comm. 2020). An expert affects internal organs of fishes more frequently than local fisher, familiar with these waterways and a witness S. parasitica (Kamilya and Baruah 2014). A. invadans to the , advises that M. peelii populations in the causes severe ulcerations on the body surfaces of fish. area were permanently impacted, with the Turon River These ulcerations are frequently fatal due to necrosis population not fully recovering and the Crudine Creek of surface tissues and haemodilution, however some population never recovering (Schaerf pers. comm. 2020). individuals of various fish species can and do recover The source of the outbreak is not known but it would from A. invadans (Rowland pers. comm. 2011; Boys et be informative to ascertain if any stockings of alien trout al. 2012; Kamilya and Baruah 2014). In aquaculture, species (Oncorhynchus mykiss and Salmo trutta) occurred juvenile fish are much more susceptible than larger fish in these reaches in the weeks leading up to the epizootic. (Rowland pers. comm. 2011; Boys et al. 2012). Similar to S. parasitica, outbreaks typically strike at times of low Chilodonella hexasticha is also strongly suspected as the cause water temperature. A. invadans is almost certainly an alien of a severe fish kill of trout cod Maccullochella macquariensis pathogen imported by alien fish movement, fitting the in Lake Sambell, Victoria, in late September 1970 (Trueman pattern of sudden eruption in endemic fish populations 2011). This event was extremely serious as it caused the around the world (Boys et al. 2012; Iberahim et al. 2018). effective extirpation of the Lake Sambell M. macquariensis Australian L Zoologist 2020 Native fish pathogens population at a time when it was one of only three • the impossibility of its eradication once established in known populations for the species. Indeed, Berra (1974) the wild nominated Lake Sambell as one of only two reliable sites to collect M. macquariensis in 1970, along with Seven Creeks. • its recent introduction to other countries via alien fish Unaware of what befell the Lake Sambell M. macquariensis imports, and population only several months after he finished sampling it, Berra’s (1974) concerns over the possibility of a natural • the need for an effective quarantine regime for imported or man-made disaster affecting these populations was very alien fish (Advertiser 1931). prescient. Again, it would be informative to ascertain if any

stockings of alien trout species (Oncorhynchus mykiss and By 1936 however, Hale was lamenting the entry of 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 Salmo trutta) had occurred in this waterbody in the weeks I. multifiliis into the Tasmanian Plenty Ponds alien trout leading up to the epizootic. hatchery (Advertiser 1936), already noted as the entry point of the virulent alien oomycete Saprolegnia parasitica It is highly likely that C. hexasticha has caused many into Australia. However, the spread of I. multifiliis more serious native fish kills in southern Australia continued and by 1939 it was present on the mainland. than recorded here. Rowland and Ingram (1991) note Here it caused mass mortalities in the Ballarat alien trout the great vulnerability of all Maccullochella species (S. trutta) hatchery (The Age 1939) and was disseminated to C. hexasticha and report numerous hatchery fish into the wild with alien trout stockings. kills. Furthermore, in addition to the 1982 Macquarie River event, they report another suspected fish kill of The Ecto-parasitic Copepod Lernaea M. peelii by C. hexasticha, during September and early cyprinacea October 1980, in and the Murray and Ovens rivers above Yarrawonga Weir. Unfortunately, Lernaea cyprinacea is an ecto-parasitic copepod up to the symptoms of C. hexasticha do not have a distinctive ~10 mm long with a complex life-cycle of three non- ‘tell-tale’ to identify it in historical accounts, unlike the parasitic nauplius stages, five copepodid stages which cottony growths etc. of Saprolegnia parasitica. There are parasitise the gills, a free-living but parasitic sexually- numerous fish kills in the historical record the author has reproducing cyclopoid stage, and the familiar final not cited either because of a lack of identifying details sedentary stage, where fertilised females permanently for the pathogen/parasite or because possible pathogen/ imbed in fish muscle and develop egg sacs (Grabda 1963). parasite kills appear confounded with other effects/ Warmer temperatures dramatically speed up the species’ events such as water quality or pollution. life-cycle, and thus the severity of infestations and their physiological impacts. Optimum temperatures ranging Ichthyophthirius multifiliis arguably has somewhat more from 25 to 32°C are suggested for L. cyprinacea (e.g. distinctive symptoms and may have been the cause of a Grabda 1963; Piasecki et al. 2004; Hossain et al. 2018). severe fish-kill event of Tandanus tandanus in Nagambie Hossain et al. (2018) report a study where the entire life Weir, Victoria, in 1908 (Argus 1908). Descriptions cycle of L. cyprinacea took 18–25 days when fish were of the ‘the white disease’ which ‘causes a scum to grow held at 29°C. Females produced batches of up to 250 over the eye of the fish’ are relatively consistent with juveniles (nauplii) every two weeks for up to 16 weeks at I. multifiliis symptoms (Rowland and Ingram 1991; Read temperatures warmer than 25°C. et al. 2007). However this outbreak occurred before the apparent date of entry of I. multifiliis into mainland L. cyprinacea is now widely found in freshwater fish of Australia freshwaters, and thus possibly may have been southern Australia (Rowland and Ingram 1991; Harris C. hexasticha. The date of entry of C. hexasticha into and Gehrke 1997; Bond 2004; Lintermans 2007). This Australian freshwaters is not known. parasite was inadvertently brought into Australia imports of diseased Cyprinus carpio, goldfish (Carassius auratus) It is noteworthy that despite the complete recklessness or Perca fluviatilis, and was spread by many years of legal with which alien fish were imported into Australia in and illegal releases of diseased fish. Alien C. carpio are the 19th and early 20th centuries, with no attempt made considered the major vector of the parasite (Rowland at disease detection or quarantine, there were insightful and Ingram 1991; Piasecki et al. 2004; Lintermans 2007). individuals who saw the risk of these imports in regards L. cyprinacea has low host specificity at all life stages and to alien pathogens such as Ichthyophthirius multifiliis. The has proven itself capable of infesting a very wide range Director of Adelaide Museum and trenchant critic of of fish species (Shariff et al. 2006). Serious infestation alien fish importation, H. M. Hale, called attention to the by final stage L. cyprinacea has profound negative risks of I. multifiliis in 1931, emphasising: effects on host fish including severe physiological stress, haemodilution, secondary bacterial infection of puncture • the desirability of keeping it out of Australia wounds, and even puncturing of internal organs in small fish (e.g. Khalifa and Post 1976; Berry et al. 1991; • its harmful effects Rowland and Ingram 1991; Goodwin 1999; Bond 2004; Pérez-Bote 2005; Shariff et al. 2006). Australian 2020 Zoologist M Kaminskas

Serious infestation of final stage L. cyprinacea is often C. carpio is the primary vector, and to a lesser extent observed by both researchers and recreational fishers in alien Gambusia holbrooki (Dove et al. 1997; Dove 1998; various native fish species, but riverine Maccullochella peelii Dove and Fletcher 2000). S. acheilognathi lodges in seem particularly susceptible. The author has observed the intestines of fish and can cause heavy mortalities large riverine M. peelii carrying up to 40-50 L. cyprinacea of small or juvenile fish through complete intestinal per flank (Figure 3). Heavy infestations of final stage blockage, and cause impaired health and growth in L. cyprinacea are known to cause severe physiological larger fish (Scott and Grizzle 1979; Dove 1998). This distress, emaciation and reproductive failure in M. peelii alien parasite has already lead to significant fish kills of (Rowland and Ingram 1991). The impact of the copepodid native carp gudgeon Hypseleotris sp. in the Australian

stages of L. cyprinacea on M. peelii, which target the gills of Capital Territory (ACT) (Lintermans 2007) and may 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 fish, warrants further investigation. pose an increasing threat to the small native fish species of south-eastern Australia, particularly those of the The Asian Fish Tapeworm Schyzocotyle Eleotridae family (Dove 1998). acheilognathi

Schyzocotyle acheilognathi was inadvertently brought into Discussion Australia with importations of Cyprinus carpio and is now It is clear that the continual importation of alien fish present throughout the Murray-Darling Basin (Dove et into Australia, from the 1860s through to the present al. 1997; Dove 1998; Dove and Fletcher 2000). Alien day, has been accompanied by the importation of an

3a. 3b.

3c. 3d.

FIGURE 3. Riverine Murray cod Maccullochella peelii specimens with severe Lernaea infestations during prolonged low flows. (3a) An average-sized M. peelii before release carrying an estimated 36 embedded final stage Lernaea parasites, with 19 on its right flank and an estimated 17 in its caudal fin (G. Peelgrane). (3b) Close-up of caudal fin with Lernaea parasites highlighted. (3c) A large M. peelii before release carrying an estimated 47 embedded final stage Lernaea parasites on its left flank. An estimated 19 parasites are in a dense cluster on the operculum, the rest of the body is carrying 8, and an estimated 20 are present in the left side of the caudal fin (G. Peelgrane). (3d) Close-up of head and operculum with Lernaea parasites highlighted. Australian N Zoologist 2020 Native fish pathogens immense diversity of alien fish pathogens and parasites specimens of the mountain galaxias species complex (Whittington and Chong 2007). Inevitably, many and (Galaxias spp.) from south-eastern Australia—these perhaps most of these alien pathogens and parasites appear to be an endemic parasite fauna of galaxiids. made their way into Australian waterways, with some succeeding in establishing themselves. Some species have Similarly, endemic viral and bacterial pathogens are to be caused severe epizootics in naïve Australian freshwater expected in Australian native freshwater fish, but even less fish species—events which may have been pivotal in is known about them. Nevertheless it is very noteworthy their decline and imperilment, extirpation or extinction that all the pathogens and parasites causing manifestly (e.g. Shoalhaven Macquaria australasica). Ranaviruses harmful effects in native fish individuals and known and

and megalocytiviruses of the Iridoviridae family, and the suspected epizootic events of native fish populations in 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 virulent alien oomycete Saprolegnia parasitica imported and the wild, are known or concluded to be alien in origin (e.g. dispersed with alien trout species (Oncorhynchus mykiss Rowland and Ingram 1991; Corfield et al. 2008). and Salmo trutta), are particularly strongly implicated. An examination of the historical record shows strong Some alien pathogens that caused historical fish kills evidence for this process and resulting fish kills, and an appear less problematic now, presumably having either examination of the extant scientific literature underscores extirpated vulnerable populations of native freshwater the inevitability of this process and these events (given fish, or native freshwater fish populations having gained levels of alien fish importation and release). The alien- some degree of resistance to them. However, many alien fish-vectored pathogen Sphaerothecum destruens is a salient pathogens and parasites are present today, and combined recent example of this process in all respects; it slowly with new introductions, are causing significant ongoing spread throughout Eurasia, it caused major population burdens for native fish. These burdens are exacerbated by crashes in naïve endemic fish species, and it went other threats such as water quality and climate change. unnoticed for over 50 years (Combe and Gozlan 2018). For example, little is known about the degree to which The paucity of knowledge on endemic pathogens egg mats of Maccullochella peelii are damaged or destroyed and parasites of Australian native freshwater fish is by Saprolegnia parasitica infections in wild, nor how many noteworthy—the lack of such a baseline, especially for caught-and-released M. peelii that have experienced rough Saprolegnia species, is unfortunate (Corfield et al. 2008). handling by anglers develop chronic or fatal S. parasitica However, parasites are recognised as an integral part of infections. Given that S. parasitica is an intractable , and are thus to be expected in Australian pathogen of incubating M. peelii eggs and handled M. peelii native freshwater fish in some form (Marcogliese 2004; individuals in hatchery settings (Cadwallader and Gooley Hudson et al. 2006; Lymbery et al. 2010; Johnson and 1981; Rowland 1988; Rowland and Ingram 1991), the Paull 2011; Okamura and Feist 2011). possibility must be considered high.

Indeed, Australian native freshwater fish clearly do have a Similarly, the final life stage of Lernaea cyprinacea rich endemic parasite fauna: parasitises diverse native fish species, but particularly infests Maccullochella peelii heavily (author’s personal • Murray (1931) reports the endemic monogenean gill fluke obs.; Rowland and Ingram 1991; Harris and Gehrke Anchylodiscus tandani from Murray-Darling Tandanus 1997). The previously discussed physiological impacts of tandanus and describes the endemic monogenean gill L. cyprinacea are likely a source of cryptic mortality in fluke Lepidotrema bidyana from Bidyanus bidyanus juvenile and adult M. peelii stocks. However, the earlier copepodid life stages parasitises the gills (Grabda 1963) • Langdon (1990) lists a small number of endemic and damage and necrotise gill lamellae (Khalifa and parasites, including endemic apicomplexans ( Post 1976; Goodwin 1999) and thus impair respiration, and Goussia sp.) of Murray-Darling Basin native fish sometimes to a fatal extent. M. peelii are already noted as having the least tolerance to hypoxia out of all the large • Dove (2000) found 109 putative parasite species from native fish species of Murray-Darling Basin (Small et al. 18 different fish species (6 native, 12 alien) in coastal 2014). Thus a heavy load of copepodid L. cyprinacea in rivers of Eastern Australia, with most parasite species the gills may make the difference between juvenile and concluded to be endemic adult M. peelii surviving warm oxygen-depleted conditions or not—conditions that are becoming far more common • Lymbery et al. (2010) found 44 putative parasite species as the Australian continent starts to experience severe from 18 fish species (12 native, 6 alien) in coastal rivers climate change effects (Steffen et al. 2018). of south-western Australia, with the vast majority of parasite species concluded to be endemic, and Climate change effects are likely to compound the impacts of alien pathogens and parasites, thereby exacerbating • Raadik (2014) observed numerous diversely coloured or compounding the risk from each. For example, the external cysts of trematode metacercariae, and some increasingly common drought-induced scenario of internal infestations of a type of small white worm, in stressed native fish crowded together into remnant pools Australian 2020 Zoologist O Kaminskas for long periods of time, in low flow or no-flow conditions endemic parasites: alien fish hosts may act as reservoirs, over long hot summers, provides optimal conditions for maintaining or amplifying the endemic parasites then L. cyprinacea infestations. Higher water temperatures spilling them back to native fish hosts, even if native fish allow L. cyprinacea to complete its life-cycle rapidly, host populations are in decline (Langdon 1990; Dove leading to very high levels of emerging copepodids in 2000; Okamura and Feist 2011). These processes likely remnant pool environments. The high densities of captive contribute to the extraordinary dominance of alien fish in host fish make successful infestation by these copepodids many Australian rivers, particularly the Murray-Darling and their subsequent life stages almost certain, paving Basin (typically ~80% by number) (Davies et al. 2008; way for further successful generations of L. cyprinacea Davies et al. 2012).

and the production of even more copepodids (Medeiros 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 and Maltchik 1999; Pérez-Bote 2005). The end result is Alien fish importation and invasion already-environmentally-stressed fish experiencing very A vast number of freshwater fish are shipped around the heavy loads of L. cyprinacea infestation and the severe world for the aquarium trade. Australia is no exception, physiological harm and stress such infestations cause. with a vast number of alien fish imported every year Conversely, low flow conditions caused by climate change (Whittington and Chong 2007; Peeler et al. 2011). and drought can also occur in winter, and these conditions The list of species that are permissible for import into are optimal for outbreaks of other pathogens and parasites Australia is long, with many species possessing this status such as Chilodonella hexasticha and Saprolegnia parasitica simply by merit of already being present/imported before (Rowland and Ingram 1991; Rowland 2009). regulation commenced. Pre-import risk assessments of alien fish species have improved over the last two decades The disproportionate effects of parasites and pathogens (e.g. the Commonwealth Environment Protection and on alien fish versus native fish are worth considering. Biodiversity Conservation Act 1999) but are possibly still The ‘competitive release’ or ‘enemy release’ hypothesis not rigorous enough. Such risk assessments must make proposes that alien species escape many of the parasites greater consideration of the risks posed by attendant alien that infect them in their native range when introduced pathogens and parasites. Unfortunately, the difficulties to new areas, due to founder effects/bottlenecks (in both and limitations of pre-import risk assessments are well the host fish species and their parasite communities) and recognised (Whittington and Chong 2007; Peeler et unsuitable new habitats. This leads to increased body al. 2011). Similarly, the difficulties of quarantining or sizes, increased fecundity, greater population densities and screening imported alien fish for pathogens and parasites enhanced competitive ability in alien species in the ‘new’ is also well recognised, requiring high technical ability and areas (e.g. Torchin et al. 2003). significant resources (Gozlan et al. 2014). Both processes are challenged by the fact that many alien pathogens and As per this hypothesis, the studies of Dove (2000) parasites have long latent periods, and that many alien fish and Lymbery et al. (2010) found parasite diversity and individuals are asymptomatic carriers. It is consistently parasite loads were significantly lower in alien species reported that World Trade Organisation (WTO) rules in the Australian river systems they studied. The vastly are an unacceptable impediment to raising the rigor of reduced parasite fauna and parasite load in G. holbrooki both processes (Whittington and Chong 2007; Peeler was particularly striking when compared to its parasite et al. 2011). The Commonwealth Biosecurity Act 2015 fauna in its home range in the southern US (Dove 2000). clearly reflects these impediments with its s.5 preamble Also concerning was that in both studies, but particularly stating that ‘the Appropriate Level of Protection (or ALOP) in Dove (2000), some alien parasites had transferred for Australia is a high level of sanitary and phytosanitary to native fish species, but very few native parasites had protection aimed at reducing biosecurity risks to a very low transferred to alien fish species. A stand-out result in level, but not to zero.’ The author would suggest that these studies involves Lernaea cyprinacea, one of the alien when the long-term survival of unique Australian native parasites of greatest concern due to its strongly harmful freshwater fish (and and crayfish) are at stake— effects, particularly on small-bodied native fish. Lymbery many with enormous cultural, Indigenous, recreational et al. (2010) found L. cyprinacea parasitised alien fish less and economic importance to Australians—this level of than native fish, while Dove (2000) found L. cyprinacea protection may not be sufficient. parasitised native fish but did not parasitise alien fish (poeciliids) at all. New alien fish species continue to establish in the wild in Australian freshwater systems, including through the In further variations of the enemy release hypothesis, insidious means of outdoor ponds overflowing in heavy Dove (2000) suggests new native fish hosts may not rainfall events (Lintermans 2004; Hammer et al. 2019; be ideal for parasite reproduction and that a reservoir NSW DPI 2020). This demonstrates that education of of infection in the alien fish may be necessary for the the public on the importance of not releasing aquarium parasite to persist in the new habitat. Thus, alien fish fish, or keeping them in outdoor ponds that can overflow, may inadvertently use their alien parasites as a biological has been completely inadequate. More effective public weapon in their interactions with native fishes. Finally, education campaigns are desperately needed, in addition alien fish may also harm native fish species with their own to more rigorous risk assessments and biosecurity measures Australian P Zoologist 2020 Native fish pathogens for the aquarium industry. Such studies are hampered by abject historical scientific neglect and the limited, reluctant attention given to alien trout species impacts today. In the rare instances Conclusion where these impacts are examined, the focus has been This analysis has presented a timely investigation into on predation and competition by alien trout species. This the impact of alien pathogens and parasites on the paper provides insights into a less-considered aspect of native freshwater fishes of southern Australia. It has alien trout species impacts—that of disease and parasites. provided confirmed and likely causes for extinctions of native freshwater fish species and extirpations of An extremely significant Murray-Darling-

local populations, in addition to probable vectors of Basin-wide epizootic of Maccullochella peelii in 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 these pathogens and parasites. This has been particularly 1929–30 is detected in the historical literature and reported illuminating for native fish of the Murray-Darling Basin in the scientific literature for the first time. M. peelii has had and their current conservation status. a multi-stepped decline since European settlement (e.g. Rowland 2005) and the 1930s was clearly one of those steps The accumulated evidence supports the proposition that or increments of decline. The sharp decline of M. peelii that alien pathogens and parasites have played a greater role became apparent in the 1930s was well-recognised by the in historical declines/extinctions of specific native fish populace, and was the subject of many newspaper letters populations than previously realised. Many of the alien and articles in that decade (TROVE 2020). The 1929–30 pathogens and parasites listed in Table 1 are inferred epizootic was likely a significant contributor to the species’ or documented to have caused historical impacts and declines in the 1930s. Similarly, the 1930s were a significant epizootics of naïve Australian native freshwater fish step or increment in the decline of Maccullochella ikei in the species. Dramatic population extirpations and species Clarence River Basin and there is some evidence to suggest extinctions of native fish in more recent times are that the 1929–30 epizootic may have been one of several putatively linked to alien pathogens and parasites using contributors to that decline. Both were the inevitable multiple lines of evidence. Of the various types of result of upper reach stockings of vectoring alien trout pathogen and parasite analysed, it appears that alien species (Oncorhynchus mykiss and Salmo trutta), which were oomycetes have had the greatest impacts in the past, incessant in streams of southern Australia from the early while alien viruses and fungal and fungal-like pathogens 1900s onwards and continue unabated today, including in pose the greatest threat into the future. It is suspected endangered Macquaria australasica habitats. that some of the more historical introductions of alien pathogens and parasites are still having significant The vast numbers of alien fish that are imported into impacts on native fish individuals and populations today. Australia each year for the aquarium/ornamental sector There is strong evidence for this with the alien parasites pose a grave threat to Australian waterways and native Lernaea cyprinacea and Chilodonella hexasticha, while the fish. Disease detection and quarantine is difficult and impacts of Saprolegnia parasitica requires more research. problematic and it is clear that alien pathogens and Climate change and over-extraction are major stressors parasites can and do get through (e.g. DGIV/ISKNV). to our river systems, and will exacerbate the already Similarly, many alien fish species posing a significant significant impact of L. cyprinacea and C. hexasticha, and invasion risk are allowed in due to historical precedence fish pathogens and parasites in general. rather than individual assessments of actual risk. While some pre-import risk assessments and biosecurity There is overwhelming evidence for alien trout species measures have improved in recent times (e.g. DoA, 2014), (Oncorhynchus mykiss and Salmo trutta) being the initial evidence strongly indicates they remain inadequate. and primary vector of some key pathogens and parasites, Many new alien fish species—and a proportion of their with indisputable subsequent severe impacts on native pathogens and parasites—continue to establish in the freshwater fish species. Hatchery breeding and stocking wild in Australian freshwater systems from deliberate and of alien trout species (O. mykiss and S. trutta) have accidental releases of aquarium trade species (Lintermans spread alien pathogens and parasites across Tasmania 2004). It is clear that, in addition to strengthening pre- and southern Australia. This includes S. parasitica and import risk assessments and biosecurity measures in this Ichthyophthirius multifiliis, and likely other ‘cosmopolitan’ sector, there is an urgent need for enhanced public and Northern Hemisphere pathogens and parasites such as industry education. L. cyprinacea and C. hexasticha. Alien Cyprinus carpio are also strongly implicated in the spread of L. cyprinacea in This paper has demonstrated the great value of historical lowland habitats of the Murray-Darling Basin while alien evidence in interpreting and providing context to past Perca fluviatilis are implicated in the spread of alien EHNV declines and extirpations of native freshwater fish. in the same Basin, though a possible role for alien O. mykiss Numerous severe epizootics linked to alien pathogens and in this spread is also noted. Of great concern is that the parasites were documented, and a completely forgotten/ impacts of alien trout species (O. mykiss and S. trutta) and overlooked epizootic unearthed using historical evidence. their incessant stocking on native freshwater fishes, frogs, In addition, the geographic and temporal spread of crayfish and remains a grossly understudied field. Saprolegnia parasitica in southern Australian freshwaters Australian 2020 Zoologist Q Kaminskas has been partially elucidated using historical evidence for for native fish and Aphanomyces astaci for native crayfish. the first time. This paper also demonstrates that historical The probability of an alien pathogen or parasite entering evidence provides context to the current conservation Australia and having the same catastrophic impacts on situation of many native fish species, for example by native fish or native crayfish as alien chytrid fungus has had leading to questions such as: on native frogs is disturbingly high. To avoid this scenario, Australians and all levels of Australian government need • what are the current impacts of long-established alien to start addressing these challenging risks. Australia’s pathogens and parasites? and, distinctive and charismatic native freshwater fish fauna, and its cutlural, social and economic values, cannot be

• what future pathogen and parasite threats may be denied and must be valued and prioritised for protection. 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 imminent? The alternative is to continue on the present pathway, resulting in ongoing loss of native fish fauna and ongoing Finally, this paper clearly demonstrates that for close to 150 biological degradation of waterways. A striking statistic years, Australia has been on a pathway of steady invasion is that alien fish already comprise approximately 80% or of our freshwaters by alien fish species and their pathogens more of fish populations in most reaches of Australia’s and parasites. Yet, there remains a noticeable lack of iconic and socio-economically critical Murray-Darling action or reform effective enough to halt this process or Basin (Davies et al. 2012). Significantly, and perhaps to set us on a new pathway, despite repeated calls to arms catastrophically, this may become 100% in the not-too- (e.g. Pollard and Burchmore 1986). Extreme risks remain, distant future if the risks and impacts of alien fish and such Megalocytivirus species and Sphaerothecum destruens their pathogens and parasites continue unabated.

Acknowledgements

This report incorporates a literature review carried out paper, and her subsequent encouragement, support and by the author for the 2012 listing of Bidyanus bidyanus proof-reading. I sincerely thank my current Director as threatened under the Australian Commonwealth Dr Michael Wilson for his support. I thank Ms Belinda Environment Protection and Biodiversity Conservation Act Stewart for kindly providing me with an image of the 1999 (EPBC Act). During this time I had the pleasure Kangaroo River, and Ms Erin Lake for providing an of working with the late Dr Keith Walker, and I wish to image of Shoalhaven Macquaria australasica. I thank my acknowledge the kind mentoring and encouragement partner, family, friends and colleagues for their support I received from him for my academic endeavours. He and encouragement. I also thank the anonymous reviewer is fondly remembered. I am indebted to my colleague of the first submission and their constructive, highly Dr Gina Newton for spurring me into writing this beneficial review.

References

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Queanbeyan Observer. 1896. Tuesday 11 August, page 2. The Rowland, S.J. 2005. Overview of the history, fishery, biology, Fish Disease. Available online at: http://nla.gov.au/nla.news- and aquaculture of Murray cod (Maccullochella peelii peelii). article240005093 [Accessed: 21 January 2020]. In: Lintermans, M. and Phillips, B. (eds) 2005. Management of Murray cod in the Murray Darling Basin: Statement, Queanbeyan Observer. 1905. Friday 8 September, page 2. Recommendations, and Supporting Papers. Murray Darling Piscatorial. Our Trout Streams. How They Were Stocked. Basin Commission, and Cooperative Research Centre for Available online at: http://nla.gov.au/nla.news-article235459905 Freshwater Ecology, Canberra Pp. 38–61. [Accessed: 18 August 2020]. Rowland, S.J. 2009. Review of Aquaculture Research and Raadik, T.A. 2014. Fifteen from one: a revision of the Development of the Australian Freshwater Fish Silver Perch, Galaxias olidus Günther, 1866 complex (Teleostei, Galaxiidae) Bidyanus bidyanus. Journal of the World Aquaculture Society 40: in south-eastern Australia recognises three previously described 291–324. https://doi.org/10.1111/j.1749-7345.2009.00252.x taxa and describes 12 new species. Zootaxa 3898: 001–198. Available online at: https://www.biotaxa.org/Zootaxa/article/ Rowland, S.J. 2011. Personal communication by email: view/zootaxa.3898.1.1 effects of Aphanomyces invadans on Australian fish species. 14 November 2011. Grafton Fisheries Centre, Department of Read, P., Landos, M., Rowland, S.J. and Mifsud, C. 2007. Primary Industries, Grafton, NSW. Silver Perch Diseases Manual. NSW Department of Primary Industries, Orange, NSW, Australia. Rowland, S.J. and Ingram, B.A. 1991. Diseases of Australian native freshwater fishes with particular emphasis on the Register. 1915. Tuesday 14 December, page 4. Tasmanian ectoparasitic and fungal diseases of Murray cod (Maccullochella Fishing. Available online at: http://nla.gov.au/nla.news- peeli), golden perch (Macquaria ambigua) and silver perch article59983528 [Accessed: 21 January 2020]. (Bidyanus bidyanus). NSW Fisheries, Sydney, NSW.

Register News-Pictorial. 1929. Saturday 26 October, page Rowland, S.J., Landos, M., Callinan, R.B., Allan, G.L., 3. Big Fish Loss on Murray. Poison in Backwaters May Have Read, P., Mifsud, C., Nixon, M., Boyd, P. and Tully, P. 2007. Caused Deaths. http://nla.gov.au/nla.news-article53443956 Development of a Health Management Strategy for the Silver [Accessed: 27 August 2020]. Perch Aquaculture Industry. NSW Department of Primary Industries, Cronulla, NSW. Rezinciuc, S., Sandoval-Sierra, J.V., Ruiz-León, Y., van West, P. and Diéguez-Uribeondo, J. 2018. Specialized attachment Sandoval-Sierra, J.V., Latif-Eugenin, F., Martín, M.P., Zaror, L. structure of the fish pathogenic oomycete Saprolegnia parasitica. and Diéguez-Uribeondo, J. 2014. Saprolegnia species affecting PLoS ONE 13: e0190361. https://doi.org/10.1371/journal. the salmonid aquaculture in Chile and their associations with pone.0190361 fish developmental stage. Aquaculture 434: 462–469. http:// dx.doi.org/10.1016/j.aquaculture.2014.09.005 Riverine Grazier. 1930. Tuesday 8 April, page 1. Doings in Different Districts. Available online at: http://nla.gov.au/nla. news-article136772413 [Accessed: 27 August 2020].

Australian X Zoologist 2020 Native fish pathogens

Saville-Kent, W. 1887. On the acclimatisation of the salmon Sydney Morning Herald. 1906. Wednesday 3 January, page 6. (Salmo salar) in Tasmanian waters, and upon the reported Australian Grayling. Available online at: http://nla.gov.au/nla. disease at the breeding establishment on the River Plenty. news-article14731541 [Accessed: 21 January 2020]. Papers and Proceedings of the Royal Society of Tasmania 1887: 54–66. Available online at: https://eprints.utas.edu.au/15662/ Threatened Species Scientific Committee (TSSC). 2012. [Accessed: 30 January 2020]. Conservation Advice for Bidyanus bidyanus (Silver Perch). Available online at: http://www.environment.gov.au/biodiversity/ Schaerf, K. 2020. Personal communication by phone and email: threatened/species/pubs/76155-conservation-advice.pdf Chilodonella epizootic of Murray cod (Maccullochella peelii) and [Accessed: 21 January 2020].

catfish (Tandanus tandanus) in the upper Macquarie River and 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 tributaries in 1982 and its impacts. Threatened Species Scientific Committee (TSSC). 2015. Conservation Advice for Maccullochella ikei (Eastern Freshwater Scott, A.L. and Grizzle, J.M. 1979. Pathology of cyprinid fishes Cod). Available online at: http://www.environment.gov.au/ caused by Bothriocephalus gowkongensis Yea, 1955 [synonym biodiversity/threatened/species/pubs/26170-conservation- of B. acheilognathi] (Cestoda: Pseudophyllidea). Journal of Fish advice-01102015.pdf [Accessed: 21 January 2020]. Disease 2: 69–73. https://doi.org/10.1111/j.1365-2761.1979. tb00141.x Tilzey, R.D.J. 1977. Key factors in the establishment and success of trout in Australia. Proceedings of the Ecological Society Shariff, M., Kabata, Z. and Sommerville, C. 2006. Host of Australia 10: 97–105. susceptibility to Lernaea cyprinacea L. and its treatment in a large aquarium system. Journal of Fish Diseases 9: 393–401. https://doi. Tonkin, Z., Stuart, I., Kitchingman, A., Thiem, J.D., Zampatti, org/10.1111/j.1365-2761.1986.tb01032.x B., Hackett, G., Koster, W., Koehn, J., Morrongiello, J., Mallen-Cooper, M. and Lyon, J. 2019. Hydrology and water Skerratt, L.F., Berger, L., Speare, R., Cashins, S., McDonald, temperature influence recruitment dynamics of the threatened K.R., Phillott, A.D., et al. 2007. Spread of chytridiomycosis has silver perch Bidyanus bidyanus in a regulated lowland river. Marine caused the rapid global decline and extinction of frogs. EcoHealth and Freshwater Research: https://doi.org/10.1071/MF18299 4: 125–134. https://doi.org/10.1007/s10393-007-0093-5 Torchin, M.E., Lafferty, K.D., Dobson, A.P., McKenzie, V.J. Small, K., Kopf, R.K., Watts, R.J. and Howitt J. 2014. and Kuris, A.M. (2003). Introduced species and their missing Hypoxia, Blackwater and Fish Kills: Experimental Lethal Oxygen parasites. Nature 421: 6 February 2003. Pp. 628–630. https://doi. Thresholds in Juvenile Predatory Lowland River Fishes. PLoS org/10.1038/nature01346 ONE 9: e94524. https://doi.org/10.1371/journal.pone.0094524 TROVE. 2020. National Library of Australia. Available Sporting Globe. 1929. Saturday 9 February, page 5. Fish and online at: https://trove.nla.gov.au/search/advanced/category/ Fishers. Trout Mortality at Eildon. Available online at: http:// newspapers [Accessed: 22 July 2020]. nla.gov.au/nla.news-article183976339 [Accessed: 31 July 2020]. Trueman, W.T. 2011. True Tales of the Trout Cod: River Steffen, W., Vertessy, R., Dean, A., Hughes, L., Bambrick, H., Histories of the Murray-Darling Basin. MDBA Publication No. Gergis, J. and Rice, M. 2018. Deluge and Drought: Australia’s 215/11. Murray-Darling Basin Authority, Canberra. Available Water Security in a Changing Climate. Climate Council of online at: https://finterest.com.au/wp-content/uploads/2020/01/ Australia, Ltd. Available online at: https://www.climatecouncil. True_tales_of_the_trout_cod_book.pdf [Accessed: 11 org.au/wp-content/uploads/2018/11/Climate-Council-Water- September 2020]. Security-Report.pdf [Accessed: 29 January 2020]. Uribeondo, J., Cerenius, L. and Söderhäll, K. 1994. Repeated Sunday Times. 1906. Sunday 7 January, page 3. Fishing zoospore emergence in Saprolegnia parasitica. Mycology Research Resorts. Cucumber Mullet. Available online at: http://nla.gov. 98: 810–815. https://doi.org/10.1016/S0953-7562(09)81060-5 au/nla.news-article126568479 [Accessed: 21 January 2020]. van Den Berg, A.H., McLaggan, D., Diéguez-Uribeondo, Sunshine Advocate. 1937. Friday 17 December, page 13. J. and van West, P. 2013. The impact of the water moulds Angling. Available online at: http://nla.gov.au/nla.news- Saprolegnia diclina and Saprolegnia parasitica on natural ecosystems article75198908 [Accessed: 31 July 2020]. and the aquaculture industry. Fungal Biology Reviews 27: 33–42. https://doi.org/10.1016/j.fbr.2013.05.001 Sydney Mail and New South Wales Advertiser. 1876. Saturday 27 May, page 691. Passing Events. Available online van West, P. 2006. Saprolegnia parasitica, an oomycete pathogen at: http://nla.gov.au/nla.news-article162649794 [Accessed: 12 with a fishy appetite: new challenges for an old problem. Mycologist August 2020]. 20: 99–104. https://doi.org/10.1016/j.mycol.2006.06.004

Australian 2020 Zoologist Y Kaminskas van West, P. 2011. Personal communication by email: Whittington, R.J., Kearns, C., Hyatt, A.D., Hengstberger, international distribution of Saprolegnia parasitica and Saprolegnia S. and Rutzou, T. 1996. Spread of epizootic haematopoietic diclina. 4 November 2011. Aberdeen Oomycete Laboratory, necrosis virus (EHNV) in redfin perch (Perca fluviatilis) in University of Aberdeen, Scotland, UK. southern Australia. Australian Veterinary Journal 73: 112–114. https://doi.org/10.1111/j.1751-0813.1996.tb09992.x Weekly Times. 1910. Saturday 7 May 1910, page 19. Fishing. Online at: https://trove.nla.gov.au/newspaper/article/221810431 Whittington, R.J., Philbey, A., Reddacliff, G.L. and MacGown, [Accessed: 31 July 2020]. A.R. 1994. Epidemiology of epizootic haematopoietic necrosis virus (EHNV) infection in farmed rainbow trout, Oncorhynchus

White, A.W. and Pyke, G.H. 2011. World War II and the mykiss (Walbaum): findings based on virus isolation, antigen 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 rise of the plague minnow Gambusia holbrooki (Girard, 1859) capture ELISA and serology. Journal of Fish Diseases 17, 205– in Australia. Australian Zoologist 35: 1024–1032. https://doi. 218. https://doi.org/10.1111/j.1365-2761.1994.tb00216.x org/10.7882/AZ.2011.057 Whittington, R.J., Reddacliff, L.A., March, I., Kearns, C., Whittington, R.J. and Chong, R. 2007. Global trade in Zupanovic. Z. and Callinan, R.B. 1999. Further observations ornamental fish from an Australian perspective: The case for on the epidemiology and spread of epizootic haematopoietic revised import risk analysis and management strategies. Preventive necrosis virus (EHNV) in farmed rainbow trout Oncorhynchus Veterinary Medicine 81: 92–116. https://doi.org/10.1016/j. mykiss in south-eastern Australia and a recommended sampling prevetmed.2007.04.007 strategy for surveillance. Diseases of Aquatic Organisms 35: 125–130. https://doi.org/10.3354/dao035125 Whittington, R.J., Becker, J.A. and Dennis, M.M. 2010. Iridovirus infections in finfish—critical review with emphasis on ranaviruses. Journal of Fish Diseases 33: 95–122. https:// doi:10.1111/j.1365-2761.2009.01110.x

Postscript As this paper was being published, Shamsi et al. (2020) reported a new alien fish parasite for Australia, Dermocystidium sp., recovered from Maccullochella peelii in a hatchery in south-eastern Australia. Shamsi, S., Xiaocheng, Z., Barton, D.P., Dang, M., Freire, R. and. Nowak, B.F. 2020. Dermocystidium sp. infection in farmed Murray cod, Maccullochella peelii. Aquaculture 528: 15 November 2020, 735596. https://doi.org/10.1016/j. aquaculture.2020.735596

Australian Z Zoologist 2020 Native fish pathogens

Historical accounts of Saprolegnia parasitica outbreaks in Australian native freshwater fish in Tasmania and the Australian mainland. Note for the first 3 records the typical pattern of Saprolegnia striking in winter when fish immune systems are weakest (winter saprolegniosis). 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 APPENDIX 1 —in plain English, a fungus. The mortality immediate of our own in the fish a fungus. —in plain English, Description An extraordinary black fatal disease has made its appearance amongst the Murray cod, principally It affects large days. river within the last few bream and perch in the Queanbeyan Numbers within the vicinity of found were in weight. to the 2lb. down from 4lb. fish, The Fisheries Commissioners fish suspect the cause is a fungus … two dying and dead. town inflamed gills and a thick membranous disclose highly on the lower growth examined today 1895) (Goulburn Post lip. but in and around Queanbeyan, not only A great deal of concern is not unnaturally excited, the discovery by the Fisheries of a strange inhabitingby Commissioners, fatality amongst fish the end Towards the waters in the immediate vicinity of town. River of the Queanbeyan dead in the deep waters was found about forty weighing pounds, cod, a fine of last week Reuben Moore Last Sunday, forming and Molonglo Rivers. the junction of Queanbeyan varying from six to ten pounds, eight or ten cod, men found other young and one or two Information of as the Egg-holes. known Queanbeyan floating dying or dead at a place above reached the Fisheriesthe discovery Commissioners seems to have … as they apprehended A close examination of those specimens … fungus in the head as cause of mortality. and on up-lifting the gill-covers… disclosed a leathery a membranous on the lips, growth in the upper partslarge extent of inflammation the gills was perceptible, destroying entirely … and giving the gills appearancethe structure, of a pinkish pus. Observer(Queanbeyan 1895a) inhabiting the watersThe disease in fish as river has been defined of the Queanbeyan ferax Saprolegnia and the disease is becoming more neighbourhood is greater than was at first imagined, All these perch and bream similarly … affected cod, found malignant … Other persons have been made in the waters and Molonglo rivers of the Queanbeyan have discoveries close to … since the outbreak here intelligence has reached us that disease made itstown appearance in some of the northern and western rivers Observer … (Queanbeyan 1895b) , , , , Bidyanus Bidyanus Maccullochella Maccullochella Maccullochella , , Maccullochella peelii Maccullochella peelii Maccullochella peelii, Species Murray cod trout cod possibly macquariensis bream [Macquarieblack perch] Macquaria australasica perch] perch [silver bidyanus Murray cod trout cod possibly macquariensis Murray cod trout cod possibly macquariensis bream [Macquarieblack perch] Macquaria australasica perch] perch [silver bidyanus State/ Territory NSW NSW ACT and NSW ACT and Location River Queanbeyan River Queanbeyan Molonglo River ‘northern and western rivers’ Date 1 August 1895 2 August 1895 9 August 1895

Australian 2020 Zoologist AA AA Kaminskas 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 APPENDIX 1 ; and from the number of dead fish seen in the locality, seen in the locality, of dead fish and from the number ; saprolegnia ferax saprolegnia Description small Murray two last night, brought to our office Urayarra mail contractor, Phillips, H. Mr G. amongst numbers of others dead in the Murrumbidgee which had been found, River cod, evidence of the presence Both specimens exhibit unmistakeable near the Urayarra Punt. as the disease known the and gills, about the fins all of them exhibiting the fungoid growths from 2lb downwards, the information should be thankful to receive of this fish We be verydisease must prevalent. Observer (Queanbeyan elsewhere in rivers if discovered 1896) of the district. epidemic, Valley It is plentiful in the Kangaroo Australia a trout. for grayling … is often mistaken The The and Queensland [sic] … Tasmania and in in the tributaries of the Shoalhaven, waters, The grayling sometimes visits the sea, name of the species is prototoctes maraena. scientific Some years such as saprolegnia ferax. in order to rid itself of parasitical or fungal annoyances, and at ago the presence of this disease was noted amongst our indigenous fresh-water fish, (Sydney Morningthat time the graylings and perch perished Herald in great numbers. 1906) Cox’s Valley, Burragorang Valley, visitors to the Kangaroo CUCUMBER MULLET.—Recent report and the upper Shoalhaven variously styled cucumber mullet, the capture of , Australian grayling (Prototroctes maraena) are really The fish locals. and trout by herring, Yarra being a delicate and but floods, when assisted by The grayling goes to sea occasionally, … the perch, like Sometimes, in a freshwater river years. for happily will live contented species, … (Sunday called saprolegnia ferox. fungoid growth a mucous by the graylings are attacked Times 1906) During days the last few Thursday. AMONGST FISH.—Sydney, MYSTERIOUS MORTALITY there has been a mysterious mortality near Canberra. River in the Queanbeyan amongst fish and Hawks a report. for analyst to the Government been forwarded have Some of the fish congregated in large and are devouring the dead fish. numbersother birds have on the scene, 1908) (Age, come upstream in shoals. Fish have mortality place as to the cause of heavy FISHING.—Much speculation has taken amongst as far the stream and, been seen floating down lately have Shoals of dead fish, Yarra. in the fish their death has not been traced of the parasitical to any diseases to which fish as is known, 1910) Times, … (Weekly are subject. , Maccullochella Prototroctes Prototroctes Maccullochella peelii Species Murray cod trout cod possibly macquariensis Australian grayling maraena Australian grayling maraena fish fish State/ Territory ACT NSW NSW NSW Victoria Location Upper Murrumbidgee River Kangaroo River River Shoalhaven Kangaroo River BurragorangValley/ River Cox’s River Shoalhaven River Queanbeyan River Yarra Date 11 August 1896 3 January 1906 7 January 1906 6 March 1908 1910 7 May

Australian AB Zoologist 2020 Native fish pathogens 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 APPENDIX 1 Description An extraordinary epidemic is reported Mortality the blackfish attacked Amongst Fish. to have It is also are to be seen. some up to 4lb in weight, Hundreds of dead fish, River. Tarwin in the is noted throughout Tarwin The with the disease. stated that eels are also becoming affected A report of the inspector Fisheries with is awaited …. blackfish Gippsland as a stream for 1918) (Argus, interest. much DISAPPOINTED. FISHING PARTIES SINGULAR DISEASE, Die in Hundreds. Blackfish River. Tarwin An extraordinary in the the blackfish epidemic has attacked Monday. Meeniyan, Johnstone of Meeniyan, Constable last, Just about the opening of season on Monday and then wired for He made an inspection, noticed. were was informed dead fish that many and with Mr. of the Fisheriesan officer Inspector Clift was sent to Meeniyan, department. hundreds of dead blackfish, They found made a careful investigation. Hamilton of the hotel, The mortality been Such an epidemic has never was enormous. some up to 4lb weight. similarly suffered in a have though it is said that catfish in a running before known stream, well Two … with the strange It is also stated that eels are becoming affected disease. lake. a graphic … supply account of the Wonthaggi and Roadley of Yardley Messrs. anglers, known every but where there a mile they tested the river, extraordinary For over phenomenon. enthusiastic angler to secure, the delight of any Fine large specimens, dead and dying fish. were in a dying condition. almost on top of the water, stream, down seen floating or wobbling were others but that flax is the cause, some say as to the cause of disease, Opinions differ it is anticipated that the whole of fish and if this is so, consider that it is due to a fungus, Express (Powlett The report of the Inspector Fisheries awaited. is anxiously will be attacked. 1918) Advertiser, Victorian State Coalfields and Disease in Blackfish. there has been some epidemic which practicallyDuring weeks wiped out the past few which runs through Mirboo Tarwin The mortality in the from district streams. the blackfish fishermen report as numerous not getting a biteSouth and Dumbalk has been indeed great, especially been seen dead, Fish in hundreds have after tryingfrom blackfish several for days. Tarwin been noticed in the understand have dead fish We Dumbalk and Meeniyan. between which seems to been practically nothing, The catches there have Allambee. which runs from that the disease has been in full swing stream. prove 1919) Advertiser, (Morwell , , Anguilla australis Anguilla australis Gadopsis marmoratus Gadopsis marmoratus Gadopsis marmoratus Species river blackfish eel [shortfinned] river blackfish eel [shortfinned] river blackfish State/ Territory Victoria Victoria Victoria Location River Tarwin River Tarwin River Tarwin Date 20 December 1918 20 December 1918 10 January 1919

Australian 2020 Zoologist AC AC Kaminskas Weir Weir

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 APPENDIX 1 Darlingford and were covered with a grey coloured Darlingford covered and were Description Angling. “PISCATOR”. By Mortality Among Blackfish. be recalled that in the springIt may of 1918 a mysterious and widespread mortality was were fish hundreds of the native Gippsland, River, Tarwin In the noted among blackfish. no satisfactory but observed explanation of stream and strewn along the banks, floating down that the death rateAt the time it was feared the actual cause of death has been vouchsafed. This belief would had been so high that the stream practically cleared of blackfish. report lately Tarwin as several parties tried the who have founded, been well appear to have (Herald, been hooked. have no blackfish odd specimens of light weight that other than a few 1920) TOO THE IN GELLIBRAND, which Another stream in which destruction is causing concern of fish in the Gellibrand River, hundreds Reports weeks that in the past few been received runs have through Beech Forest. … (Sporting been floating to the surface. Globe, and [alien] trout have of dead blackfish 1929) reportsContinued of diseased Macquarie perch in the upper reaches of Eildon are causing the Fisheries specimens to 3 and Game department Last week concern. grave from the water at taken were weight lb. similar reports have a lesser extent, To consumption. for unfit being totally the fish fungus, 1937). Advocate, (Sunshine from the Big River. been received … It was reported delegates at the Piscatorial two Councils meeting that Macquarie by perch floating in the Delatite and Goulburn found arms were of Eildon weir. to 4lb. ranging from 1lb. and in a helpless condition at first numerous sight appeared to be injured. were The fish marksThere were scars not unlike on from the water they died immediately. When taken rapidlyafflicted with a fungoid decomposed it was thought that they were As the fish the fish. Members of the council are unanimous that an earlyis necessarydisease. investigation to find 1937) (Argus, the cause of trouble. Macquaria Macquaria Gadopsis marmoratus Gadopsis marmoratus Species river blackfish river blackfish Macquarie perch australasica Macquarie perch australasica State/ Territory Victoria Victoria Victoria Victoria Location River Tarwin Other waterways? Gellibrand River Eildon Weir Big River Eildon Weir Date 7 February 1920 9 February 1929 17 December 1937 18 December 1937

Australian AD Zoologist 2020 Native fish pathogens

Records of the 1929–30 Murray Cod Maccullochella peelii epizootic. 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 APPENDIX 1 2 Key Passages Key states that large numbers“Fisherman” of cod and perch are dying in the He asks me if from some disease. apparently reaches of Upper Clarence River, I will bring the matter under notice of Fisheries with the Department, and to sent to the district an investigation an officer to make object of having ascertain what is the cause of mortality which is depleting the streams of … fish to cod but confined world been merely The sickness in the fish has not yet bream and jew … extends to bony including some big cod have largeDuring weeks numbers the past few of fish, This strange not limited to happening is apparently died in the . A strange malady is reported George … in the Condamine, among fish St. … is the method to capture Novel resulting in their dying numbers. the surface of cod floating just below not quite inanimate, but almost, water … The DarlingWilcannia. presents a sorry River miles on either side of aspect for Large numbers on its banks or floating down of dead Murray are laying codfish Experienced fishermen are at They vary from 1 lb to 40 lb. in size the stream. that cod caught in the nets die within and say the deaths, a loss to account for half an hour after being tethered. been seen floating have of dead fish Tuesday.—Numbers (N.S.W.), ALBURY include The fish on their backs the surface of water in Hume Reservoir. One theory in the debris been suffocated have is that the fish cod and bream. is the fact however, Against this, collected against the wall on upstream side. wall, about the weir been seen floating hundreds of yards have fish that many It is stated that similar mortalitywhere there is no debris. has been among fish noted in other reservoirs when the storing of the water has begun. , , Tandanus Tandanus Macquaria Maccullochella , Species Cited eastern freshwater cod ikei perch [Australian bass] novemaculeata Murray cod Maccullochella peelii bream bony Nematalosa erebi jew [catfish] tandanus Murray cod Maccullochella peelii Murray cod Maccullochella peelii Murray cod Maccullochella peelii State or Territory NSW QLD QLD NSW NSW Locations Cited Upper Clarence River , Warwick, Lyndhurst Balonne River, Condamine River, St George, Warwick, Lyndhurst Darling River, Wilcannia Hume Reservoir Article Title Inquiry Requested— Cause of Fish Dying in the Upper Clarence AmongMalady Fish AmongSickness Fish District News Hume Reservoir. Mysterious Mortality Amongst Fish Paper Farmer and Settler (Sydney) Brisbane Courier Balonne Beacon Mudgee Guardian and North- Western Representative ArgusThe Date 7 June 1929 August16 1929 August22 1929 20 September 1929 2 October 1929

Australian 2020 Zoologist AE AE Kaminskas 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 APPENDIX 1 2 Key Passages Key cause, from some inexplicable and varieties of all sizes are, Thousands of fish Australian portiondying in the South of the Upper Murray … Australian and varieties of all sizes are dying in the South Thousands of fish portion Lock 4 …Steamer Lock 6 to below of the Upper Murray from above never years that they have been on the rivermany say for officers who have river periods dead cod in the main stream low seen so many in the past. … misfortune industry to the fishing Murray dying on the River through fish cause … On practicallyin shoals from some unknown the full length of the direful phenomenon of Mildura Mannum, to below from above Murray, and from in shoals, not as isolated instances but can be witnessed, dead fish and before, seen the like never captains have River in weight. to 80 lbs. 5 lbs. All sorts point of view the position is very of reasons have from a fish serious. been attributed the disaster … for speaking. comparatively the river has stopped, down of dead fish The flow fishermen claim are which, There has been an enormous depletion of the fish, Several large the writer cod inspected by nearly bear this out—each, all female. or roe as they are more properly “eggs” the “postmortem” showed a following the bad water for A high authority in this state … blames on fishing known. trouble. and Renmark, above about 26 miles Clair is camped near Chowilla, Mr St. stream past his states than in 24 hours pass down more dead fish he saw caught in 12 months … hundreds of pounds worthhouse than he has ever of mortality the sudden and heavy been lost by among cod and boney have fish also died and these have in the river is the catfish, The hardiest fish brim [sic]. Clair noticed one large with part fish … Mr St. of its bladder in large numbers. one morning and Another fisherman … awoke … sticking out of its mouth. them full of He opened some and found 28 dead cod close to his camp. saw dead in every fish many along a back water and saw Then he walked slime. direction. , , , , Tandanus Tandanus Species Cited Murray cod Maccullochella peelii all varieties [of fish] Murray cod Maccullochella peelii all varieties [of fish] Murray cod Maccullochella peelii Murray cod Maccullochella peelii Murray cod Maccullochella peelii bream bony Nematalosa erebi catfish tandanus State or Territory South Australia South Australia South NSW, Australia South Australia South Australia Murray River, Renmark, 6 5, Locks 4, Murray River, Mildura, Mannum Murray River, Loxton, Cobdogla Murray River, Chowilla, Renmark Locations Cited Murray River, Renmark, 6 5, Locks 4, Article Title Death Of Fish— Serious Losses on Murray Big Fish Loss on Murray—Poison in Backwaters Have May Caused Deaths Fish Die In Shoals Wholesale Death Of River Fish—Alarming Occurrence Attributed to Causes Various The Dying Fish Paper Chronicle (Adelaide) Register News-Pictorial (Adelaide) Bunyip SA) (Gawler, Murray Pioneer and Australian Record River SA) (Renmark, Murray Pioneer and Australian Record River SA) (Renmark, 26 October 1929 1 November 1929 1 November 1929 8 November 1929 Date 25 October 1929

Australian AF Zoologist 2020 Native fish pathogens 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 APPENDIX 1 2 Key Passages Key been made to the great have several references Sir—in the Register recently, back water, to locks, and this is put down dying in the Murray, of fish number the cause of death. go a lot deeper than this for must We and salt water. been dying for are and have up to large cod, of all kinds, Thousands of fish There are Wilcannia and Bourke. between several months in the upper Darling, no locks and backwaters in these parts to cause the trouble. Fisheries Department Concerned. at reports“Argus”, from places received states yesterday’s Game Department, on the Murray and its tributaries of the deaths hundreds Murray cod. persons floating on the surface of water by been found have The dead fish Reports of similar Albury. living in places as far apart Nagambie and as Mildura, the Department by been received occurrences have Fisheries from the and fishermen on where the professional Game DepartmentAustralia, of South the Murray perturbed are greatly … Mr Lewis pointed out that the deaths such a wide area as to suggest that serioushad occurred epidemic of over It appeared to be affecting some disease was taking place among Murray cod. all the waters and it might assume serious of the Murray and its tributaries, … proportions if not checked. officers concern by of the FisheriesGrave is felt states and Game Department, at reports“Argus”, from places on the Murray received and its yesterday’s been have The dead fish tributaries of the deaths hundreds Murray cod. persons floating on the surface of water by found living in places as far Reports of similar occurrences have Albury. apart Nagambie and as Mildura, the Department by been received from the Fisheries and Game Department fishermen on the Murray where the professional are greatly Australia, of South perturbed … As above , Species Cited Murray cod Maccullochella peelii of all kinds fish Murray cod Maccullochella peelii Murray cod Maccullochella peelii Murray cod Maccullochella peelii State or Territory NSW NSW, Victoria NSW, Victoria, South Australia NSW, Victoria, South Australia Murray and River tributaries Murray and River tributaries, Mildura, Nagambie, Albury, South Australia Murray and River tributaries, Mildura, Nagambie, Albury, South Australia Locations Cited Murray River, Darling River, Wilcannia, Bourke Article Title Wrong What’s The With Murray? Murray Cod Dying. There Is An Epidemic? Fish Dying— Epidemic Feared Fishing Notes Paper Observer (Adelaide) ArgusThe Riverine Herald (Echuca, Victoria) Australasian 20 November 1929 21 November 1929 30 November 1929 Date 9 November 1929

Australian 2020 Zoologist AG AG Kaminskas 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 APPENDIX 1 2 Key Passages Key Victorian Fisheries Department reports concerned is much over The received of the death large and its tributaries, from all parts of the Murray River, been seen floating on the surface have dead fish Many numbers of Murray cod. personsof the water by living in places as far apart Nagambie and as Mildura, in the even but been found, the dead fish in this State have Not only Albury. fishermen are and the professional Australian portionSouth of the Murray, is a complete mystery,” “The cause of the death fish perturbed. greatly “and I am very anxious Lewis), said the chief inspector of department (Mr. … Mr Lewis pointed out that to obtain all the information that I can about it.” such a wide area as to suggest that seriousthe deaths had occurred over It appeared to epidemic of some disease was taking place among Murray cod. all the watersbe affecting and it might assume of the Murray and its tributaries, serious proportions if not checked. and other parts… I am told that about the Nagambie weir of the Goulburn Murray are where so many dead the [alien] redfin [River] cod are being found … numerous Anglers trips who returned from fishing on the Murray… to Bendigo today At a district that the river in the Gunbower is strewn with dead fish. River washed upon were up to 45lb., weighing bend in the river more than 500 fish, that the mortality It was believed was due to some among the fish the banks. pollution of the stream on its higher reaches. Victoria passing through Bendigo from districts in NorthernTravellers … traversed the Murray by and its tributary speak of the alarming River streams, of The banks are litter with dead fish mortality in the bends of river. of fish returnedAnglers trips from fishing to the Murray who have state the all sizes. the impression of having given in the water, their frantic by movements fish, game and birds and they become an easy prey to the native “doped”, been … that frequent the river. Species Cited Murray cod Maccullochella peelii Murray cod Maccullochella peelii Murray cod Maccullochella peelii Other species? Murray cod Maccullochella peelii Other species? State or Territory NSW, Victoria, South Australia Victoria Victoria Victoria Locations Cited Murray and River tributaries, Mildura, Nagambie, Albury, South Australia Weir, Nagambie Goulburn River Murray River, District Gunbower Murray River, tributary streams Article Title Deaths Of Murray Cod About Redfin Dead Fish In Pollution Murray. Causes Mortality. Fish The In Alarming Murray. Anglers Mortality. Puzzled About Cause. Paper Standard Daily (Brisbane) ArgusThe ArgusThe ArgusThe Date 6 December 1929 December10 1929 28 January 1930 29 January 1930

Australian AH Zoologist 2020 Native fish pathogens 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 APPENDIX 1 2 Key Passages Key made into the mortality… Investigations in the Murray of the fish river show that the destruction to certain confined has been mostly river sections of The reports confirm the great districts. Torrumbarry and Gunbower in the mortality areas. in the affected of the fish and also the frantic movements and the stream, made along stretches of river down investigations … Police indicate that the conditions higher up from the scene of greatest mortality, the police that by It is believe are normal are concerned. as far the fish is but the mortality pollution of the water, is not due to any among the fish attributed to the use of explosives. who Clair, The mortality Mr Chas St. in the Murray in the codfish still continues. more dead has been engaged in that industrystates he saw 40 years, for caught than he has ever his house, by in 24 hours, pass downstream cod fish at least 200 he saw Within a three mile radius of his camp, in 12 months. The Murrumbidgee does not appear to … up to 70 lbs in weight dead fish, to the systematic work owing of the big fishing but extent, be suffering to any in that stream now. codfish few plants in the past there are but An Upper Copmanhurst correspondent states that serious consideration Around 1920, to re-stocking the Upper Clarence with cod. should be given which indicated that the conditions suited this type plentiful, cod were he says, Many died out suddenly. the fish Either from disease or polluted water, of fish. as perch such, Other fish floating dead on the top of water. found were are plentiful at present. and mullet Maccullochella ikei Species Cited Not specified— Murray cod however Maccullochella peelii been the have would principal species Murray cod Maccullochella peelii eastern freshwater cod State or Territory Victoria South Australia NSW Locations Cited Murray River, Torrumbarry District, District Gunbower Murray River, Renmark Upper Clarence River Article Title Mortality of Fish. Due to Use of Explosives. Destruction in Water-holes. Doings in DistrictsDifferent Cod Wants Re-introduced Paper ArgusThe Riverine Grazier (Hay, NSW) Daily Examiner (Grafton, NSW) Date 31 January 1930 April8 1930 1952

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