ABSTRACT

This collection addresses the complexities of water management and the impact of environmental developments such as dams, reservoirs and irrigation schemes on public health.The main focus of the book is on vector-borne diseases such as malaria, arboviruses (dengue and encephalitides) and snail- borne schistosomiasis. These are examined from a wide

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6 UNEP policy on reservoirs

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Environmental indicators of healthy water resources

2.1 The need for environmental indicators of water quality
ByRichard Pearson

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References

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waterbird populations and provide additional mosquito breeding habitats, which would be conducive to increased arbovirus activity (Stanley 1972; 1975). Indeed the potential problems were expected to become more acute as the population in the area increased with the development of Kununurra township and nearby farming activities, and with increased tourism and mining opportunities. More than sixty-five arboviruses have been isolated in tropical Australia, but only a few have been implicated in human disease (Mackenzie et al. 1994a). These include the flaviviruses Murray Valley encephalitis (MVE), Kunjin, Kokobera, Alfuy, Edge Hill and dengue; and the alphaviruses Ross River, Barmah Forest, and Sindbis (Mackenzie et al. 1994a; 1994b). With respect to the Ord River irrigation area, the most important of these viruses is MVE, the major cause of Australian encephalitis. MVE virus has a natural biocenose between waterbirds, particularly members of the order Ciconiiformes, and mosquitoes, particularly the fresh-water breeding species, Culex annulirostris. MVE virus is a member of the Japanese encephalitis serological complex of flaviviruses, and is more closely related to Japanese encephalitis virus than are the other Australian members of the complex (Kunjin, Kokobera, Alfuy and Stratford viruses).

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Little was known about MVE virus, its vertebrate hosts or its vectors before the establishment of the Ord River irrigation area. Early serological studies by Stanley and Choo (1961; 1964) on human sera collected in 1960 from Halls Creek in East Kimberley and Derby in West Kimberley had demonstrated that the virus was circulating in these areas. However, no clinical cases of encephalitis had been reported, which may have been due to the small human population in the region prior to 1960, to a lack of awareness by clinicians, to low virus carriage rates in mosquitoes, or to a combination of these factors. Similarly, no cases of encephalitis had been reported in the Northern Territory. The first clinical case of Murray Valley encephalitis (now known as Australian encephalitis) occurred in 1969 (Table 8.1), a fatal case that was acquired by a tourist south of the Ord River irrigation area (Cook et al. 1970). Only limited information was available on the mosquito species prevalent in the Ord River area before 1972, although Culex annulirostris, believed to be the major vector for MVE virus from studies carried out by Doherty and colleagues in north Queensland (Doherty et al. 1963), was found to be present (H. Paterson, personal communication to Stanley 1972), and was the dominant species (H. Paterson, personal communication to Stanley 1975). Thus prior to the completion of stage one of the Ord River irrigation area, serological evidence had been obtained to demonstrate that MVE virus caused subclinical human infections, but no clinical cases had been reported. Between the completion of stage one and stage two, the first clinical case of encephalitis was reported, and limited information on the mosquito fauna was obtained but without details of mosquito numbers or population dynamics. 8.3 Studies on Murray Valley encephalitis from 1972 8.3.1 Early studies, 1972—1976 A series of investigations on the ecology of MVE virus in the Ord River irrigation area and on the effect of the completion of the Ord River dam were initiated by Stanley and colleagues in 1972. The major components comprised: regular mosquito collections obtained just before and immediately after the wet season to determine the number and proportion of each species at different sites, and for isolation of viruses; serological studies of animals and birds to investigate their roles as possible vertebrate or reservoir hosts; and serological studies of the human population, both Caucasian and Aboriginal, to determine subclinical infection rates and to assess potential risks. These studies yielded a number of important findings which have provided the basis for much of our knowledge of MVE ecology in north-western Australia. The major findings were as follows. • Mosquitoes. Using live bait traps to collect mosquitoes, it appeared that there had been a significant increase in mosquito numbers since the construction of the diver-

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sion dam (Stanley 1979). Most of the species collected in the bait traps were those associated with permanent and semipermanent fresh water breeding sites, and the dominant species was Culex annulirostris, which accounted for over 70 per cent of the collections (Liehne et al. 1976a; Stanley 1979). Thus the major vector species for MVE virus was shown to be abundant in the Ord River irrigation area. The major mosquito breeding areas were in swampland adjacent to the diversion dam. Little breeding activity was found in the irrigation area probably due to the excessive use of insecticides applied by aerial spraying for controlling insect pests on cotton crops. However, cotton was discontinued as a crop in 1975, and an increased number of mosquitoes began to appear in 1976. • Viruses. Pools of mosquitoes were processed for virus isolation by intracerebral inoc-ulation of macerated mosquito supernatants into suckling mice. A total of 195 strains of 16 arboviruses were isolated from 1075 pools, of which 29 were identified as MVE virus and 21 as Kunjin virus. The majority of the isolates were made from Culex annulirostris (153 of 195 isolations), including 28 of 29 identified as MVE. Thus the overall virus isolation rate was high (18 per cent). For MVE virus from Culex annulirostris, 3.5 per cent of pools yielded virus at an approximate rate of 1 infected mosquito per 1459 uninfected mosquitoes (Liehne et al. 1976b; 1981). • Serological studies of animals and birds. All the early serological investigations employed the haemagglutination-inhibition (HI) assay. Cattle sera obtained from the Ord River irrigation area exhibited a high incidence of antibody to MVE virus (80 per cent positive), but the incidence declined to 37 per cent positivity in sera collected elsewhere in the Kimberley region (Liehne et al. 1976c). A very significant increase in the incidence of antibody to MVE was observed in cattle between 1972 and 1975 in the irrigation area and nearby cattle properties, with increases ranging from between 22 and 36 per cent to between 75 and 90 per cent (Stanley 1979). While the establishment of the irrigation area and the completion of the Ord River dam were undoubtedly responsible for some of this increase, it is probable that the very heavy ‘wet’ season rainfall in 1973–74 also contributed. • Of 335 sera collected from 31 avian species, 195 were found to have antibody to MVE virus. Although only a few species were sampled in moderate or large num-bers, it was interesting to note that the incidence of antibody was similar between waterbirds and non-waterbirds (56 and 59 per cent, respectively), and between differ-ent avian orders: Ciconiiformes (herons, egrets), 62 per cent; Anseriformes (ducks, grebes), 55 per cent; and Psittaciformes (parrots), 56 per cent, (Liehne et al. 1976c). • Human serological studies. A total of 441 human sera were collected in the Ord River area, of which 293 were from Caucasians and 148 from Aboriginals. A very high incidence of MVE antibodies was observed in the Aboriginal population, with 96 per cent of adults and 77 per cent of children exhibiting antibodies. In the Caucasian pop-ulation, the incidence of MVE virus antibodies was 53 per cent in adults and 24 per

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cent in children, but the length of residence in the Ord River area was an important determinant, with those who had lived in the area fewer than three years having a lower incidence (26 per cent) than those who had lived in the area for more than three years (64 per cent) (Liehne et al. 1976c). Thus these early results demonstrated that the mosquito density and bird numbers had increased since the establishment of the Ord River irrigation project, particularly around the diversion dam and Lake Kununurra, that the major mosquito vector of MVE virus was the predominant species Culex annulirostris, and that MVE virus was actively circulating in the area. However, the serological results must be treated with caution as the HI test cannot differentiate clearly between MVE and Kunjin viruses, and therefore a number of seroconversions may have been due to infection with the latter. Nevertheless, the results suggested that MVE virus may have become enzootic in the Ord River irrigation area. A single case of Australian encephalitis occurred in Kununurra in 1974; this was the last case of the 1974 epidemic that affected all Australian mainland states (Table 8.1). The first cases to be reported in the Northern Territory also occurred during the 1974 epidemic. 8.3.2 Studies carried out between 1977 and 1995 The early studies between 1972 and 1976 laid the foundation for the more detailed investigations of MVE virus ecology in north-western Australia that have been undertaken over the past twenty years. These investigations became increasingly important as cases of Australian encephalitis became more frequent, particularly with respect to surveillance methodology to enable early warnings to be given of impending epidemic activity and to understand the spread and possible persistence of the virus. In addition, the apparently ideal conditions for arboviral ecology in the Ord River irrigation area have made it essential to monitor for possible incursant mosquito vector species and viruses that could potentially become established in the region. Improved methods for mosquito collection, virus isolation, and antibody detection have been introduced over the past twenty years, which have allowed a more accurate picture to emerge of the ecology of MVE virus and a more effective surveillance system to be established to provide an early warning of increased virus activity. Human cases of Australian encephalitis, surveillance for virus activity, virus isolations, factors affecting mosquito populations, and virus spread and persistence are discussed below. Human encephalitis cases Increasing numbers of Australian encephalitis cases have occurred in Western Australia and the Northern Territory since 1977 (Mackenzie and Broom 1995; Mackenzie et al. 1993a; Smith et al. 1993). Indeed the majority of cases reported in Australia since 1977, thirty of

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cases, have been from Western Australia, with a further thirteen cases from the Northern Territory. It is also interesting to note that the first confirmed case of encephalitis due to Kunjin virus occurred in Western Australia in 1978, and three additional cases have been diagnosed since, two from Western Australia in 1991 and 1995, and one in Victoria in 1984 (Table 8.1). Most of the cases of Australian encephalitis in Western Australia have occurred in areas distant from the Ord River irrigation area. Of particular significance was the spread of MVE virus from the Kimberley area south to the Pilbara and Gascoyne regions causing one case of encephalitis in 1978 and three cases in 1981. It is hypothesized that movement of virus to the Pilbara region in 1978 was due to an increase in viral activity in the West Kimberley area following heavy rainfall and flooding, and that with subsequent extensive cyclonic rainfall in the Pilbara region, viraemic waterbirds moved south down the narrow coastal strip, introducing the virus into Pilbara (Stanley 1979). It is probable that a similar mechanism may have occurred in 1981. Although there has been evidence (see next section), of MVE virus activity in the Pilbara region in recent years, there have been no further cases. Analysis of the cases of Australian encephalitis has indicated that Aboriginal infants, particularly male infants, are most at risk of fatal or severe disease (Mackenzie et al. 1993a). However, tourists and visitors to the Kimberley region (and Northern Territory) have also been shown to have an increased risk of disease. Sentinel chicken surveillance Following the 1978 outbreak of Australian encephalitis, a number of sentinel chicken flocks were established in the Kimberley area. Six flocks had been established by 1981 and the number rose to twenty-four flocks in twenty-two regional centres in the Kimberley, Pilbara and Gascoyne regions by 1989 (Broom et al. 1989; Mackenzie et al. 1992; 1994c). Each flock contains twelve chickens which are bled at two weekly intervals between November and June, the period of increased risk of virus transmission, and monthly at other times. The sera are then assayed for antibody to MVE and Kunjin viruses in our laboratory in Perth to provide an early warning system of increased virus activity. Initially sera were tested by HI for the presence of antibody, and positive sera were then subjected to neutralization assay to determine the identity of the infecting virus. A more rapid enzyme-linked immunosorbent assay (ELISA) was introduced in 1986 (Broom et al. 1987), and more recently a competitive ELISA using specific monoclonal antibodies to identify the virus is being used (Hall et al. 1992; 1995). Sentinel chicken flocks were also established in 1992 in the Northern Territory to monitor MVE activity (Aldred et al. 1992). The sentinel chicken programme has clearly shown that MVE virus is enzootic in several areas of the Kimberley region, particularly in the Ord River area at Kununurra. Seroconversions in sentinel chickens occur every year during the latter half of the wet season

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in Kununurra; indeed, occasional seroconversions have been recorded in every month of the year. Elsewhere in the Kimberley region, seroconversions occur in most years towards the end of the wet season at all sites monitored, but the overall frequency tends to be less than that observed in Kununurra, except when flooding is extensive and widespread. Until about 1990, most seroconversions in sentinel chickens in the Pilbara region were due to infections with Kunjin virus, but over the next three years seroconversions to MVE virus showed a significant increase in incidence, suggesting that virus movement from the Kimberley region may be occurring more often. Since 1993, however, Kunjin virus activity has once again become more prevalent in the Pilbara area. Mosquito collections Continuing studies in 1976 and 1977 in the Ord River area using bait traps showed that while Culex annulirostris continued to dominate the mosquito fauna of the area, other species such as Coquillettidia xanthogaster, Mansonia uniformis and Anopheles bancroftii increased in number following stabilization of the margins of Lake Kununurra and the prolific growth of aquatic plant species (Wright 1981). Studies in the West Kimberley area in 1977 in the Derby area also found that Culex annulirostris was the dominant mosquito species (Wright et al. 1981). A major advance in mosquito trapping in the north of Western Australia was the introduction of the EVS-CO light trap in 1978, which replaced the use of bait traps after 1979. This resulted in a ninefold increase in the number of mosquitoes being collected, and a significant increase in the species diversity, although Culex annulirostris remained the dominant species (Stanley 1979). Annual mosquito collections have continued to be undertaken in the Ord River area and at other sites in the Kimberley region since 1978, particularly at the end of the wet season although also at other times if unusual environmental conditions such as cyclones or early wet season flooding have occurred. With the stabilization of Lakes Argyle and Kununurra and of the area under irrigation, the results obtained have provided a clearer association between environmental conditions, mosquito numbers and virus activity (see below). Although the mosquito density, and thus the number collected, is always relatively high in the Ord River area, heavy wet season rainfall and flooding result in a significant increase in the mosquito density. In other areas of the Kimberley, a similar pattern has emerged but the increase in the mosquito density is often more marked than in the Ord River area, and the proportion of different mosquito species tends to vary considerably. Nevertheless, regardless of the study area, Culex annulirostris dominates after widespread heavy rainfall and flooding, but if the rainfall is more localized, other floodplain breeding species such as Aedes normanensis may dominate initially (e.g. Broom et al. 1992).

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Virus isolations Mosquito collections obtained during most field trips to the north-west of Western Australia have been processed for virus isolation. Until 1985, virus isolation was undertaken by intracerebral inoculation of suckling mice, but this was then replaced by cell culture using C6/36 mosquito, PSEK, BHK and Vero cells. The use of cell culture has significantly reduced the overall virus isolation rate by largely excluding arboviruses, rhabdoviruses and most bunyaviruses, but is as effective as suckling mice for the isolation of flaviviruses and alphaviruses. MVE virus has been isolated every year that significant numbers of adult mosquitoes have been processed except 1983 (Broom et al. 1989; Broom et al. 1992; Mackenzie et al. 1994c). Isolations of MVE, Kunjin and other flaviviruses are shown in Table 8.2. There was a strong correlation between the number of virus isolates in any given year and the prevailing environmental conditions. Thus those years with a heavy, above average wet season rainfall and subsequent widespread flooding yielded large numbers of virus isolates (1981, 1991, 1993) compared with years with average or below average rainfall and with only localized flooding. Although most MVE virus isolates were obtained from Culex annulirostris mosquitoes, occasional isolates were also obtained from a variety of other species, including Culex quinquefasciatus, Culex palpalis, Aedes normanensis, Aedes pseudonormanensis, Aedes eidvoldensis, Aedes tremulus, Anopheles annulipes, Anopheles bancroftii, Anopheles amictus and Mansonia uniformis (cited in Mackenzie et al. 1994b; Mackenzie and Broom 1995), although the role of these species in natural transmission cycles has still to be determined. Virus carriage rates in Culex annulirostris mosquitoes are shown in Table 8.3 for the Ord River area (Kununurra–Wyndham) and Balgo and Billiluna in south-east Kimberley. Very high mosquito infection rates were observed in those years with above average rainfall. Virus spread and persistence Stanley (1979) suggested that viraemic waterbirds, which are often nomadic, may generate epidemic activity of MVE in south-east Australia and in the Pilbara region. In an attempt to understand the genesis of epidemic activity better, our laboratory initiated a long-term study in the arid south-east Kimberley area at Billiluna and Balgo, two Aboriginal communities on the northern edge of the Great Sandy Desert. Occasional cases of Australian encephalitis had occurred in both communities (1978, 1981). The studies have clearly shown that MVE virus activity only occurs following very heavy, widespread rainfall both locally and in the catchment area of the nearby watercourse, Sturt Creek, which results in extensive flooding across its floodplain (Broom et al. 1992). Localized flooding is insufficient to generate virus activity. Two possible explanations can be proposed to account for the reappearance of MVE virus activity when environmental conditions are suitable: either virus can be reintroduced into the area by viraemic waterbirds arriving from enzootic areas further north; or virus may

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from Halls Creek in the East Kimberley region and Derby in West Kimberley in 1960 had demonstrated that subclinical infections with both MVE and Kunjin viruses had occurred in the human population (Stanley and Choo, 1961; 1964), there had been no reported cases of Australian encephalitis in Western Australia or in the Northern Territory. Unfortunately no baseline studies were undertaken on either mosquito densities or virus incidence before the completion of stage one of the irrigation project; indeed no studies were initiated until completion of stage two, the construction of the Ord River dam. While the Ord River irrigation area undoubtedly had enormous and profound effects on the ecology of the region, most of the evidence for increases in mosquito densities and waterbird populations is circumstantial. The climate in the Kimberley and adjacent areas of the Northern Territory comprises a relatively short (four month) monsoonal wet season during which heavy rainfall events occur and the major rivers extend across vast floodplains, and a very dry ‘dry’ season during which most of the country becomes arid and, in the latter half, even large rivers cease to flow. Results from studies at various locations, such as Billiluna and Halls Creek, suggest that MVE virus is occasionally epizootic in many arid areas of the Kimberley. It is probable, therefore, that the area in which the Ord River irrigation area was established was similar and, consequently, that prior to the irrigation scheme being implemented, MVE was also epizootic. Since 1972, our studies in the Ord River irrigation area and elsewhere in the Kimberley region on virus isolations from mosquitoes, on serological investigations of humans, animals and sentinel chickens, and on human cases of Australian encephalitis, have clearly shown that MVE virus is now enzootic in the Ord River area and probably in other foci such as the Derby and Broome areas of the West Kimberley region. Elsewhere, in arid areas of the Kimberley and in the Pilbara, MVE virus is epizootic and virus activity is probably initiated either by virus reactivation from desiccation-resistant mosquito eggs or by introduction through viraemic vertebrate hosts. The situation in the Northern Territory is less clear as insufficient data have been accumulated. However, it is probable that MVE is enzootic in the wetlands in the north of the Northern Territory, but epizootic in the more arid areas further south extending east from the Kimberley border. Since 1978 there has been a substantial increase in the number of cases of Australian encephalitis throughout the Kimberley and Northern Territory that cannot be ascribed to either an increase in population or a heightened awareness among clinicians. Thus, although based largely on circumstantial evidence, we believe that the Ord River Irrigation Area has had a profound effect on MVE virus activity and indeed has resulted in the virus becoming enzootic in the area. We also believe that this large, stable enzootic focus has provided the source for regular epizootic incursions to other areas of the Kimberley and adjacent arid areas of the Northern Territory, and to the Pilbara, and has probably established smaller enzootic foci in the West Kimberley. As virus can persist in desiccation-resistant mosquito eggs, it is probable that most areas of the Kimberley and adjacent areas of the

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Northern Territory, and possibly parts of the Pilbara, have been ‘seeded’ with virus which could result in epizootic activity when appropriate environmental conditions occur. Our conclusions could have important health implications as the population in north-western Australia increases through intensive agriculture, mining, service industries and tourism and, in the longer term, through possible effects of climate change (Mackenzie et al. 1993b; Lindsay and Mackenzie 1997). Furthermore, increased virus activity could be exacerbated as new irrigation areas are developed in the Wyndham–East Kimberley shire and the adjacent part of the Northern Territory. Finally, there is little doubt that the profound ecological changes resulting from the establishment of the Ord River irrigation area have provided ideal conditions for increased arboviral activity. These conditions are also suitable for other exotic arboviruses, such as Japanese encephalitis and chikungunya viruses, and exotic mosquito vectors, such as Aedes albopictus. Indeed an unusual strain of MVE has been isolated from the Ord River area, which was believed to have been introduced from the Indonesian archipelago (Mackenzie et al. 1991). Further-more, the recent incursion of Japanese encephalitis virus into islands in the Torres Strait and Cape York, and its possible enzootic presence in the south of Papua New Guinea, provide additional cause for concern. It is therefore essential that monitoring and surveillance of mosquitoes and arboviruses is continued so that exotic virus or vector incursions can be rapidly detected. Acknowledgments We would like to thank our many colleagues who have contributed to these studies of MVE virus activity in the north-west of Western Australia. We would also like to acknowledge the support of the Health Department of Western Australia and the National Health and Medical Research Council, and the Commonwealth Department of Health. References

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The report recognized the need to minimize disturbance of fauna and flora and suggested that ‘swimmer’s itch’, caused by avian schistosome cercariae, and mosquito-borne viruses should be investigated. Because the 26 km northern boundary, e.g. Big Bay, Antill Creek, had steeper foreshores and deeper water, it was recommended as a primary site for public access. The 7 km western boundary formed by the dam wall was seen as ideal for viewing opportunities of the lake and surrounding hills and mountains, and for water sports. Because of inaccessibility, potential management difficulties and shallowness, the 47 km southern and eastern margins did not offer significant recreational opportunities. 9.3 Tropical itch mite The stage 1 lake was surrounded with open schlerophyll woodland which afforded kangaroos and wallabies shelter during the hottest times of the day. Part of their exoparasitic fauna is the mite Eutrombicula macropus, whose offspring spend part of their life-cycle hanging off grass stems and other vegetative matter waiting to encounter a new host. Much to their misfortune, campers and bushwalkers consequently often find themselves with an itchy rash called ‘tropical itch’, often around the lines of underclothing. Prior to the filling of the stage 2 lake, the land in the zone between the stage 1 and stage 2 margins was selectively cleared. This probably diverted the macro-pods to other wooded habitat. From November 1990 to 1992, 350 litter samples were processed using Berlese funnels and 40 W incandescent bulbs to drive any inhabitants into sample bottles containing 70 per cent alcohol. No Eutrombicula macropus were collected. Thus clearing would seem to present an effective management option against this pest, as well as having the other benefits detailed below. 9.4 Mosquitoes and arboviruses 9.4.1 Mosquitoes From April 1984 to September 1985 (stage 1), the primary questions related to definition of mosquito taxa and the suitability of different methods of catching adult mosquitoes for surveillance purposes. Twenty-six taxa were collected by all night carbon dioxide supplemented light traps or by human bait collections for one hour after sunset (Barker-Hudson et al. 1993; Jones et al. 1991). The numerically dominant species were Culex annulirostris and Anopheles annulipes (both species groups), which are traditionally associated with temporary fresh water pools along the lake margins, often among emergent vegetation. Of considerable surprise during September 1985 was the discovery of immatures of these species, plus Aedeomyia catasticta, utilizing extensive floating mats of the aquatic weed Hydrilla verticillata which sometimes covered 37 per cent of the surface of the lake.

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This will be discussed later. Two species, Mansonia uniformis and Mansonia septempunctata, which breed in association with macrophytes such as water hyacinth Eichhornia crassipes, became less common from stage 1 to 2. The saltmarsh species Aedes vigilax was also collected in reasonable numbers at all localities around the reservoir. This species is known for its wide dispersal powers and was undoubtedly blown in from the extensive intertidal wetlands on the coast. Thus on the basis of abundance, two taxa – Culex annulirostris and Anopheles annulipes s.1. – warranted further consideration. The former species is considered to be the major vector of arboviruses in Australia (Russell 1995), transmitting Ross River, Barmah Forest, Kunjin, Kokobera, Alfuy and Edge Hill viruses and Murray Valley encephalitis, as well as dog heartworm. Of these, Ross River is by far the most common arbovirus in coastal northern Queensland, with morbidity approximating 400 cases per 100,000 population. Thus from first principles, this arbovirus and perhaps Barmah Forest, about which little is known, would constitute the greatest hazard to recreational use. Although Anopheles annulipes has previously been implicated in malaria transmission at Sellheim during the Second World War, this species group has returned isolated positives of Ross River and Barmah Forest viruses and Murray Valley encephalitis from other parts of Australia. However, no transmission studies have been done on the population from the reservoir. Thus on the evidence to date, it could not be regarded as a major concern at the Ross River dam. Both Culex annulirostris and Anopheles annulipes were shown to have seasonal peaks of abundance during the late post-wet season (March to May), with populations building up with the onset of spring (September to October). Spatially, the trapping programme was designed to compare mosquito numbers on the foreshore of the stage 1 lake with two localities expected to be on the margins of the stage 2A lake, with two remote localities (and therefore theoretically unaffected by any water resource project activity) as negative controls. Mosquito numbers (i.e. for those species known to breed at the dam) decreased with distance away from the Ross River dam. Both light trapping and human bait collections carried out twice per month were reasonable indicators of broad seasonal trends in mosquito abundance. However, the statistical analysis indicated that occasionally the light traps could miss short periods of high biting activity (Jones et al. 1991). If greater resolution was required, it was recommended that light traps could be supplemented with animal baited traps, although it is probable that this could be rectified by intensifying the light trapping regimen. Cluster analyses of dam breeding species in both 1984–85 and 1991–93 indicated that light trap catches along the northern (Big Bay, Ti-Tree Bay, Round Island) and western sides (Ross River) gave similar patterns, but the profile towards the east (Antill Creek, Toonpan, Oak Valley) was somewhat different (Barker-Hudson et al. 1993; Hearnden and Kay 1995). On this basis, adult mosquito surveillance would therefore need to be based on two localities at either end of the lake.

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The lake trapping was continued twice monthly from February 1991, two years after the first filling of the stage 2A reservoir, until June 1993. The trapping locality at Toonpan was essentially the same as for the 1984–85 studies except that for Big Bay was moved a few hundred metres up the incline. Because the expansion from stage 1 to 2A involved extensive clearing of marginal scrub, grassland and forest, almost total control of five mosquito species utilizing tree holes and plant axils (Aedes alboscutellaris, Aedes mallochi, Aedes purpureus, Aedes quasirubithorax) or shaded pools (Uranotaenia nivipes) occurred. The transformation of temporary wetland with ti-trees (Melaleuca spp.), lilies (Nymphoides indica, Nymphaea gigantea) and submerged plants into an unvegetated muddy foreshore similarly reduced Mansonia spp. and Coquillettidia crassipes, whose larvae depend on attachment to arenchymatous or lacunate macrophytes. Larvae of these genera have pointed reinforced tips to their siphons which are used to pierce these plants to breathe. Because of the devastating nature of the inundation and the time required for new breeding habitat to re-establish, mosquito populations increased through to the end of 1993 but the mean abundance of adult Culex annulirostris had not changed significantly from stage 1 levels. The trend for this species and for Anopheles annulipes was upward, and one can only speculate on population levels when the marginal vegetation has fully established. Due to the extensive loss of marginal vegetation and the creation of expanses of shallow muddy pools, especially towards Toonpan, Anopheles amictus and Aedes normanensis populations increased by 36-fold and 282-fold, respectively (Figure 9.2). The ramifications of this are interesting as Aedes normanensis is well recognized as a vector of Ross River virus and Murray Valley encephalitis, especially inland where Anopheles amictus (probably another species complex) has been the source of Ross River, Barmah Forest and Edge Hill viruses. Control of mosquitoes is usually directed at removal of breeding habitat (source reduction) or aimed at larvae which often aggregate in large numbers in discrete sites. Aedes normanensis is ephemeral and its desiccation-resistant eggs characteristically hatch in response to wet season rainfall filling up temporary pools. Plague numbers appear one month and may be gone the next. More accurate definition of these breeding sites, particularly at Toonpan, Antill Creek and Ross River, is required before control options can be considered. As already mentioned, the clearing process created vast expanses of bare muddy pools, particularly at the north-eastern end (e.g. Toonpan). As the lake gradually receded during the dry season, ideal breeding sites were created and populations increased through spring (from September) and also in the late wet season (March to April) when dry sites were refilled by rainfall. Thus, although the land clearing had benefits in eliminating tropical itch mites and some minor mosquito species, it probably paved the way for population growth of Aedes normanensis and Anopheles amictus. This could possibly be considered a dubious swap, although time will tell. Little is known of their biology and their flight range, the latter being of obvious importance to recreational activity at the other end of the lake. Fortunately, however, they are mainly active at night.

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lake was larger, aerial photography was used to estimate the extent of the floating algal mats. This was then scanned into a computer, digitized and estimates made. During April and November 1991 and in September 1992, Hydrilla covered between 13.3 and 16.6 km of the stage 2A lake, and this was estimated to contain populations of 5.6 billion, 275 million and 513 million immatures, respectively, mainly Culex annulirostris and Anopheles annulipes as before. However, whereas Culex annulirostris comprised 90–98 per cent of aquatic stages during 1985–86, now Anopheles annulipes s.l. comprised 43.7 per cent of all the immatures identified. Although natural mortality will reduce the numbers actually reaching adulthood, these numbers are so high that some form of control is indicated. As discussed previously, one can only speculate on the abundance of mosquito larvae that will utilize marginal emergent vegetation when it develops fully along the foreshores of the stage 2A lake. At present, from the 1991–93 data, the average number of mosquito immatures based on transects 5 m wide was 85.7/m Because the shoreline contains bare

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a water purifier and a food source and haven for the abundant wildlife at the reservoir? We think not. This option will be discussed later. 9.4.2 Arboviruses From 1983 to 1987, domestic chicken flocks were maintained as sentinels (Figure 9.3) and bled for the presence of antibodies to both alphaviruses (e.g. Ross River virus) and flaviviruses (e.g. Murray Valley encephalitis, Kunjin viruses). These data showed that alphavirus activity occurred annually but this infection was somewhat unpredictable and did not necessarily correlate with the zones of highest mosquito abundance closest to the reservoir. Flavivirus infection occurred far less frequently. From 1990–93, 51,497 adult female mosquitoes were processed for the presence of alphaviruses using enzyme immunosorbent assay and polymerase chain reaction methods (Kay et al. 1996; Oliveira et al. 1995). Ten isolates of Ross River, one of Barmah Forest and two of Sindbis virus strains were recovered from Aedes normanensis, Anopheles amictus and Culex annulirostris, which indicated that they were probably local vectors. All virus stains were recovered from mosquitoes collected during the wet seasons (February or March) of 1991 or, especially, 1992. Relative hazard was assessed for four Ross River dam localities: Big Bay (north); Antill Creek (north-east); Toonpan (east); and Ross River (south). These were compared with more

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limited data for the greater Townsville area (Kay et al.1996). Based on the prevalence of key vector species and their abundance and that of the viruses recovered, it was concluded that Big Bay, originally recommended as a prime site for recreational development by the Department of Local Government in 1985, actually presented lower risk than any other locality. Antill Creek also proved relatively safe in terms of mosquito-borne infections, whereas Toonpan during the wet season was a place to be avoided. Both Ross River and the environs of Townsville offered intermediate risk, the latter due to large numbers of saltmarsh mosquitoes breeding in intertidal wetlands. 9.5 Snails and swimmer’s itch Schistosome dermatitis, known as swimmer’s itch, is a common global problem for users of recreational swimming areas in water resource developments. The rash is caused by free living larvae called cercariae (Figure 9.4) of parasitic flukes which burrow into exposed parts of the body. Normally the life-cycle involves water birds such as ducks and pulmonate snails, so infection of humans is accidental. A large number of cercariae may penetrate the skin where they die but cause a localized allergic reaction in sensitized persons. In northern Australia, swimmer’s itch (Trichobilharzia) has been traditionally associated with Austropeplea (= Lymnaea) lessoni (= vinosa) although two planorbid snails, Amerianna carinata and Gyraulus stabilis, have also been identified as intermediate hosts in Lake Moondarra near Mt Isa, Queensland. Our recent data implicates Gyraulus gilberti at the Ross River dam. Snails are also commonly infected with other trematode cercariae, mainly echinostomes, strigeids/diplostomids and clinostomids.

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Because of previous isolated reports of swimmer’s itch at the stage 1 lake, periodic surveys by sweep netting commenced in July 1990. For each of six localities covering three distinct habitat types (open bays within the lake, along the margins of permanent creeks, temporary ponds), 1 m quadrats containing all vegetation types were scoured for snails. Austropeplea snails were not present in the lake proper until February 1991, but in November 1990 they were first located in ponds along the north-east, east and south-western shorelines. Egg masses were often found attached to the undersides of nardoo (Marsilea mutica) and sometimes wrapped around the stalks and ventral surfaces of the water lily, Nymphaea gigantea. Thus its absence from the lake was attributed to the lack of established vegetation in the stage 2A lake, and from this we developed a working hypothesis that host snails were possibly vegetation-specific. Thus to facilitate recreational use, control of infected Austropeplea could be achieved by simply clearing the appropriate water plant. By July to August 1991, however, schistosome-infected Austropeplea were collected from various types of vegetation along the margins of Ross River, close to the lake. A few Amerianna and Gyraulus gilberti were found in Ti-Tree Bay contiguous with Big Bay and Round Island, which were still negative for snails. By February 1992, planorbids were present in all three habitat types, with Austropeplea in two, i.e. ponds and creeks around the lake. Until 1993, 2,365 snails were dissected to detect both patent and pre-patent Trichobilharzia infection. Four different species of snails were identified, size classed according to shell length or width using vernier calipers. Snails were crushed on a microscope slide or in a Petri dish with a few drops of water under a warm light. A heavy infection of cercariae is evident to the naked eye, but any worm-like animals were removed on to another slide, stained with two to three drops of 0.1 per cent neutral red dye, covered with a coverslip and examined microscopically. Schistosome cercariae are distinctive with their eye spots, forked tail and presence of oral and ventral suckers (see Figure 9.4). Schistosomes were recovered from 4.5 per cent and 1.7 per cent of Austropeplea and Gyraulus gilberti snails, but not from Amerianna nor Thiara. In terms of management solutions, several questions seemed paramount: • Which habitat types presented the greatest (and lowest) risk? • Which time of the year presented the greatest hazard? • Can certain indicators be used to predict infection? Statistical analysis of the presence and abundance of Austropeplea snails did not correlate with any particular vegetation type (Hurley et al. 1995) but was connected with vegetation generally. There was no clear-cut relationship with snail density and physicochemical parameters including temperature, biomass of periphyton or with percentage surface coverage. However, highest densities of Austropeplea lessoni (45/m and Amerianna

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greatest. Periphyton is mostly composed of diatoms, epiphytic algae, bacteria, fungi and protozoa and builds up as a food source for snails on submerged waterplants and on the undersides of floating plants. Highest densities of Gyraulus gilberti (15/m) occurred in permanent creeks such as Ross River. Thus, rather fortuitously, likely recreational sites such as Big Bay and Ti-Tree Bay along the northern foreshore were relatively safe, especially if some vegetation cleating was added. Austropeplea was never collected from bare areas. Although infected snails were collected at all times of the year, the greatest densities of Austropeplea occurred during the late dry season. Blair and Finlayson (1981) noted the catastrophic effect of heavy wet season rainfall on Austropeplea populations at the Ross River dam in 1978 due to substrate scouring and vegetation clearing. It is likely that since Austropeplea were mainly associated with ponded habitats, maximum densities were influenced considerably by dry season habitat shrinkage as well as by food concentration. In contrast, peak densities of Amerianna and Gyraulus were recorded during the late wet seasons of 1992 and 1993. In terms of surveillance, the prevalence of infection within each size class of snail provided a handy indicator to streamline efforts. For Austropeplea lessoni, for example, 80 per cent of snails of 20 mm or greater shell length were infected with trematodes, 39 per cent of these being with Trichobilharzia spp. For the Ross River dam, smaller snails, i.e. < 3 mm for Gyraulus gilberti, < 6 mm for Amerianna carinata and < 10 mm for Austropeplea lessoni, need not be collected (Hurley et al. 1994).

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As an adjunct to this, egg masses of Austropeplea were hatched out and reared in constant temperature rooms at 15°C, 25°C and 30°C with weekly changes of water and vegetation (Figure 9.5). Shell length was measured weekly until time of reproduction. At 15°C the snails grew slower but lived longer, but at 25°C and 30°C, there was little difference in growth rates, although those at 25°C were marginally larger at equivalent periods. Although water temperatures at the Ross River dam do occasionally drop to 16°C on occasions, generally they average 25–28°C (Hurley et al. 1995). Thus from this, an Austropeplea of 12 mm shell length collected during summer will be around one month old and capable of reproducing. One of 20 mm at either 25°C or 30°C water temperature would be approximately 100 days old. On this basis, it is suggested that monitoring could be comfortably done every two to three months. 9.6 Management options 9.6.1 General conclusions There are several other lakes, man-made or otherwise in northern Queensland, that support diverse recreational activities without apparent mishap. All are subjected to tropical conditions conducive to year round production of mosquitoes, snails, mites and pathogens. What is different about the Ross River dam stage 2A is its shallowness and proximity to large human populations. Nevertheless, the studies carried out in two blocks (1983–1987 and 1990–1995) have defined its mosquito and alphavirus hazard as considerable but no greater in the northern and north-eastern areas of Big Bay, Ti-Tree Bay, Round Island and Antill Creek than that experienced by local residents in everyday life. The relative hazard would change considerably, however, if the responsible local authorities ever decided to mount a broadscale aerial control programme against larval Aedes vigilax, which breed in the extensive intertidal wetlands. Restriction of activities to daylight hours will not only facilitate easier control of the public but will also reduce exposure to key vector species such as Culex annulirostris, Anopheles amictus and Aedes normanensis. However, who takes the responsibility for an estimated 5 billion mosquito larvae found periodically in the floating Hydrilla beds? As discussed, both Culex annulirostris and Anopheles annulipes are quite capable of dispersing from the reservoir into the urban populace. Recreational management issues are probably far less complicated than the moral issues. Whereas land clearance prior to the flooding of the stage 2A lake was effective in controlling tropical itch mites and some mosquito species, it also probably effected a redistribution of the kangaroos and wallabies, known to be most effective intermediate hosts of some arboviruses, including Ross River and the often fatal Murray Valley encephalitis. They have probably been driven towards the quieter eastern areas around Toonpan, where in 1992 Ross River virus was detected in wet season Aedes normanensis at rates as low as 1:217

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mosquitoes. What is the impact of such ecological change and what will it look like in the future? 9.6.2 Mosquito or aquatic plant control? The options for control of aquatic plants such as Hydrilla are mechanical, biological, chemical, or a combination of these methods. The objective of aquatic weed control should be to control growth sufficiently to permit the water to be used in the desired way but without a change in the balance of species (Bill 1977). Aquatic plants are only weeds if they pose a major nuisance or hazard. Clearly there is a case as mentioned previously for clearing buffer zones to mitigate against swimmer’s itch or to facilitate boating and safe swimming. Aquatic plant growth generally relies upon nutrient availability, light availability, adequate physicochemical characteristics and habitat stability. Nutrient availability relies upon substrate type and the presence of dissolved organic and inorganic matter. Light intensity decreases with depth to the point where the energy acquired by photosynthesis cannot meet the energy requirement of vegetation and plant growth ceases. The interrelationships of key factors such as depth, wave exposure, littoral slope and sediment characteristics are complex (Duarte and Kalff 1990), although slopes of greater than 15° are regarded as the first limit to plant growth and the second is depth. The Ross River reservior is shallow with an average depth of less than 3 m, which explains why Hydrilla beds sometimes cover up to 37 per cent of the surface area of the lake. Bill (1977) discussed a protocol for deciding the best and most effective control measures to be used and outlined a checklist of questions. • To what extent is plant growth responsible for the particular problem, e.g. reduction of channel capacity, interference with recreational use? • Are chemical methods of control more suitable than mechanical or biological methods, or could more than one method be used? • What is the most economical long-term approach? • What degree of control is required to provide adequate relief from the particular problem? • If chemical methods are most appropriate, which material is likely to be most effective and how should it be used? Are residues of chemicals in the water following a treatment likely to be detrimental to human health or to fish, wildlife or irrigated crops? • Is it desirable to retain some plants for the benefits of fish and waterbirds? Biological control is not the universal solution to all pest problems, but it may be applied to a vast array of problems and when effective it is the most satisfactory and economical form

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of control. The state of Queensland has generous expertise in this area, with the CSIRO Division of Entomology – Lands Department group in Brisbane boasting spectacular success against Salvinia and Eichhornia, and near the reservoir at James Cook University a USDA unit was involved in successes with the Tennessee Valley Authority (TVA) (see Chapter 12) using a range of stem-boring and leaf-mining insects (Balciunas et al. 1993). One might consider the herbivorous grass carp Ctenopharyngodon idella, originally from China, more as a harvester than a biological control agent. This fish grazes on submerged weeds such as Hydrilla, Myriophyllum, Chara, Potamogeton and Ceratophyllum, and at stocking rates of 75 fish/ha control is rapidly achieved. Some introductions in the USA have resulted in removal of all vegetation (Leslie et al. 1987), and in the Australian context the use of sterile (triploid) fish (Cassani and Canton 1985) could be the only consideration. However, in view of the damage already done by grass carp to some inland waterways in Australia, it is suspected that this option would be greeted with horror. Mechanical control involves the physical removal of weeds from a problem area and is useful in situations where the use of herbicides is not practical or poses risks to human health or the environment. Mobile harvesters sever, lift and carry plants to the shore. Most are intended for harvesting submerged plants, though some have been designed or adapted to harvest floating plants. Handling the harvested weed is a problem because of their enormous water content, therefore choppers are often incorporated into harvesting machinery design. However, many mechanical harvesters have a small capacity and the process of disposing of harvested plant material is time-consuming. Any material that remains may affect water quality during the decay process by depleting the water of oxygen. Furthermore, nutrients released by decay may cause algal blooms (Mitchell 1978). Another disadvantage of mechanical removal is that disturbance often promotes rapid new growth and germination of seed, and encourages the spread of weed by fragmentation. Some direct uses of macrophytes include the following: livestock food; protein extraction; manufacture of yeast; production of alcohol and other by-products; the formation of composts, mulches and fertilizers; and use for methane generation (Williams 1977). Herbicides either kill on contact, or after translocation through the plant. Some are residual and retain their toxicity for a period of time. Where herbicides are used for control of plants, some contamination of the water is inevitable (Bill 1977). The degree of contamination depends on the toxicity of the material, its fate and persistence in the water, the concentration used and the main purpose served by the water. After chemical defoliation of aquatic vegetation, the masses of decaying organic debris produced can interfere with fish production. Several factors must be taken into account when selecting and adapting herbicides for aquatic purposes, including: type of water use; toxicity of the herbicide to humans, fish, stock, and wildlife; rate of disappearance of residues, species affected and duration of control; concentration of herbicide; and cost (Bill 1977). The TVA has successfully used EPA-approved herbicides such as Endothall, Diquat, Fluridone and Komeen against Hydrilla (Burns et al. 1992), and a list of approved

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the dosages used to kill mosquitoes, non-target organisms are safe. Both of these products, especially Bacillus, break down quickly and should therefore present no hazard to water quality. Given that a site such as Big Bay may become a mecca for those wishing to swim, sail or even fish, a surveillance programme and some environmental modifications are necessary. The deeper open waters of this bay coupled with a vegetation-free foreshore as a buffer zone, perhaps 400 m on either side of a swimming zone, should minimize or even negate swimmer’s itch. Adjacent Hydrilla and other macrophytes will require clearing as these will also present a physical hazard to swimmers and watercraft. The monitoring programmes could ideally be done three to four weeks prior to extensive public usage to allow time for any remedial action. The prevalence of key mosquito species and of large Austropeplea (and Gyraulus and Amerianna) snails can be established quickly as can cercarial infection in the snails. If it is found necessary to establish infection rates in mosquitoes, the newly developed Ross River and Barmah Forest virus testing procedures using mosquito cell cultures and enzyme immunosorbent assay (Oliveira et al. 1995) would require six days processing time. This offers considerable economy over previous methods using intracerebral inoculation of baby suckling mice. We would suggest that prior to selected recreational events, especially those from March to May, the Water Supply Board should initiate the action shown in Figure 9.6. The information supplied in response to a request should be communicated to recreational users to ensure that they are aware of the risks. Perhaps mosquito, arbovirus, and schistosome status could be displayed in the same way as fire hazard status is commonly indicated. It would be remiss of us to generate the impression that we had all the answers to the Ross River dam. The stage 2A lake and its surrounds are undergoing a process of ecological change and realization of this must remain paramount. There are issues relating to mosquito biology and behaviour and to do with snail ecology generally that would repay further study. Thus further selective monitoring and research should not be forsaken. References

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Artificial wetlands and mosquito control in Australia

10.1 The general scenario
ByRichard C. Russell

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Acknowledgments

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2 The challenge

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