Journal of the American Mosquito Control Association, 37(2):101–105, 2021 Copyright Ó 2021 by The American Mosquito Control Association, Inc. SCIENTIFIC NOTE

RESPONSE OF MOSQUITOES ASSOCIATED WITH ESTUARINE WETLANDS TO BUSHFIRE IN AUSTRALIA

1,2 3 3 CAMERON EWART WEBB, RAFFAELE CATANZARITI AND STEVEN HODOSI

ABSTRACT. The response of mosquitoes to bushfire is poorly understood. During the 2019–20 summer, many regions of Australia were impacted by devastating bushfires. An area of estuarine and brackish-water wetlands

alongside the Georges River, Sydney, New South Wales, was burned in January 2020. Mosquito populations within Downloaded from http://meridian.allenpress.com/jamca/article-pdf/37/2/101/2855383/i8756-971x-37-2-101.pdf by guest on 28 September 2021 the area were monitored as part of the local authority’s mosquito management program, providing a unique opportunity to record the response of key mosquitoes of pest and public health concern to bushfire. Ground pools within a tidally influenced swamp oak forest dominated by Casuarina glauca and associated wetlands dominated by Phragmites australis and Bolboschoenus spp. had been identified as suitable habitat for a range of mosquitoes, including Aedes alternans, Ae. vigilax, and Verrallina funerea. Surveys of immature stages of mosquitoes within recently burned habitats inundated by tides demonstrated that mosquito eggs survived the direct and indirect impacts of fire and immature stages successfully completed development as reflected in concomitant changes in adult mosquito populations following the bushfire. This unique observation has implications for mosquito management following bushfire in Australia and internationally.

KEY WORDS Aedes alternans, Aedes vigilax, Verrallina funerea, wetlands, wildfire

Mosquitoes associated with coastal regions of has been identified from the region that are of pest Australia are of significant pest and public health and public health concern, the dominant species is importance (Webb et al. 2016). Notwithstanding the Ae. vigilax. The productive mosquito habitats are nuisance-biting impacts abundant mosquito popula- tidally influenced salt marshes (dominated by tions have on coastal residential communities and Sarcocornia quinqueflora (Bunge ex Ungen-Stern- recreational activities, the health risks associated berg) A.J. Scott), mangrove forests (dominated by with mosquitoes are of increasing concern for local Avicennia marina L.),andswampoakforests authorities. The most commonly reported mosquito- (dominated by Casuarina glauca Sieber ex Sprengel borne disease in Australia is caused by Ross River and Melaleuca spp.). There are also brackish-water virus and while dozens of mosquito species have and freshwater wetlands dominated by various been implicated in its transmission, one of the key macrophytes (e.g., Juncus spp., Bolboschoenus spp., vectors in coastal regions is considered Aedes vigilax Phragmites australis (Cavanilles) Trinius ex Steudel) (Skuse) (Ryan et al. 2000, Claflin and Webb 2015). in addition to ephemeral ground pools in terrestrial This is an often very abundant mosquito that is a woodlands and water-holding containers and other known nuisance-biting pest and disperses widely water-holding infrastructure associated with residen- from larval habitats (Webb et al. 2016, Claflin and tial areas. In addition to Ae. vigilax, there is a suite of Webb 2017, Webb and Russell 2019). This mosquito other key mosquitoes of pest and public health is typically associated with tidally influenced habi- concern in the local area (Crocker et al. 2017) and tats, most commonly estuarine wetlands including local authorities undertake routine surveillance of salt-marsh and mangrove communities (G´ıslason and mosquito populations and regularly issue warnings Russell 1997), and is a key target of mosquito control regarding mosquito-borne disease risk (Glasgow et programs in coastal regions (Webb and Russell 1999, al. 2018). Russell and Kay 2008). The 2019–20 summer in Australia was marked by The Georges River, which runs along the southern hot and dry conditions that led to catastrophic edge of the Sydney metropolitan region, contains a bushfires (often referred to as wildfire in other combination of estuarine, brackish-water, and fresh- countries) in many parts of southeastern Australia, water habitats and while a suite of mosquito species with .5 million ha burned and significant impacts on the local environment and wildlife (Dickman and McDonald 2020). On January 5, 2020, bushfire swept 1 Marie Bashir Institute for Infectious Diseases and Biosecurity, The University of Sydney, Sydney, NSW through a section of wetlands, swamp oak forest, and 2006, Australia. Eucalypt woodland alongside the Georges River in 2 Medical Entomology, NSW Health Pathology, West- the suburbs of Hammondville and Voyager Point, mead Hospital, Westmead, NSW 2145, Australia. New South Wales. An estimated 60 ha was burned, 3 Liverpool City Council, Locked Bag 7064, Liverpool including wetland areas where mosquito monitoring BC, NSW 1871, Australia. sites had already been established in association with

101 102 JOURNAL OF THE AMERICAN MOSQUITO CONTROL ASSOCIATION VOL. 37, NO.2 a mosquito control program undertaken by a local government authority (Liverpool City Council 2019). Mosquito monitoring commenced in early De- cember 2019 with approximately weekly adult mosquito trapping undertaken using carbon diox- ide–baited encephalitis virus surveillance traps (Rohe and Fall 1979) at 2 sites in the local area (Hammond- ville 3385701200 S, 15085800500 E; Voyager Point 3385702600 S, 15085800700 E). In addition, immature mosquito sampling was undertaken following tidal and/or rainfall inundation of habitats using a 300-ml dipper at 20 predetermined sampling sites to Downloaded from http://meridian.allenpress.com/jamca/article-pdf/37/2/101/2855383/i8756-971x-37-2-101.pdf by guest on 28 September 2021 determine the need for, and assess effectiveness of, larvicide applications (Webb and Russell 2001). Following the bushfire, an additional 10 sampling sites were established. All mosquito specimens were identified according to the taxonomic keys of Russell Fig. 1. Example of ground pools containing mosquito (1993) and pictorial guides of Webb et al. (2016). No larvae within swamp oak forest following bushfire impact mosquito control had been undertaken during these at Georges River, New South Wales, Australia. early stages of summer due to above average temperatures, below average rainfall, and a lack of vigilax (mean larval density 4.48 6 1.49 per dip) and extensive tidal inundation of local habitats. Due to Ae. alternans (mean larval density 0.06 6 0.06 per the prevailing environmental factors and a number of dip) and in partly burned habitats (n ¼ 14) with Ae. operational matters associated with bushfires, no vigilax (mean larval density 6.56 6 1.66 per dip) and mosquito control was undertaken at the site until Ae. alternans (mean larval density 0.14 6 0.12 per March 2020, outside the period discussed in this note. dip). Specimens of immature Verrallina funerea Prior to the bushfire, habitat and mosquito surveys (Theobald) were also collected but at very low were undertaken on December 19, 2019, and abundances (mean larval density ,0.05 per dip; n ¼ December 28, 2019, following partial tidal inunda- 20). This mosquito is rarely collected locally given tion of the area. Immature stages of Ae. vigilax (mean this species is close to its known southern geographic larval density 2.13 6 0.71 per dip; n ¼ 20) and Ae. limit (Webb et al. 2016). alternans (Westwood) (mean larval density 0.06 6 Given the short time between the bushfire, tidal 0.05 per dip; n ¼ 20) were collected. This difference inundation of habitats, and hatching of immature in relative abundance was not surprising given that stages, it seems highly likely that the eggs of these the larvae of Ae. alternans are predatory (Webb et al. mosquitoes survived the fire. While it is not possible 2016) and typically collected at much lower densities to rule out completely that eggs were laid shortly than Ae. vigilax (Webb and Russell 2001). No larval after the fire and then hatched on inundation, given abundance data were recorded on December 28, 2019, given the extremely limited areas of habitats adult mosquito monitoring suggested adult mosquito inundated. populations had sharply declined immediately after Postbushfire, these habitats were again inundated the fire (Table 1), it is concluded that there was by tides, and much more substantially than during the unlikely to be substantial oviposition throughout the previous month, between January 10–14, 2020 area during the short period between bushfire and (approximately 2 wk following the bushfires). tidal inundation of wetlands. There is also generally a Surveys of immature mosquitoes within ground period of at least 48–52 h of embryonic development pools remaining following retreat of tides were after oviposition before hatching (Sinclair 1976) that undertaken on January 14, 2020, and included a would likely further reduce the likelihood that the range of ground pools that were variously catego- larvae observed in these areas of burned wetland had rized as either burned or partly burned (Fig. 1). There hatched from eggs laid following the fire. While there were some small areas of habitat that remained only is some evidence that larvae of Ae. vigilax may be marginally impacted by fire, but these were not redistributed by movement of tidal water (Dale et al. sufficient to allow for a formal comparison of larval 1986), in this situation, it was unlikely that larvae densities. Habitats categorized as burned were those were redistributed from unburned areas outside these where all vegetation had been burned, whereas those study areas as there were no substantial areas of categorized as marginally burned that had the unburned habitat, apart from a few small unburned unburned vegetation remained within the ground areas described above, in close enough proximity to pools, but the surrounding vegetation and/or canopy the study site. The nature of the microtopography of cover had burned. the site also meant that tidal water tended to flow into Immature stages, mostly 3rd- to 4th-stage larvae, and out of the site through a series of smaller of a range of mosquito species were collected from tributaries connected to main creekline, as opposed to ground pools within fully burned (n ¼ 16) with Ae. traveling across the site as a whole, and unlikely to JUNE 2021 SCIENTIFIC NOTE 103

Table 1. Total adult mosquito abundance across 2 mosquito trap locations at Hammondville and Voyager Point adjacent to swamp oak forest, Georges River, New South Wales, Australia. Prebushfire Postbushfire Mosquito species Dec 15, 2019 Dec 29, 2019 Jan 6, 2020 Jan 12, 2020 Jan 19, 2020 Jan 26, 2020 Feb 2, 2020 Aedes alternans 0110347 Ae. camptorhynchus 0000001 Ae. flavifrons 0000011 Ae. multiplex 0000001 Ae. notoscriptus 2131529326034 Ae. procax 00000012

Ae. vigilax 265 255 58 18 570 615 916 Downloaded from http://meridian.allenpress.com/jamca/article-pdf/37/2/101/2855383/i8756-971x-37-2-101.pdf by guest on 28 September 2021 Anopheles annulipes 0392729 Coquillettidia linealis 0223100 Culex annulirostris 04630417 Cx. australicus 0001001 Cx. pipiens molestus 0010001 Cx. orbostiensis 0110000 Cx. quinquefasciatus 1411118113 Cx. sitiens 00010029 Mansonia uniformis 0000001 Verrallina funerea 0000100 Weekly totals 268 283 94 68 632 697 1,133

move larvae long distances between burned and any Australia (Ross et al. 2019). The observations unburned habitats. There is also little evidence that reported here demonstrate that the eggs of some the unhatched eggs of Ae. vigilax are redistributed by mosquitoes are tolerant to the impacts of bushfire; tidal flows (Ritchie 1994). this tolerance may be due to eggs being laid in A total of 3,175 mosquitoes were collected over microhabitats that provide a buffer against the the 7-wk sampling period, 2 wk before bushfire and thermal stress associated with bushfire. Eggs of Ae. 5 wk postbushfire, representing 17 species (Table vigilax are known to be desiccation resistant and 1). Adult mosquito collections made within 48 h of there is evidence that they can persist for extended the bushfire (January 6, 2020) demonstrated a sharp periods in the environment (Lee et al. 1984). There reduction in abundance. However, it should be is little information available on their susceptibility noted that with the lack of substantial rainfall and to extreme heat or indirect consequences of thermal tidal inundation of habitats in late December 2019, stress. While it would not be expected that eggs it would be expected that a decline in adult would survive direct exposure to fire, it is likely mosquito abundance is likely to have been observed that eggs, known to typically be deposited below an irrespective of the bushfire. Therefore, it is difficult accumulation of vegetation and debris, at the base to determine the relative impact of the bushfire on of dense vegetation (e.g., S. quinqueflora)orin the immediate decline in abundance of adult cracks within the sediments (Kay and Jorgensen mosquitoes. There was a substantial increase in 1986, G´ıslason and Russell 1997), were somewhat adult mosquito abundance, especially Ae. vigilax, insulated to lethal temperatures. Similarly, other from January 19, 2020, approximately 10 days mosquito species, especially Aedes spp., may following tidal inundation of local habitats. This survive bushfire-prone habitats where eggs are was consistent with the pattern of emergence of Ae. deposited in damp soil and base of vegetation vigilax following inundation of wetlands by tides or associated with depressions or rock pools within rainfall that trigger an egg hatch (Webb and Russell woodland or forest habitats (Webb et al. 2016). It is 2001, Claflin and Webb 2017). The continued important to note that without information on the abundance of Ae. vigilax over subsequent weeks specific temperatures mosquito eggs were exposed strongly suggests that survivorship and emergence to, it is difficult to draw conclusions on specific from immature mosquitoes recorded within burned thermal tolerances. habitats was relatively high and that conditions The observations reported here are consistent with within the burned habitats did not adversely impact the limited published accounts of fire and impact on larval survivorship. It was beyond the scope of mosquitoes elsewhere, due either to the wildfire or existing monitoring program to sample more intentional use of fire as a mosquito control strategy. frequently following the bushfire to confirm survival Wildfire has been observed having an impact on the rates of immature stages. pest mosquito Culex salinarius Coq. in Texas, where There is a paucity of information on the impact mosquito populations rapidly declined and took of bushfire in coastal wetlands on fauna and flora in months to recover following fire (Janousek and 104 JOURNAL OF THE AMERICAN MOSQUITO CONTROL ASSOCIATION VOL. 37, NO.2

Olson 1994). Controlled burning of habitats where Dale PER, Hulsman K, Harrison D, Congdon B. 1986. the eggs of Ae. melanimon Dyar, Ae. nigromaculis Distribution of the immature stages of Aedes vigilax on a (Ludlow), and Ae. taeniorhynchus (Wied.) were coastal salt-marsh in south-east Queensland. Aust J Ecol present had been investigated as possible mosquito 11:269–278. Dickman C, McDonald T. 2020. Some personal reflections control strategies, but while it was reported that there on the present and future of Australia’s fauna in an was a decline in larval hatching from eggs exposed to increasingly fire-prone continent. Ecol Manag Restor fire, the decrease was not significant and nor was 21:86–96. there evidence that this approach would be a practical G´ıslason GM, Russell RC. 1997. Oviposition sites of the mosquito management strategy (Wilder and Takaha- saltmarsh mosquito, Aedes vigilax (Skuse) (Diptera: shi 1980, Wallace et al. 1990). 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