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Mosquito-Borne Viruses and Non-Human Vertebrates: History
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Subjects: Virology
Contributor: Oselyne Ong

Mosquito-borne viruses are well recognized as a global public health burden amongst humans, but the effects on non-human vertebrates is rarely reported. 

  • mosquito vectors
  • arboviruses
  • disease reservoirs
  • animal diseases
  • animal distribution

1. Mosquitoes: The Link between Vertebrate Host and Disease

There are more than 300 species of mosquitoes identified in Australia and almost 100 of these are capable of transmitting pathogens to wildlife and domestic animals (see Table 1), of which Aedes, Culex, and Anopheles species are the most common genera of vectors [7]. Feeding preferences by these species are highly variable with some species (such as Aedes aegypti) reported to have host specific feeding patterns, while other species (such as Aedes vigilax) exhibit more generalist feeding behaviors [8], both of which can play an important role as bridging vectors [9,10]. Individual feeding patterns are often dependent on host abundance and availability, both of which are strongly linked to habitat identity, and which can change annually and seasonally depending on the biology and ecology of individual host species (see [11] for a review). To date, vertebrate blood-meal hosts have been identified for a variety of taxonomic groups, including Carnivora (e.g., cats, dogs, and foxes), Aves (birds), Diprotodontia (e.g., possums and macropods), Artiodactyla (e.g., cattle, sheep, pigs, and goats), and Equidae (horses), with individual vector species displaying a trade-off between host preference and host availability [11]. For example, in rural Queensland, Australia, bloodmeal origins for Culex annulirostris, were dominated by cattle [12], but in Sydney, a highly urbanized city, Cx. annulirostris bloodmeal origins were mostly from birds, rodents and rabbits [8]. Thus, the ecologies of Australian mosquito-borne viruses can be driven by complex interactions between vector species, host availability, and host preference, which may be a derivative of habitat or climate. This will ultimately drive the spread of pathogens.
Table 1. A summary of pathogen, pathogen distribution, mosquito vectors, and symptomatic a and asymptomatic b host distribution in Australia. Dengue and Rift Valley fever are not listed as there have been no known non-human vertebrate hosts in Australia.
Pathogen Pathogen Distribution in Australia Mosquito Vectors Asymptomatic Hosts of Pathogen in Australia Symptomatic Hosts of Pathogen in Australia
Ross River virus (RRV) All of Australia [13] Aedes and Culex mosquitoes, particularly Aedes vigilax, Aedes camptohynchus, and Culex annulirostris [14] Marsupials: wallabies, wallaroos [15], common brushtail possums [16], eastern grey kangaroos [17], western grey kangaroos [18]
Australian birds: little corella, magpie larks, Australian brown flycatcher, masked finch [19,20]
Wild eutherian mammals: rodents, Pteropus spp. [20]
Domestic mammals: cattle, dogs [20], cats [21]		 Domestic mammals: horses [20,22]
Barmah Forest virus (BFV) All of Australia [23] Culex annuliristris, Aedes normanensis, Aedes vigilax and Aedes procax [24] Marsupials: eastern grey kangaroo [25], koalas [25] and brushtail possums [21].
Wild eutherian mammals: Australian bush rats and swamp rats [26]
Domestic mammals: cats, dogs, horses [27]		  
Sindbis virus (SINV) Most of Australia (excluding Tasmania) [28] Culex annulirostris, Aedes normanensis, Aedes camptorhynchus [29], Aedes pseudonormanensis [30] Marsupials: chudditch [31]
Wild eutherian mammals: European rabbits [31]
Domestic mammals: horses [31]
Birds: Emus [31]		  
Murray Valley encephalitis virus (MVEV) Western Australia [32], Northern Territory [33], New South Wales, and Victoria [34] Culex annulirostris [35], Culex sitiens and other Culicine mosquitoes [36] Marsupials: eastern grey kangaroos [37], western grey kangaroos, agile wallabies [38]
Australian birds: galahs, sulphur-crested cockatoos [38], chickens [39]
Wild eutherian mammals: rabbits [37], wild mice [38]
Domestic mammals: dogs, sheep, pigs, cattle [37]
Water birds: rufous night herons [34], Pacific black ducks [38]		 Domestic mammals: horses [22,40,41]
West Nile virus (WNV) All of Australia [42,43] Mainly isolated from Culex annulirostris [44]. Other Culex species, Aedes species and Anopheles amictus can also transmit the virus [45,46] Marsupials: western grey kangaroos, agile wallabies [37]
Australian bird: Australian white ibis [47]
Ardeid birds: herons, egrets [48]
Introduced bird: house sparrow [49].		 Wild eutherian mammals: rabbits [50,51]
Domestic mammals: horses [22,42], cats (mild) [52]
Japanese encephalitis virus (JEV) Torres Strait (incursion) [53], North Peninsula Area and mainland [54] Culex annulirostris [53]. Ardeid birds: herons, egrets [55,56,57]
Domestic mammals: pigs [58], horses [59]		 Wild eutherian mammals: Frugivorous bats i.e., black flying fox [60]
Other birds: pigeons, sparrows, ducks, chickens [60]
Kokobera (KOKV) and related viruses Queensland, New South Wales, Northern Territory, Western Australia, and Papua New Guinea [61,62] Aedes species including Aedes aculeatus, Aedes alternas, Aedes notoscriptus, Aedes procax, Aedes vigilax and Anopheles annulipes [63] Marsupials: mainly kangaroos and wallabies [17,64].
Domestic mammals: cattle [26]		 Domestic mammals: horses [64,65]
It is unknown whether horses are affected by Kokobera and related viruses, as it could be associated with a known equine disease.
Gan Gan (GGV) and Trubanaman viruses (TRUV) Queensland, New South Wales, and Western Australia [66] Aedes vigilax (GGV) [67], Culex annulirostris (GGV and TRUV) [62,68], Anopheles annulipes (TRUV) [66] and Anopheles meraukensis [69] Marsupials: eastern grey kangaroos (GGV, TRUV), red-necked wallaby (GGV, TRUV) [26], western grey kangaroos (TRUV) [70]
Wild eutherian mammals: Australian bush rat (GGV) [26], feral pigs (TRUV), rabbits (TRUV), foxes (TRUV), quokkas (TRUV) [70]
Domestic mammals: sheep (GGV), horses (GGV, TRUV), cattle (GGV) [26,70]		  
a A asymptomatic host would be a reservoir host species that does not experience the symptoms of disease but is able to produce sufficient pathogen levels to infect mosquitoes that blood-feed on that animal. b A symptomatic host would be a non-reservoir host species that show symptoms of the disease and also produces sufficient pathogen levels to infect mosquitoes that blood-feed on that animal.
 

2. Uniquely Australian Vertebrate Hosts

Australia provides a unique opportunity to investigate the transmission of viruses between vertebrates and mosquitoes. The long geographic isolation of Australia has led to the co-evolution of viruses, mosquitoes, and endemic vertebrate hosts, which offer unique insights into immunology and physiology. Over the last 200 years, Australia has also experienced the introduction of viruses and domestic species, and an expansion of urbanization, all of which have shifted the dynamics of disease and ecology among native species. This crockpot of co-evolution and introductions mean that Australian fauna have highly heterogenic roles for transmitting different viruses within the community (Figure 1), or are affected by viruses in different ways (i.e., asymptomatically vs. symptomatically; Table 1).
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Figure 1. Relationship between Australian wildlife, mosquitoes, and humans. Often mosquito-borne diseases are often spread from human to human via the bite of a mosquito; however, consideration of Australian wildlife is important as they are often hosts for these pathogens. There are also many factors that can determine the spread of mosquito-borne disease, including the change in wildlife distribution, which should be considered when developing strategies to minimize the spread of disease.

Marsupials

There are more than 300 extant marsupial species globally, of which close to 70% occur on the Australian continent (the mainland, Tasmania, New Guinea, and nearby islands), representing the most diverse extant marsupial radiation [71]. Many species exhibit unique physiological characteristics, such as adaptations to specific climatic envelopes, which have allowed them to succeed in even the harshest of Australian environments. However, immunological characteristics of marsupials may increase their susceptibility to infection for mosquito-borne viruses. When compared to eutherian mammals, neonatal marsupials are born without histological mature immune tissues [72,73] and are therefore unable to mount specific immune responses and are presumably highly reliant on maternal and innate immune strategies. Furthermore, some studies have reported marsupial immune systems are slower to mount some specific immune responses and occur at lower levels than those mounted by eutherian species [74,75]. However, the impact of such differences on disease susceptibility are poorly understood and the many similarities between eutherian and marsupial immune systems [76] cannot be overlooked (Figure 1).
The immediate threat of land use and climate change on the survival of many Australian marsupial species highlights a need to better understand the impacts disease on marsupial health and reproductive fitness. Additionally, we need to consider the ecological impacts of exotic mosquito introductions and range expansions on native species. The proliferation of global trade and travel makes the introduction exotic mosquito species highly likely (see [77,78] for reviews), whereas climate change is already changing native species distributions [3].
 

3. A Changing Australia and Its Consequences

The infection, amplification and transmission of the pathogens mentioned are often affected by environmental and climatic change (see [157] for a review). A study collating 19 articles concerning the impact of climate change on RRV outbreaks demonstrated that the complex ecology, interactions between social and environmental factors, and climate change and socioeconomic development needs to be considered when trying to understand the ecology of RRV and prevent/reduce viral transmission [158]. Climate change can influence mosquito and wildlife distribution directly and/or indirectly by changing behaviors or movements. For example, while rainfall is predicted to decrease in certain areas of Australia, sea levels are predicted to increase which can potentially create another source of water for mosquito breeding [158]. This potential environmental change should be considered particularly for viruses that can be transmitted by various mosquito species. While the population of some mosquito species will decrease, others may consequentially thrive. Additionally, humans respond to climate change by altering their surroundings, which could influence the survival of wildlife and distribution of mosquito species depending on their ability to adapt. Human land-use change is one of the primary drivers of a range of infectious disease outbreaks and modifiers of the transmission of endemic infections [159]. Anthropophilic mosquito species such as Aedes aegypti often increase in response to urbanization, particularly taking advantage of man-made objects and preferentially feeding on human hosts [160].
Australia also has one of the highest extinction rates of mammalian fauna in the world [161,162]. The surviving Australian species are currently threatened by competition and predation from a range of introduced mammalian species, the low levels of conservation funding compared to other countries and the effects of climate change. The problem with losing biodiversity in Australia is that it can result in the loss of a “dilution effect”, which predicts that high host species richness can lower pathogen transmission [163]. This particularly applies to vectors that feed on multiple host species varying in their competence for a particular pathogen. For example, lower incidence of human WNV and Lyme disease has been observed in areas of the United States with greater host diversity [164,165]. Thus, continued population decline, and loss of species represents a significant public health threat in Australia.
There is also concern for the transmission of mosquito-borne diseases between countries. Other than migrating animal reservoirs such as birds and bats, increased human movements are now influencing mosquito and mosquito-borne disease distribution. Many mosquito species have been found to survive long-distance flights, including Anopheles mosquito species which transmits malaria [137,166]. Global travel and trade also enables the establishment of exotic zoonotic pathogens due to the availability of suitable vectors and hosts in many different countries [167]. It is therefore important to discuss the potential effects of such changes in Australia, particularly for future disease management purposes.

3.1. Climate and Its Significance to Australia’s Unique Vertebrate Communities

Climatically, higher temperatures have swept the whole of Australia and have created a dry landscape that is prone to bushfires. Bushfires have occurred in areas unaccustomed to fires, and are predicted to be more severe and frequent in the future [168]. Unexpected fires cause stress on wildlife, triggering immunosuppression, which increases the chances of infectious diseases [169]. Most recently in 2019, New South Wales, Queensland, South Australia and Victoria experienced intense bushfires [170], and undoubtedly have led to a decrease in wildlife populations [171]. Previous intense bushfires have caused devastating impacts on various marsupials including the koala [172], quokka [173], and possums [174].
Drought is a long term trend that is a natural part of the Australian hydroclimate; however, in addition to natural drought, the continuously changing agriculture and infrastructure landscape and societal context leads to a limited time to learn, adapt and prepare for droughts (see [175] for a review). While it is true that egg laying by mosquitoes decline during droughts, some mosquito species are able to retain their eggs for extended periods allowing them to search out remnant water sources during prolonged periods of drought [176]. Drought conditions may also increase the vector competence of Cx. quinquefasciatus for WNV by altering the immune response against the virus [177]. Increased temperatures associated with drought may also extend the length of disease transmission by increasing the normal seasonal activity of major vector species. For example in urban environments, Culex mosquitoes have been shown to breed earlier and extend their breeding season due to an increase in environmental temperatures [178]. Drought also leads to humans storing more water containers around houses, leading to increased mosquito breeding and disease outbreaks, particularly diseases associated with container-inhabiting species like dengue, chikungunya, and Zika [179,180].
Increased drought will also likely affect the abundance and distribution of competent vector species. In Australia, repeated drought events have decreased the survival and reproductive fitness of some smaller marsupials. After experiencing drought, the female agile antechinus (Antechinus agilis) survival and number of young per litter decreased and some females failed to give birth [181]. The brush-tailed phascogale (Phascogale tapoatafa) delayed births by increasing period of sperm storage beyond the drought and while beneficial, would decrease populations if the drought was long-term [182]. Bigger marsupials such as kangaroos change their distribution depending on drought and rainfall, with red kangaroo (Macropus rufus) populations moving long distances and aggregating at areas with a higher quality food supply and water [183]. Higher temperatures also lead to heat stress, which coincides with larger admissions of Australian birds and marsupials into veterinary clinics [184]. It is also important to mention that some Australian animals have a proven ability to cope with higher temperatures, however many also suffer from heat stress [185].

3.2. Climate and Its Significance to Mosquitoes

Climatic factors influence mosquito breeding and disease transmission [9]. The Australian continent has increased in temperature by 0.9 °C between 1910 to 2011, which is higher than the global temperature increase of 0.7 °C [186]. Predicted climate change in Australia will likely increase the distribution of Australian vector-borne diseases such as RRV [187]. Disease distribution also relies on the type of vector and its efficiency in spreading disease. For example, the Ae. aegypti population in Australia migrated from Western Australia, Northern Territory and New South Wales to Queensland, which led to repeated outbreaks of dengue [188]. Thus, the spread of disease will ultimately rely upon the distribution of suitable vector species. The distribution of the principal vectors of dengue, malaria, and other global vector-borne diseases are projected to increase considerably under current climate change scenarios as warming temperatures will allow them to spread to areas previously unsuitable for survival [189,190,191]. If correct, such increases will surely result in the spread of disease to previously uninfected areas. Although transmission of vector-borne diseases can be limited by seasonal temperature change in temperate environments [192], many mosquito species have proven highly adaptable to survive in areas of lower humidity [193] and even in areas that under winter [194].
Rising sea levels in response to climate change will dramatically change shoreline hydrology, causing marshes and seagrass beds to migrate landward, and will push salinity up the estuary [195]. The landward expansion of saline habitat may increase the risk of vector-borne disease outbreaks in many regions of the world by increasing the distribution of salt-associated mosquito species [196]. In Australia, the major salt marsh mosquitoes Ae. vigilax and Ae. camptorhynchus are important vectors of RRV and BFV [16] and any increase in their distributions represents a significant public health threat [197]. In addition to increased disease risk, the landward expansion of saline environments will increase the already extreme biting nuisance potential of these species [198,199] decreasing the quality of life in may coastal areas.

3.3. Urbanization and Habitat Fragmentation

Ecological change resulting from land-use modification often leads to the transmission of infectious diseases from wild animals to humans [200], and Australia is no exception. Vector-borne disease outbreaks from Australian wildlife almost always involve the installation of wetlands, encroachment of residential developments on reclaimed coastal wetlands or remote locations and deforestation (see [201] for a review). Although urbanization has led to the decline of certain marsupial populations due to decreased habitat [202,203], the impacts of such reductions on endemic arboviruses is not currently known.
Deforestation also leads to changes in wildlife movements, either away from the development, or adapting to human settlement. Whereas, urbanization decreases host species richness, as only some are capable of adaptation. Marsupials such as koalas have been historically and significantly affected by changing landscapes. As koalas are specialized feeders of predominantly Eucalyptus and Corymbia species, their diet also varies within regional areas due to different soil characteristics, tree structures, leaf water, and chemical content [204,205], which makes it difficult for koalas to adapt with the cumulative threats from environmental and landscape changes. They are also threatened by disease (i.e., chlamydial infections and koala retrovirus) and stress from habitat fragmentation or clearing, is expected to result in population decline (see [206] for a review). Some koala populations persist in urban landscapes where resources are available; however, patchy resources also increase their risk of death [207]. Reduced nutritional and population health likely compromise immunological fitness [208] and enhance the potential of some koala species to act as reservoirs or reduce the removal of certain pathogens from a host.
Even marsupials that are found in high densities in urban landscapes have been affected by urbanization and human population growth. The eastern grey kangaroo declined in overall population by 42% in south east Queensland, with a further decline anticipated with the increase of humans [202]. Additionally, land clearing and timber harvesting have also had an impact on the structure and distribution of various marsupial species because of the change in predation and food availability. For example, eastern grey kangaroos prefer the relatively open foraging sites for grazing and swamp wallabies prefer dense vegetation sites for feeding, suggesting that there will be changes of marsupial distribution depending on specific preferences of the species (see [209] for a review). Koalas from south east Queensland, Australia are more exposed to major RRV mosquito vector, Cx. annulirostris, because of their confinement to edges of permanent wetlands that are not suitable for urban development [89]. However, while some Australian wildlife species are struggling to adapt to rapid environmental and climatic change, some are proliferating. Possums, for example, have been seen thriving in urban environments as they are more tolerant of disturbances compared to other marsupials [203,210]. While this is good for the maintenance of the possum population, it is also suspected that they might cause disease outbreaks in urban areas due to the lack of biodiversity and the close proximity to humans or domestic animals [211].
 
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