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Aedes japonicus japonicus (Diptera: Culicidae) arrives at the most easterly point in North America

DOI:10.4039/tce.2015.5
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Miles A. Fielden
Miles A. Fielden
Miles A. Fielden
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Andrew C. Chaulk at The University of Western Ontario
Andrew C. Chaulk
Kate Carson at Memorial University of Newfoundland
Kate Carson
Yolanda Wiersma at Memorial University of Newfoundland
Yolanda Wiersma
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Abstract and Figures

Aedes japonicus japonicus (Theobald) (Diptera: Culicidae), the Asian bush mosquito, is a keen biter linked to the transmission to humans of a variety of diseases. It has moved significantly from its historical Asian distribution, with its arrival in North America first noted in 1998 in New York and New Jersey, United States of America. Here we report the presence of A. j. japonicus within our collections of mosquitoes in the capital city of the easternmost province in Canada: St. John’s, Newfoundland and Labrador, in 2013. This observation provides further evidence of this mosquito’s ability to significantly expand its geographic range, potentially affecting connectivity between subpopulations globally.
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Aedes japonicus japonicus (Diptera: Culicidae)
arrives at the most easterly point in North America
Miles A. Fielden, Andrew C. Chaulk,
1
Kate Bassett, Yolanda F. Wiersma,
Mardon Erbland, Hugh Whitney, Thomas W. Chapman
Abstract—Aedes japonicus japonicus (Theobald) (Diptera: Culicidae), the Asian bush mosquito, is a
keen biter linked to the transmission to humans of a variety of diseases. It has moved significantly from
its historical Asian distribution, with its arrival in North America first noted in 1998 in New York and
New Jersey, United States of America. Here we report the presence of A.j.japonicus within our
collections of mosquitoes in the capital city of the easternmost province in Canada: St. John’s,
Newfoundland and Labrador, in 2013. This observation provides further evidence of this mosquito’s
ability to significantly expand its geographic range, potentially affecting connectivity between
subpopulations globally.
Résumé—Aedes japonicus japonicus (Theobald) (Diptera: Culicidae), le moustique asiatique Bush,
transmet aux humains une variété de maladies via ses piqûres. L’espèce a augmenté son aire de
distribution de façon significative, à partir d’une répartition historique en Asie jusqu’à son arrivée en
Amérique du Nord en 1998, à New York et à New Jersey, Les états-unis d'Amérique. Nous rapportons
ici la présence d'A.j.japonicus dans nos collections de moustiques dans la capitale provinciale la plus à
l’est au Canada, St Jean, Terre-Neuve, en 2013. Cette observation fournit une preuve supplémentaire
de la capacité de ce moustique d'élargir considérablement son aire de répartition, impactant
potentiellement la connectivité entre les sous-populations à l'échelle mondiale.
Aedes japonicus japonicus (Theobald) (Diptera:
Culicidae) is an aggressive biter (Kampen and
Werner 2014) with one study estimating that over
one third of its blood meals are taken from
humans (Molaei et al. 2009). In part due to its
willingness to bite humans, it is a competent
vector of disease for humans in both its native
(Takashima and Rosen 1989) and expanded range
(Turell et al. 2001). Aedes j. japonicus, native to
eastern Asia, was first documented in North
America in 1998 when specimens were collected
during a standard mosquito collection program in
New York and New Jersey, United States of
America (Peyton et al. 1999). Since its initial
introduction to North America, A.j.japonicus has
spread rapidly and is now found in over 30 states
in the United States of America (Kampen and
Werner 2014). In 2001, the first collections of this
species were made in Canada (southern Ontario
and Québec) during an annual West Nile virus
surveillance programme (Thielman and Hunter
2006). The mosquito species has since spread east
in Canada, through Québec and New Brunswick
by 2005 and Nova Scotia by 2008 (J. Ogden,
Department of Natural Resources, Nova Scotia,
Canada, personal communication).
While insular Newfoundland is geographically
isolated from mainland Canada, non-native
insects have been known to arrive through various
routes (e.g., drift migration via air currents),
making direct mosquito migrations possible
(Morris 1983). There is also potential for insect
transfer through travel and commerce (Reiter and
Sprenger 1987). Sampling of the mosquito fauna
of insular Newfoundland in 2005 (Hustin 2006)
and in 2011 (K.B., personal observation) did not
M.A. Fielden, A.C. Chaulk,
1
K. Bassett, Y.F. Wiersma, M. Erbland, T.W. Chapman, Department of Biol-
ogy, Memorial University, St. John’s, Newfoundland, Canada A1B 3X9
H. Whitney, Animal Health Division, Newfoundland and Labrador Department of Natural Resources, St. John’s,
Newfoundland, Canada
1
Corresponding author (e-mail: a.chaulk@mun.ca).
Subject editor: David McCorquodale
doi:10.4039/tce.2015.5
Received 19 June 2014. Accepted 6 November 2014.
Can. Entomol. 00:1–4 (2015) © 2015 Entomological Society of Canada
1
include A.j.japonicus within their collections.
However, in 2013 A.j.japonicus larvae did
appear within an array of containers that were
placed (with some experimental attractants, see
below) in search of another container breeder,
Culex pipiens Linnaeus (Diptera: Culicidae). The
appearance of A.j.japonicus was unanticipated
and, consequently, any life history details that can
be gleaned from this initial sampling are limited in
scope. However, A.j.japonicus was the most
abundant within our collections suggesting a rapid
spread after introduction that is characteristic of
this species (Kaufman and Fonseca 2014).
Twenty-seven containers (potential oviposition
sites) were deployed at residential or residential-
adjacent sites within the city of St. John’s,
Newfoundland and Labrador, Canada, non-
systematically covering an area of ~4 km
2
. Each
container was an 11.4 L translucent white plastic
bucket measuring 34 cm high with a radius of
10.3 cm. A volume of attractant solution was
added to each trap sufficient to result in a depth of
5 cm (~1.7 L). The attractant solutions that we
describe here were part of an experiment investi-
gating the use of an established attractant (grass:
Allan et al. 2005), a potential attractant (white
button mushrooms containing 1-octe-3-ol:
Berendsen et al. 2013; Mathew et al. 2013) and a
unique local ingredient, indeterminately aged
moose feces (collected from Salmonier Nature
Park, Newfoundland and Labrador). Fielden
(2014) contains a full description of this experi-
ment and outcomes. Attractant solutions that were
used within the area that lured A.j.japonicus
consisted of either mushrooms, moose feces, or a
mixture of the two aforementioned solutions and
grass clippings (collected from the St. John’s area)
blended with 5 L of tap water in each case. Of
particular note, during the period this manuscript
was in submission, we observed A. j. japonicus
adults emerging from a bucket containing rain-
water and cigarette butts. An identical comment
was made by Thielman and Hunter (2006). Both
notes highlight the enormous range of larval
habitats these mosquitoes are capable of using.
Traps were positioned in the shade beneath
trees to reduce evaporation rate of the attractant
solution. Also, increased shade cover is known
to increase pupal productivity (Vezzani and
Albicocco 2009). Aedes japonicus japonicus larvae
were collected from nine of the 27 containers.
Buckets were monitored weekly and when larvae
were detected they were collected and trans-
ferred to mosquito breeders (BioQuip, Rancho
Dominguez, California, United States of America)
that were kept in a laboratory with windows open,
such that the temperature approximated exterior
conditions.
Emerged adult mosquitoes were killed by
freezing, pinned and identified to species using
Darsie and Ward (2005). Identification was cor-
roborated and a voucher specimen was retained
by The National Identification Service of Agri-
culture and Agri-Food Canada (Ottawa, Ontario,
Canada). Additional specimens are available
in room SN-4113 at Memorial University of
Newfoundland. In total, 99 A.j.japonicus adult
females emerged from the collected larvae. The
eclosion of larvae in the laboratory occurred
between 13 August and 29 September 2013.
Additionally, a single adult specimen that was
naturally seeking a blood meal from a human was
Fig. 1. Photograph of Aedes japonicus japonicus
from the area of Devereaux Lane, Outer Cove,
Newfoundland and Labrador, Canada during the
evening of 24 September 2013. Mardon Erbland took
the photograph using a Canon EOS-1D Mark IV
camera equipped with a Canon MP-E 65 mm f/2.8
1–5× Macro Photo lens and Canon Macro Twin Lite
MT-24EX flash. A manual exposure (f/16, 1/160 sec,
ISO 250) and manual flash were used. The image
shows both the characteristic lyre shaped pattern of
gold coloured thoracic scales, and silvery-white scale
patches on the lateral thorax and abdomen indicative
of this species (Darsie and Ward 2005).
2 Can. Entomol. Vol. 00, 2015
© 2015 Entomological Society of Canada
photographed in Outer Cove, Newfoundland
and Labrador (~10 km north of St. John’s) on
24 September 2013 (Fig. 1). This photograph,
submitted by M.E. to the citizen science website
NLNature.com (which is administered by Y.F.W.),
clearly shows the lyre shaped pattern of gold
coloured thoracic scales, and silvery-white scale
patches on the lateral thorax and abdomen
indicative of this species (Darsie and Ward 2005).
The detection of a new species for the province
via NLNature.com is an example of how citizen
science may contribute to early detection of range
expansions (Catlin-Groves 2012).
Our identification of A.j.japonicus in insular
Newfoundland marks an ultimate eastern bound-
ary of the species in North America. The intro-
duction and establishment of A.j.japonicus has
the potential to alter mosquito community
dynamics by outcompeting congeneric and inter-
generic mosquito species (Kaufman and Fonseca
2014). Consequently, this mosquito also holds
the potential to indirectly alter the viral risks
of a region and, therefore, requires monitoring
(Kaufman and Fonseca 2014). Kaufman and
Fonseca (2014) projected a continued but slowed
expansion of A.j.japonicus into more northern
regions of North America. The observations made
here support a continued expansion; however, the
speed of the expansion requires more substantial
evaluation. A study focused on the geographic
connectivity of Newfoundland and Labrador
populations with populations in neighbouring and
distant regions is currently underway.
Acknowledgements
The authors thank the funding bodies that
enabled this work: Natural Sciences and Engineer-
ing Research Council of Canada; Animal Health
Division, Newfoundland and Labrador Department
of Natural Resources; Memorial University. They
are grateful for the help of H. E. Caravan, P.G.
Chaffey, P. J. Coates III, and S.C. Dufour.
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The Asian bush mosquito Aedes japonicus, endemic to East Asia, is one of the most expansive mosquito species in the world and has as yet established in 15 countries of Europe. Within Germany, the species has been spreading tremendously during the last years, and its four once geographically isolated populations were on the verge of merging in 2017. To reveal relationships and carry-over ways between the various populations, and thus, migration and displacement routes, the genetic make-up of Ae. japonicus from ten different locations throughout its German distribution area was investigated. For this purpose, a part of the mitochondrial DNA (nad4 gene) of collected specimens was sequenced and seven loci of short tandem repeats (microsatellites) were genotyped. When related to similar genetic studies carried out between 2012 and 2015, the results suggest that admixtures had since occurred, but no complete genetic mixture of populations had taken place. At the time of sampling for the present study, the western collection sites were still uniform in their genetic make-up; however, a carry-over of individuals from the southeastern to the northern and southwestern German populations was determined. Further introductions from abroad are possible. In summary, the genetic diversity of Ae. japonicus in Germany had grown considerably, thus increasing ecological variability and adaptability of the species. At this point (10 years after the first detection), it is not possible anymore to draw conclusions on the origins of the populations.
Out of the bush: The Asian bush mosquito Aedes japonicus japonicus (Theobald, 1901) (Diptera, Culicidae) becomes invasive
Article
Full-text available
  • Feb 2014
The Asian bush or rock pool mosquito Aedes japonicus japonicus is one of the most expansive culicid species of the world. Being native to East Asia, this species was detected out of its original distribution range for the first time in the early 1990s in New Zealand where it could not establish, though. In 1998, established populations were reported from the eastern US, most likely as a result of introductions several years earlier. After a massive spread the mosquito is now widely distributed in eastern North America including Canada and two US states on the western coast. In the year 2000, it was demonstrated for the first time in Europe, continental France, but could be eliminated. A population that had appeared in Belgium in 2002 was not controlled until 2012 as it did not propagate. In 2008, immature developmental stages were discovered in a large area in northern Switzerland and bordering parts of Germany. Subsequent studies in Germany showed a wide distribution and several populations of the mosquito in various federal states. Also in 2011, the species was found in southeastern Austria (Styria) and neighbouring Slovenia. In 2013, a population was detected in the Central Netherlands, specimens were collected in southern Alsace, France, and the complete northeastern part of Slovenia was found colonized, with specimens also present across borders in adjacent Croatia. Apparently, at the end of 2013 a total of six populations occurred in Europe although it is not clear whether all of them are completely isolated. Similarly, it is not known whether these populations go back to the same number of introductions. While entry ports and long-distance continental migration routes are also obscure, it is likely that the international used tyre trade is the most important mode of intercontinental transportation of the mosquito. Aedes j. japonicus does not only display an aggressive biting behaviour but is suspected to be a vector of various disease agents and to displace indigenous culicid species. Therefore, Aedes j. japonicus might both cause public health problems in the future and have a significant impact on the biodiversity of the invaded territories.
Invasion Biology of Aedes japonicus japonicus (Diptera: Culicidae)
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Aedes japonicus japonicus (Theobald) (Diptera: Culicidae) has recently expanded beyond its native range of Japan and Korea into large parts of North America and Central Europe. Population genetic studies begun immediately after the species was detected in North America revealed genetically distinct introductions that subsequently merged, likely contributing to the successful expansion. Interactions, particularly in the larval stage, with other known disease vectors give this invasive subspecies the potential to influence local disease dynamics. Its successful invasion likely does not involve superior direct competitive abilities, but it is associated with the use of diverse larval habitats and a cold tolerance that allows an expanded seasonal activity range in temperate climates. We predict a continued but slower expansion of Ae. j. japonicus in North America and a continued rapid expansion into other areas as this mosquito will eventually be considered a permanent resident of much of North America, Europe, Asia, and parts of Hawaii.
Rickettsial infection in Amblyomma cajennense ticks and capybaras (Hydrochoerus hydrochaeris) in a Brazilian spotted fever-endemic area
Article
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  • Jan 2014
Brazilian spotted fever (BSF), caused by the bacterium Rickettsia rickettsii, is the deadliest spotted fever of the world. In most of the BSF-endemic areas, capybaras (Hydrochoerus hydrochaeris) are the principal host for the tick Amblyomma cajennense, which is the main vector of BSF. In 2012, a BSF case was confirmed in a child that was bitten by ticks in a residential park area inhabited by A. cajennense-infested capybaras in Itu municipality, southeastern Brazil. Host questing A. cajennense adult ticks were collected in the residential park and brought alive to the laboratory, where they were macerated and intraperitoneally inoculated into guinea pigs. A tick-inoculated guinea pig that presented high fever was euthanized and its internal organs were macerated and inoculated into additional guinea pigs (guinea pig passage). Tissue samples from guinea pig passages were also used to inoculate Vero cells through the shell vial technique. Infected cells were used for molecular characterization of the rickettsial isolate through PCR and DNA sequencing of fragments of three rickettsial genes (gltA, ompA, and ompB). Blood serum samples were collected from 172 capybaras that inhabited the residential park. Sera were tested through the immunofluorescence assay using R. rickettsii antigen. A tick-inoculated guinea pig presented high fever accompanied by scrotal reactions (edema and marked redness). These signs were reproduced by consecutive guinea pig passages. Rickettsia was successfully isolated in Vero cells that were inoculated with brain homogenate derived from a 3rd passage-febrile guinea pig. Molecular characterization of this rickettsial isolate (designated as strain ITU) yielded DNA sequences that were all 100% identical to corresponding sequences of R. rickettsii in Genbank. A total of 83 (48.3%) out of 172 capybaras were seroreactive to R. rickettsii, with endpoint titers ranging from 64 to 8192. A viable isolate of R. rickettsii was obtained from the tick A. cajennense, comprising the first viable R. rickettsi isolate from this tick species during the last 60 years. Nearly half of the capybara population of the residential park was seroreactive to R. rickettsii, corroborating the findings that the local A. cajennense population was infected by R. rickettsii.
The Citizen Science Landscape: From Volunteers to Citizen Sensors and Beyond
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  • Sep 2012
Within conservation and ecology, volunteer participation has always been an important component of research. Within the past two decades, this use of volunteers in research has proliferated and evolved into “citizen science.” Technologies are evolving rapidly. Mobile phone technologies and the emergence and uptake of high-speed Web-capable smart phones with GPS and data upload capabilities can allow instant collection and transmission of data. This is frequently used within everyday life particularly on social networking sites. Embedded sensors allow researchers to validate GPS and image data and are now affordable and regularly used by citizens. With the “perfect storm” of technology, data upload, and social networks, citizen science represents a powerful tool. This paper establishes the current state of citizen science within scientific literature, examines underlying themes, explores further possibilities for utilising citizen science within ecology, biodiversity, and biology, and identifies possible directions for further research. The paper highlights (1) lack of trust in the scientific community about the reliability of citizen science data, (2) the move from standardised data collection methods to data mining available datasets, and (3) the blurring of the line between citizen science and citizen sensors and the need to further explore online social networks for data collection.
Effects of the mushroom-volatile 1-octen-3-ol on dry bubble disease
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Dry bubble disease caused by Lecanicillium fungicola is a persistent problem in the cultivation of the white button mushroom (Agaricus bisporus). Because control is hampered by chemicals becoming less effective, new ways to control dry bubble disease are urgently required. 1-Octen-3-ol is a volatile that is produced by A. bisporus and many other fungi. In A. bisporus, it has been implicated in self-inhibition of fruiting body formation while it was shown to inhibit spore germination in ascomycetes. Here, we show that 1-octen-3-ol inhibits germination of L. fungicola and that enhanced levels of 1-octen-3-ol can effectively control the malady. In addition, application of 1-octen-3-ol stimulates growth of bacterial populations in the casing and of Pseudomonas spp. specifically. Pseudomonas spp. and other bacteria have been demonstrated to play part in both the onset of mushroom formation in A. bisporus, as well as the inhibition of L. fungicola spore germination. A potential role of 1-octen-3-ol in the ecology of L. fungicola is discussed.
Human Bloodfeeding by the Recently Introduced Mosquito, Aedes japonicus japonicus, and Public Health Implications
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Knowledge of the host-feeding behavior and extent of interactions with human hosts are important in evaluating the role and vector potential of invasive mosquitoes in transmission of native arboviruses. We collected blood-engorged females of the recently established exotic species Aedes japonicus japonicus from sites in New Jersey during 2000 to 2007 and identified the sources of vertebrate blood meals by sequencing portions of the cytochrome b gene of mitochondrial DNA. Over 1/3 (36%, n = 36) of the engorged mosquitoes acquired blood meals from humans. Other mammalian hosts included white-tailed deer (53%), fallow deer (5%), horse (3%), and Virginia opossum (3%). No avian, amphibian, reptilian, or mixed blood meals were identified. Our detection of a comparatively high prevalence of human bloodfeeding in Ae. j. japonicus in association with its local abundance, vector competence, and repeated detection of West Nile virus from field-collected specimens illustrates the potential for this invasive mosquito to serve as a "bridge" vector in transmission of West Nile and other mosquito-borne viruses in North America.
Introduced terrestrial insects.
Article
  • Jan 1983
Reviews the origin of Newfoundland's insect fauna, stressing the criteria for distinguishing introductions and patterns of arrival (early trade, ballast, human transport and migrants). An extensive list of introduced insects is provided, arranged taxonomically, with notes on probable time and means of arrival and on distribution. Introductions for biological control are listed separately, with notes on intended host, release sites and whether established.-P.J.Jarvis
Identification and Geographical Distribution of the Mosquitoes of North America, North of Mexico
Article
  • Jan 2006
Mosquito attractant blends to trap host seeking Aedes aegypti
Article
Aedes aegypti is the key vector of three important arboviral diseases -dengue, yellow fever and chikungunya. To identify volatile chemicals which could be used in odour based traps for Aedes mosquito surveillance, a few synthetic compounds and compound blends have been evaluated in an indigenously designed olfactometer. A total of 24 compounds and seven compound blends were screened against unfed adult female Ae. aegypti mosquitoes for attraction and compared with control group. The attractancy or repellency index of the test material to mosquitoes was calculated and rated them as class-1, class-2 and class-3 with rating values ranging 1-15, 16-33 and 34-100 respectively. Out of the 24 compounds tested, six were showing significant attractancy (P < 0.05) and among that 1-octene-3-ol showed maximum attractancy with a rating value of 57.81. Sixteen compounds showed significant repellency (P < 0.05) and among that with a rating value of 72.47, 1-hexene-3-ol showed strong repellent action against Ae. aegypti. All the seven blends showed significant mosquito attractancy (P < 0.05) and among that with a rating of 62.08 Myristic acid, Lactic acid and CO(2) blend exhibited first-rate mosquito attractancy.
The effect of shade on the container index and pupal productivity of the mosquitoes Aedes aegypti and Culex pipiens breeding in artificial containers
Article
The aim of this study was to assess whether certain attributes of larval breeding sites are correlated with pupal productivity (i.e. numbers of pupae collected per sampling period), so that these could be used as the focus for control measures to enhance control efficiency. Therefore, the objectives were to identify the months of highest pupal productivity of Aedes aegypti (L.) and Culex pipiens L. (Diptera: Culicidae) in an urban temperate cemetery in Argentina where artificial containers of < 6 L (flower vases) were the predominant breeding habitats, to compare various measures of the productivity of sunlit and shaded containers and to determine whether the composition of the containers affected pupal productivity. Over a period of 9 months, 200 randomly chosen water-filled containers (100 sunlit and 100 shaded), out of approximately 3738 containers present (approximately 54% in shade), were examined each month within a cemetery (5 ha) in Buenos Aires (October 2006 to June 2007). In total, 3440 immatures of Cx pipiens and 1974 of Ae. aegypti were collected. The larvae : pupae ratio was 10 times greater for the former, indicating that larval mortality was greater for Cx pipiens. Both mosquito species showed a higher container index (CI) in shaded than in sunlit containers (Ae. aegypti: 12.8% vs. 6.9% [chi(2) = 17.6, P < 0.001]; Cx pipiens: 6.3% vs. 1.8% [chi(2) = 24, P < 0.001]). However, the number and the density of immatures per infested container and the number of pupae per pupa-positive container did not differ significantly between sunlit and shaded containers for either species. Therefore, the overall relative productivity of pupae per ha of Ae. aegypti and Cx pipiens was 2.3 and 1.8 times greater, respectively, in shaded than in sunlit areas as a result of the greater CIs of containers in shaded areas. Neither the CI nor the number of immatures per infested container differed significantly among container types of different materials in either lighting condition. The maximum CI and total pupal counts occurred in March for Ae. aegypti and in January and February for Cx pipiens. The estimated peak abundance of pupae in the whole cemetery reached a total of approximately 4388 in the middle of March for Ae. aegypti and approximately 1059 in the middle of January for Cx pipiens. Spearman's correlations between monthly total productivity and monthly CI were significant at P < 0.001 for Ae. aegypti (r(s) = 0.975) and P < 0.01 for Cx pipiens (r(s) = 0.869). Our findings indicate that the efficacy of control campaigns against the two most important mosquito vectors in temperate Argentina could be improved by targeting containers in shaded areas, with maximum effort during species-specific times of year when pupal productivity is at its peak.