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INTRODUCTION
Mosquitoes (Diptera: Culicidae) are the world’s deadliest animals,1 vectoring myriad pathogens that result in untold pain and misery. Seventy nine native mosquito species are known from Canada,2–4 though several more are suspected to occur based on their distributions in the United States,4 and five invasive species are currently known.2,4,5 In this review, we define invasive mosquitoes as those that have been accidentally or deliberately introduced into areas beyond their native range and whose presence negatively impact the environment, the economy, or the society including human and animal health.6 Invasive mosquitoes threaten human and animal health as they can vector pathogens not previously known from Canada, or act as more efficient vectors of native pathogens. While the permanent establishment of many exotic mosquito-borne pathogens discussed here is unlikely in Canada, this may not always be the case due to novel mutations or climate change. Furthermore, localized seasonal outbreaks resulting from travel-related or other imported cases have occurred elsewhere.7 With increasing globalization and the landscape of emerging pathogens constantly changing, and as demonstrated by literature for other areas,8 an entomological, medical, and veterinary knowledge of the invasive mosquitoes of Canada is more important than ever.
IMPORTANT MOSQUITO-BORNE PATHOGENS CURRENTLY OR FORMERLY ENDEMIC TO CANADA
Snowshoe hare virus (SSHV; Family: Bunyaviridae, genus: Bunyavirus) undergoes an enzootic transmission cycle in wild mammals with mosquitoes with non-Culex mosquitoes acting as the primary vectors.9 It is not clear what species are the principal hosts of SSHV, although small mammals are thought to be important in SSHV maintenance and amplification.9 Snowshoe hare virus is found across Canada10 as well as Alaska11 and parts of northern Eurasia.12 This virus has been reported to cause clinical encephalitis in humans,13 predominantly in children,9 and horses.14
Dog heartworm, Dirofilaria immitis, is a parasitic filarial worm that is an obligate parasite of mosquitoes and canids,15 although rare cases in other animals, such as humans, also occur.16 Endemic foci of D. immitis occur in many parts of Canada, particularly southern regions.17,18 A variety of mosquito species in the genera Aedes, Culex, and Anopheles vector D. immitis.19
West Nile virus (WNV; Family: Flaviviridae, genus: Flavivirus) undergoes an enzootic transmission cycle in avian hosts with mosquitoes in the genus Culex acting as primary vectors,20,21 though other mosquitoes with wide host ranges can carry WNV as well.22 The primary vectors of WNV in Canada are Culex pipiens and Cx. restuans in Eastern Canada, and Cx. tarsalis in Western Canada.20–25 Culex spp. are often ornithophilic, with some species feeding on humans as well. Ornithophilic biting behavior in the spring, by early emerging Culex spp. (such as Cx. restuans in Ontario) may vector enzootic transmission within local or migratory bird populations.26 During late summer vector species such as Cx. tarsalis or Cx. pipiens may increase their biting of humans27 leading to the transmission of WNV from birds to humans. West Nile virus first arrived in North America in 1999,28 and was first detected in Canada during 2001 in Ontario.29 By 2009, it had spread all the way west to British Columbia.25 West Nile virus can cause disease in several animals, including mortality in horses and birds.30,31
St. Louis encephalitis virus (SLEV; Family: Flaviviridae, genus: Flavivirus) undergoes an enzootic transmission cycle among birds and is vectored mainly by mosquitoes of the genus Culex.32 It may undergo vertical transmission and persist in mosquitoes through winter.32,33 During the 1970s, Canada experienced epidemics of SLEV, with the virus reported in Saskatchewan, Manitoba, Ontario, and Quebec,10 although in the United States it has been reported from coast-to-coast but predominantly in the southern States.32 St. Louis encephalitis virus can cause disease in horses as well.34
Jamestown Canyon virus (JCV; Family: Peribunyaviridae, genus: Orthobunyavirus) is transmitted primarily among wild ungulates by non-Culex mosquitoes.9 One study in the eastern United States found more than 20 field-collected mosquito species tested positive for JCV, with Anopheles punctipennis, Coquillettidia perturbans, and several Aedes spp. incriminated as likely vectors.35 Jamestown Canyon virus is widespread in temperate North America and, while human infections and disease are rare, they are likely underrecognized.36
Cache Valley virus (CVV; Family: Peribunyaviridae, genus: Orthobunyavirus) is transmitted primarily among ungulates by non-Culex mosquitoes.9 In the Canadian prairies, CVV has been isolated from Aedes vexans, Culiseta incidens, and Culex tarsalis.37 In rare instances, CVV can cause disease in humans,38 and congenital malformations in sheep and goats.39,40
The human malaria parasite, Plasmodium vivax, is transmitted by mosquitoes of the genus Anophleles. Plasmodium vivax was formerly endemic to parts of Eastern Canada,41 and the southern interior of British Columbia.42 Contemporary imported cases continue to result in local malaria outbreaks.43
Eastern equine encephalitis virus (EEEV; Family: Togaviridae, genus: Alphavirus) undergoes an enzootic transmission cycle among passerine birds and mosquito vectors.32 Eastern equine encephalitis virus is vectored between birds by the mosquito Culiseta melanura,44 which does not bite humans.45 Transmission of EEEV to humans and other mammals occurs through mosquitoes that feed on passerine birds and mammals, including Coquillettidia perturbans, Cs. morsitans, Culex spp., and some mosquitoes of the genus Aedes.32,46 In Canada, EEEV is found in Ontario and Quebec and can cause mortality in humans and horses.44 Domestic poultry has been reported in some cases to suffer a decrease in egg production as a result of infection with EEEV,47 and even mortality.47
Western equine encephalitis virus (WEEV; Family: Togaviridae, genus: Alphavirus) is transmitted between birds and mammals by a variety of mosquitoes, although the western encephalitis mosquito, Cx. tarsalis, is thought to be the most important vector.32 Western equine encephalitis virus can cause mortality in humans and horses,32 and it may affect domestic poultry as well including decreased egg laying.48 In Canada, WEEV is found from British Columbia to the Great Lakes.10
SELECT EXOTIC PATHOGENS RELEVANT TO THIS REVIEW
Dengue virus (DENV; Family: Flaviviridae, genus: Flavivirus) is an arbovirus ubiquitous in the tropics that is vectored by some mosquitoes in the genus Aedes,49 primarily between humans but also nonhuman primates.50 There are several serotypes of dengue individuals who experience a subsequent infection with a different serotype are at increased risk of developing severe dengue.51
Japanese encephalitis (JEV; Family: Flaviviridae, genus: Flavivirus) undergoes enzootic transmission between birds and pigs and has recently spread from southeast Asia into Australia.52 This virus is the leading cause of encephalitis in eastern and southern Asia and is primarily vectored by mosquitoes of the genus Culex, although some Aedes spp. also act as vectors.52–54
Usutu virus (USUV; Family: Flaviviridae, genus: Flavivirus) is primarily vectored by Culex mosquitoes, and some members of the genus Aedes. Usutu virus was previously only known from Africa, but it has recently spread to Europe.55 Usutu virus primarily circulates in humans and birds, where it can cause encephalitis in humans56 and has caused severe mortality in bird populations that have not developed immunity.55
Yellow fever virus (YFV; Family: Flaviviridae, genus: Flavivirus) is transmitted among humans and other primates primarily by some Aedes, Sabethes, and Haemogogus mosquitoes.57 There is a vaccine for YFV; however, it has historically been considered a very dangerous pathogen.57 Yellow fever virus is primarily tropical in distribution; however, sporadic outbreaks have occurred as far north as New York City and Philadelphia,57 and there is risk of travel-related cases initiating autochthonous transmission cycles.58
Zika virus (ZIKV; Family: Flaviviridae, genus: Flavivirus) is transmitted between nonhuman primates and humans, primarily by many mosquitoes of the genus Aedes, although there are other transmission routes.59 Travellers returning from areas with endemic ZIKV may be at risk of initiating autochthonous transmission if competent vectors are present.59
Chikungunya (CHIKV; Family: Togaviridae, genus: Alphavirus) is primarily vectored by some Aedes mosquitoes.60 Nonhuman primates serve as potential reservoir or amplifying hosts,60 although vertical transmission in mosquitoes has also been reported.61
La Crosse virus (LACV; Family: Peribunyaviridae, genus: Orthobunyavirus) is the primary cause of viral encephalitis in children in the United States.9 The primary LACV vectors, Aedes triseriatus and Ae. albopictus, have a limited distribution within Canada.4,5
Rift Valley fever (RVFV; Family: Phenuiviridae, genus: Phlebovirus) is known from Africa and Arabia where it causes morbidity and mortality in humans and ruminants and is vectored by several pathways, including mosquitoes of a variety of genera.62
INVASIVE MOSQUITOES KNOWN FROM CANADA
Aedes aegypti distribution.
The yellow fever mosquito, Aedes (Stegomyia) aegypti (L.), originated in sub-Saharan Africa where its sylvatic form can still be found today.63 As it adapted to a synanthropic lifestyle, this species managed to spread to tropical and subtropical areas around the globe via human-assisted dispersal, particularly in association with ship traffic connected with the slave trade.64 One of the most globally widespread species in tropical and subtropical environments, Ae. aegypti has been present in North America for centuries but is intolerant of temperate winters.65 While Ae. aegypti has historically been limited to areas with mean January temperatures above 10°C,65 there are sporadic northern populations that exist in areas where mean January temperatures get as low as about 2°C.66 Habitat models for Ae. aegypti do not predict suitable year-round climate conditions for this species in Canada now or in the near future.67,68
In 2016 and 2017, low numbers of Ae. aegypti were reported from Southern Ontario, representing the first records of this species in Canada5 (Figure 1). A record from southern Quebec in the summer of 2017 also exists.69,70 Although these records are believed to represent transient incursions,5 Ae. aegypti is thought to have managed to persist through the winter in other cooler locales as larvae in warm subterranean microenvironments.66
Female Aedes aegypti, photo by Adam Blake. This figure appears in color at www.ajtmh.org.
Citation: The American Journal of Tropical Medicine and Hygiene 107, 2; 10.4269/ajtmh.21-0167
Female Aedes aegypti, photo by Adam Blake. This figure appears in color at www.ajtmh.org.
Citation: The American Journal of Tropical Medicine and Hygiene 107, 2; 10.4269/ajtmh.21-0167
Female Aedes aegypti, photo by Adam Blake. This figure appears in color at www.ajtmh.org.
Citation: The American Journal of Tropical Medicine and Hygiene 107, 2; 10.4269/ajtmh.21-0167
Life history.
Historically, a sylvatic tree-hole breeder that fed on animals, almost all populations of Ae. aegypti now preferentially blood-feed on humans,63,71–73 are adapted to human-altered habitats, and breed in a wide variety of artificial containers such as tires, gutters, vases, and buckets74 as well as indoor and underground aquatic habitats.75 Eggs are deposited near the water surface, hatch when the water level rises, and are resistant to desiccation.72,76,77 They are aggressive biters that can feed on multiple hosts during a single gonotrophic cycle, increasing the risk of pathogen transmission.78 Adult female Ae. aegypti are primarily diurnal79,80 and readily enter human habitations to seek a blood meal or rest72; however, they are weak fliers and don’t often fly more than a few hundred meters from breeding sites unless inadvertently transported by humans.81
Taxonomy and identification.
Aedes aegypti is a small black mosquito with stripes of white scales on the tarsomeres and a lyre-shaped pattern of white scales on the scutum74,82 (Figure 2). It looks similar to Ae. sierrensis, Ae. albopictus, Ae. japonicus, and Orthopodomyia spp.; however, the presence of white scales on both the base and apex of tarsomeres of Ae. sierrensis, prominent longitudinal middorsal white stripe of Ae. albopictus, the bronze-scaled lyre-shaped pattern on the scutum of Ae. japonicus, and the lack of distinct stripes of white scales on the fore tarsi of Orthopodomyia spp. can be used to separate these species from Ae. aegypti.
Collection records of Aedes aegypti in Canada.5,70 Note that these records are of ephemeral introductions that are not believed to represent established populations. This figure appears in color at www.ajtmh.org.
Citation: The American Journal of Tropical Medicine and Hygiene 107, 2; 10.4269/ajtmh.21-0167
Collection records of Aedes aegypti in Canada.5,70 Note that these records are of ephemeral introductions that are not believed to represent established populations. This figure appears in color at www.ajtmh.org.
Citation: The American Journal of Tropical Medicine and Hygiene 107, 2; 10.4269/ajtmh.21-0167
Collection records of Aedes aegypti in Canada.5,70 Note that these records are of ephemeral introductions that are not believed to represent established populations. This figure appears in color at www.ajtmh.org.
Citation: The American Journal of Tropical Medicine and Hygiene 107, 2; 10.4269/ajtmh.21-0167
Public health and veterinary importance.
Aedes aegypti is thus far only believed to present in Canada on a seasonal basis during the summer months.5 However, Ae. aegypti is a principal vector of several important arboviruses including DENV,72 YFV,72 ZIKV,83 and CHIKV.84 The CHIKV and ZIKV are among the most frequent travel-acquired pathogens in Canada,9,85,86 and the presence of Ae. aegypti in Canada, even on an ephemeral basis, raises concerns for autochthonous seasonal transmission of imported arboviruses.
Aedes albopictus distribution.
The Asian tiger mosquito, Aedes (Stegomyia) albopictus (Skuse), is native to southeast Asia but has expanded is range to include an almost global occupation of tropical to temperate habitat.67 Its intercontinental dispersal is thought to be largely due to its use of used tires as breeding habitat,87,88 and within continents it is likely to spread via human-assisted means such as car travel.89
Aedes albopictus was first detected breeding in the United States in 198590