Impacts of climate change on high priority fruit fly species in Australia

Pacific [1, 2], and are yet to establish populations in Australia. Of the 11 species that are cur- rently present in Australia [1–3] (Table 1), seven are reported to cause significant economic losses (Bactrocera aquilonis, B. jarvisi, B. neohumeralis, B. musae, B. tryoni, Ceratitis capitata, and Zeugodacus cucumis) [1, 4]. Combined, these species infest a wide variety of hosts, with some (e.g. B. frauenfeldi, B. jarvisi, B. neohumeralis, B. tryoni and Ceratitis capitata) being highly polyphagous [3]. The distributions of Australia’s pest fruit fly species are influenced by their climatic toler- ances and the distributions of their hosts. Bactrocera originated in tropical regions, and have their highest richness in rainforests [5]. However, over the last 100 years, as horticulture has proliferated across Australia, some species have expanded their geographic range and host breadth [6]. Of the 11 high priority fruit fly species presently on the continent, three are cur- rently restricted to north-east Queensland (B. frauenfeldi, B. kraussi and B. musae) [7]. In con- trast, the geographic range of B. neohumeralis (Lesser Queensland fruit fly) extends along eastern Australia, from Queensland to central New South Wales (NSW) [3, 4, 7]. Previous cli- matic analysis indicates that this species also has the potential to establish elsewhere in north- ern Australia [4]. The remaining species have substantially wider climate tolerances, and are found across broad regions of the continent. For instance, B. tryoni (Qfly) ranges across much

of eastern Australia, eastern Queensland and northern regions of the Northern Territory [8]. Bactrocera jarvisi (Jarvis’ fruit fly) extends from northwest Western Australia, across the Northern Territory to northern Queensland and the Torres Strait Islands [4, 9], and in favour- able years may spread down the east coast of Australia into northern coastal NSW [4, 9]. Hence, B. jarvisi and B. tryoni have overlapping geographic ranges and infest many of the same hosts [4]. Ceratitis capitata (Medfly) originated in the Afrotropical region [10], and was introduced into the Perth area (Western Australia) in the late 1800s [4]. Before quarantine controls were developed, this species spread to NSW, Victoria, and other parts of Australia [11]. However, for reasons that remain unclear, Qfly is believed to have displaced Medfly throughout most of its former Australian range [12], and now Medfly is confined to Western Australia, with occasional detections in South Australia [13]. Given the threat that these 11 fruit fly species pose threats to Australia’s horticulture indus- tries, and to backyard growers, controlling them is imperative for the viability of Australian horticulture, necessitating in-farm management and pest treatment, monitoring to demon- strate pest freedom, and quarantine and trade restrictions [1, 2]. These controls, along with loss of market access, are estimated to cost Australian growers $100 million per annum [4], in addition to losses of up to $159 million per annum due to infestation of fruit and vegetable

crops [14]. The annual cost, as reported in 2012, of bait and cover spray, and post-harvest treatments, amounts to $269 ha-1 and $62.36 tonne-1, respectively [15], while maintaining fruit fly free areas is estimated to exceed $28 million per annum based on data from 2009–2011 [16]. However, restrictions were recently placed on the use of insecticides to control fruit flies due to concerns about toxicity [17], with dimethoate and fenthion suspended or highly restricted for many horticultural crops [17–20]. Other approaches, including Sterile Insect Techniques, are now being explored. Regardless, it has been estimated that the annual likeli- hood of an incursion by an exotic fruit fly species is 21% [15], and the annual cost of eradicat- ing these incursions is ~$13 million [16], with rapid responses to outbreaks being crucial for eradication success [21]. Even brief incursions can result in significant economic damage due to market access restrictions that may be imposed. However, climate change is likely to alter the distribution of suitable habitat for fruit fly species and the areas vulnerable to outbreaks, and this could have serious repercussions for Australian horticulture [22]. Previous studies [22–24] have used the semi-mechanistic species distribution model (SDM), CLIMEX, to estimate the potential geographic distributions of several high priority Impacts of climate change on high priority fruit fly species in Australia PLOS ONE | https://doi.org/10.1371/journal.pone.0213820 February 13, 2020 2 / 19 Industries, NSW; Biosecurity Queensland and the

Queensland Department of Agriculture and Fisheries; Department of Economic Development, Jobs, Transport and Resources, Victoria; and Department of Primary Industries and Regions South Australia (PIRSA)). Restrictions apply to the availability of these data, which were used under license for the current study. Climate data were sourced from WorldClim (http://www.worldclim. org), and are publicly available. Code availability All modelling and post-modelling analyses and calculation of statistics were performed in R version 3.1.2. We used the sp and raster packages for preparation and manipulation of spatial data, the dismo package to fit Maxent models, and custom R code for rapid projection of fitted models. Funding: "Project Raising Q-fly Sterile Insect Technique to World Standard (HG14033) is funded by the Hort Frontiers Fruit Fly Fund, part of the Hort Frontiers strategic partnership initiative developed by Hort Innovation, with co-investment from Macquarie University and contributions from the Australian Government." Competing interests: The authors have declared that no competing interests exist