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

RESEARCH ARTICLE Impacts of climate change on high priority fruit fly species in Australia Sabira SultanaID1,2*, John B. Baumgartner1,3, Bernard C. Dominiak4, Jane E. Royer5, Linda J. Beaumont1 1 Department of Biological Sciences, Macquarie University, North Ryde, New South Wales, Australia, 2 Department of Zoology, Jahangirnagar University, Savar, Dhaka, Bangladesh, 3 Centre of Excellence for Risk Analysis (CEBRA), School of BioSciences, University of Melbourne, Parkville, VIC, Australia, 4 New South Wales Department of Primary Industries, Orange, New South Wales, Australia, 5 Queensland Department of Agriculture and Fisheries, Biosecurity Queensland, Brisbane, Queensland, Australia * sabira.sultana@hdr.mq.edu.au Abstract Tephritid fruit flies are among the most destructive horticultural pests posing risks to Austra- lia’s multi-billion-dollar horticulture industry. Currently, there are 11 pest fruit fly species of economic concern in Australia. Of these, nine are native to this continent (Bactrocera aquilo- nis, B. bryoniae, B. halfordiae, B. jarvisi, B. kraussi, B. musae, B. neohumeralis, B. tryoni and Zeugodacus cucumis), while B. frauenfeldi and Ceratitis capitata are introduced. To varying degrees these species are costly to Australia’s horticulture through in-farm manage- ment, monitoring to demonstrate pest freedom, quarantine and trade restrictions, and crop losses. Here, we used a common species distribution model, Maxent, to assess climate suit- ability for these 11 species under baseline (1960–1990) and future climate scenarios for

Australia. Projections indicate that the Wet Tropics is likely to be vulnerable to all 11 species until at least 2070, with the east coast of Australia also likely to remain vulnerable to multiple species. While the Cape York Peninsula and Northern Territory are projected to have suit- able climate for numerous species, extrapolation to novel climates in these areas decreases confidence in model projections. The climate suitability of major horticulture areas currently in eastern Queensland, southern-central New South Wales and southern Victoria to these pests may increase as climate changes. By highlighting areas at risk of pest range expan- sion in the future our study may guide Australia’s horticulture industry in developing effective monitoring and management strategies. Introduction Tephritid fruit flies are one of the most destructive and economically significant pest insect families, attacking a wide range of fruit and vegetables. While the family contains more than 4000 species, around 350 are recognized as economically important horticultural pests [1] that have significant impacts on global horticultural production and market access. In Australia, the average annual value of crops susceptible to fruit flies is ~$4.8 billion [1], and the National Fruit Fly Strategy has identified 46 species as ‘high priority pests’ [2] of concern. The majority of these species are exotic to Australia, primarily found in South-East Asia and the South PLOS ONE | https://doi.org/10.1371/journal.pone.0213820 February 13, 2020 1 / 19 a1111111111 a1111111111 a1111111111 a1111111111

a1111111111 OPEN ACCESS Citation: Sultana S, Baumgartner JB, Dominiak BC, Royer JE, Beaumont LJ (2020) Impacts of climate change on high priority fruit fly species in Australia. PLoS ONE 15(2): e0213820. https://doi.org/ 10.1371/journal.pone.0213820 Editor: Nikos T. Papadopoulos, University of Thessaly School of Agricultural Sciences, GREECE Received: March 1, 2019 Accepted: January 22, 2020 Published: February 13, 2020 Copyright: © 2020 Sultana et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Data Availability Statement: Data availability The findings of our study were supported by publicly available data sourced from the Atlas of Living Australia (ALA; http://www.ala.org.au, 22nd December, 2016) and the Global Biodiversity Information Facility (GBIF, https://www.gbif.org, 28th June, 2017). Additionally, we sourced data from the Australian Plant Pest Database (APPD; http://www.planthealthaustralia.com.au/resources/ australian-plant-pest-database, accessed 15th March 2017) and from Australian State Government department collections (Biosecurity and Food Safety, Department of Primary

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

fruit fly species, based on their performance along climatic gradients. While highly useful in furthering our understanding of climate impacts on fruit flies, these studies have either focused on other countries or have explored global patterns of the distribution of suitable climate [22– 26]. Here we assess how climate change may result in shifts to the distribution of climatically suitable habitat for the 11 high priority fruit fly species present in Australia, using the correla- tive SDM, Maxent [27]. This SDM has been used extensively to assess the distribution of suit- able habitat for a broad range of pests and invasive species [26, 28–31]. We also highlight areas at risk of pest range shifts, to guide Australia’s horticulture industries in developing effective monitoring and management strategies. Methodology Species occurrence data We collected occurrence data for the 11 species from five sources: the Australian Plant Pest Data- base (APPD; http://www.planthealthaustralia.com.au/resources/australian-plant-pest-database, accessed 15th March 2017), the Atlas of Living Australia (ALA; http://www.ala.org.au, 22nd December, 2016), the Global Biodiversity Information Facility (GBIF, https://www.gbif.org, 28th June, 2017, see S1 File for DOIs), trap data, and existing literature. APPD is a national digital Table 1. Eleven economically-significant tephritid pest species present in Australia. Species Common name Geographical Range Major Commercial Hosts [32] References Bactrocera aquilonis (May) Northern Territory fruit fly

Top End of the Northern Territory (NT), northern areas of Western Australia Bell pepper, tomato, lemon, mandarin, grapefruit, apple, mango, peach [1] Bactrocera bryoniae (Tryon) N/A Torres Strait Islands, mainland Queensland, northern Western Australia, NT, NSW as far south as Sydney Chilli, tomato [3] Bactrocera halfordiae (Tryon) Halfordia fruit fly North Queensland to the Sydney region in NSW Citrus [3] Bactrocera jarvisi (Tryon) Jarvis’ fruit fly Northwest Western Australia, NT, northwest Queensland, eastern Australia from Cape York to Sydney, NSW Mango, peach, banana, pear, apple, pawpaw, persimmon [3] Bactrocera kraussi (Hardy) Krauss’ fruit fly Torres Strait Islands, northeast Queensland as far south as Townsville Grapefruit, mandarin, orange, mango, peach and banana [3, 7] Bactrocera musae (Tryon) Banana fruit fly Torres Strait Islands, northeast Queensland as far south as Townsville Banana [3, 7] Bactrocera neohumeralis (Tryon) Lesser Queensland fruit fly Torres Strait Islands, eastern Queensland, northern NSW Mango, pawpaw, persimmon, avocado, banana, passionfruit, apple, apricot, plum, peach, citrus, capsicum, chilli, tomato [3] Bactrocera tryoni (Froggatt) Queensland fruit fly (Qfly) Central and Top End of NT, eastern Australia, Victoria Mango, pawpaw, avocado, grapefruit, passionfruit, strawberry, peach, pear, apple, banana, persimmon, chilli, capsicum, tomato, eggplant [3,31] Zeugodacus cucumis (French) (formerly Bactrocera cucumis) Cucumber fruit fly Eastern Queensland, northeast NSW, NT Cucumber, pumpkin, zucchini, squash,

passionfruit, tomato, pawpaw [3] Bactrocera frauenfeldi (Schiner) Mango fruit fly Native to Papua New Guinea and surrounding islands, spread to Torres Strait Islands and northern Queensland as far south as Townsville Mango, banana, passionfruit, citrus, chilli [7] Ceratitis capitata (Wiedemann) Mediterranean fruit fly (Medfly) Native to Africa, spread to the Mediterranean regions, Western Australia, occasional detections in South Australia and NT are eradicated. Mango, pawpaw, apple, peach, pear, citrus [3, 28, 31] Eleven tephritid pest species present in Australia, including nine natives (B. aquilonis, B. bryoniae, B. halfordiae, B. jarvisi, B. kraussi, B. musae, B. neohumeralis, B. tryoni and Z. cucumis) and two introduced species (B. frauenfeldi and C. capitata), and their major commercial hosts. https://doi.org/10.1371/journal.pone.0213820.t001 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 3 / 19

database of plant pest and pathogen specimens held within herbaria and insect collections across Australia. It is a powerful tool for market access and emergency responses to pest incursion, and supports associated research activities. ALA is Australia’s largest digital database of species occur- rence records, containing information from a wide array of data providers including Australia’s major museums and government departments. GBIF provides similar data at a global scale. Before downloading data from APPD, ALA and GBIF, we applied filters to restrict records to those that were resolved to species-level, were dated no earlier than 1 January 1950, contained valid geo- graphic coordinates, and were not flagged as ‘environmental outliers’. We also collected trap data from various state government departments (Biosecurity and Food Safety, Department of Primary 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)). Trap data from these sources were collected at different periods from 1996 to 2017. Finally, we also obtained occurrence data from the literature [1–4, 6, 7, 11, 33–37]. Major commercial fruit and vegetable hosts For each of the 11 fruit fly species, we compiled information on the major commercial hosts on which infestation has been recorded. For this purpose, we defined major fruit and vegetable

host species according to the Australian Horticulture Statistics Handbook (HSHB; www. horticulture.com.au) for the year 2016/2017 [32]. This document consolidates horticulture sta- tistics of interest to industry members and other stakeholders. The data contained in HSHB were derived from the Australian Bureau of Statistics, projects funded by Hort Innovation, international trade sources and horticulture industry representative bodies where available. Climate data For baseline and future climate conditions we used the bioclimatic variables available within the WorldClim database (v1.4), at a spatial resolution of 30 arc-seconds [38] (approximately 1 km; http://www.worldclim.org). These data, based on meteorological records for the period 1960–1990, comprise 19 climatic variables, 11 of which are temperature-based while eight relate to precipitation. Combined, the data represent annual trends, seasonality, and limiting or extreme environmental conditions. Assuming that host plants are available, temperature and moisture are the key factors influencing fruit fly reproduction and survival [18, 39]. Thus, these variables were chosen as predictor candidates based on the fruit flies’ biology and eco- logical requirements, and similar habitat suitability studies undertaken on other insects [40]. For each species, we identified a set of ecologically-relevant variables, with minimal collinear- ity, that resulted in high predictive power for the model [41] (described below). When projecting future suitability, we considered a range of climate scenarios to acknowl-

edge this important aspect of uncertainty. CSIRO recommends eight global climate models (GCMs) as being useful for Australian climate impact assessments [42]. Data from six of these models were available from the CCAFS GCM Data Portal (http://www.ccafs-climate.org/data_ spatial_downscaling/), at a spatial resolution of 30 arc seconds. These data were developed from anomalies of the original GCM data that were statistically downscaled using a thin plate spline spatial interpolation, and then applied to the WorldClim v1.4 baseline. The GCMs included: CanESM2 (The Second Generation of Canadian Earth System Model); ACCESS1.0 (The Australian Community Climate and Earth System Simulator); MIROC5 (Model for Interdisciplinary Research on Climate); HadGEM2-CC (Hadley Centre Global Environmental Model Version 2 Carbon Cycle); NorESM1-M (The Norwegian Earth System Model-Part-1); 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 4 / 19

and GFDL-ESM2M (Global Coupled Climate Carbon Earth System Model Part-1). CanESM2 projects a hot future with drying across central regions of Australia and higher precipitation in the north-east. ACCESS1.0 projects a hot and dry future across most areas of Australia, while MIROC5 projects moderate warming, with drying in the north-east and south-west but higher precipitation in central Australia. NorESM1-M projects moderate warming. HadGEM2-CC and GFDL-ESM2M project a hot future with greater warming typically in central regions. We downloaded the 19 bioclimatic variables from these six models from CCAF, for 20-year periods centred on 2030, 2050 and 2070, for the Representative Concentration Pathway 8.5 (RCP8.5) [43]. With a radiative forcing exceeding 8.5 Wm-2 by 2100, this is the highest of the four RCPs presented in the Intergovernmental Panel on Climate Change’s Fifth Assessment Report [43]. It is also the RCP that emissions are currently tracking most closely [44]. After downloading, we reprojected data to a spatial resolution of 1 × 1 km (Australian Albers Equal Area, EPSG: 3577) via bilinear interpolation, using the gdalwarp function provided by the R package gdalUtils [45] in R version 3.1.2 [46]. Species distribution models We used the machine learning approach, Maxent (v3.3.3k [27]), to assess climate suitability for species under baseline and future climate scenarios. Maxent accommodates presence-only data and has performed well in multimodel assessments [47]. It produces a continuous proba-

bility surface, which can be interpreted as an index of climatic suitability given the predictor variables included in model calibration. Detailed descriptions of Maxent are given elsewhere [48, 49]. We optimized models by assessing the effects of different combinations of feature types, of competing predictor sets deemed ecologically sensible a priori, and of the extent of regularization on model performance. We found that Maxent performed best when product (first-order interactions), linear and quadratic features were used, with a regularization multi- plier of 1 (the default), and used this configuration to calibrate our final models. Maxent requires background data, to which it compares the environmental characteristics of presence locations. There is flexibility for users to specify which points to use as background, as well as the number of records and the spatial extent from which they are chosen [48]. Fol- lowing Ihlow et al [50], we generated background points by randomly selecting up to 100,000 cells from terrestrial areas within 200 km of occurrence records of the target species. Our choice of background achieves a balance between fine-scale discrimination of suitable and unsuitable sites along environmental gradients, and generalization of model predictions. To assess model performance, we used five-fold cross-validation to reduce model errors that may occur from the random splitting of data into test and training subsets. The perfor- mance of each model was evaluated using the area under the receiver operating characteristic

cells assigned 0 when unsuitable and 1 when suitable) for each time period were summed to produce a consensus map, identifying agreement about the suitability of grid cells across the six climate scenarios. Each species’ consensus map was then converting to a binary map indi- cating whether cells were projected to be suitable under the majority of GCMs (i.e., suitable in < 4 GCMs = 0, suitable in 4 or more = 1). The resulting binary maps were summed across species to identify hotspots—grid cells suitable for multiple pest species. Finally, we compared the distribution of hotspots to that of major horticultural crops. When projecting models, extrapolation to conditions beyond the range of the training data may be unreliable. Following Elith et al. [53] we developed MESS (multivariate environmental similarity surface) maps to identify regions of extrapolation [53]. By revealing areas with novel environmental conditions, MESS maps can be used as a projection mask, highlighting regions for which less confidence can be placed in projections, or as a quantitative measure of predic- tion uncertainty [53]. We then recalculated the size of projected suitable climate with novel environments excluded. All modelling and post-modelling analyses and calculation of statistics were performed in R version 3.1.2 [46]. We used the sp [54] and raster [55] packages for preparation and manipula- tion of spatial data, the dismo [56] package to fit Maxent models, and custom R code for rapid projection of fitted models. Results Model performance

Model performance for all species was better than random, with average cross-validated AUC ranging from 0.815 (SD = 0.05; B. frauenfeldi) to 0.907 (SD = 0.02; B. neohumeralis) (S1 File). Bactrocera aquilonis. Our model suggested that, during the baseline period, climatically suitable habitat for B. aquilonis existed in the northern regions of the Northern Territory and Western Australia, as well as northern Queensland where this fly has not been reported (S1 File). The variables with the highest permutation importance were precipitation of the wettest quarter (68.9%) and annual mean temperature (28.9%) (S1 File). As the century progresses, the geographic extent of climatically suitable habitat for this spe- cies is projected to increase and expand southwards under all six scenarios, with many areas suitable in the baseline period projected to remain so until at least 2070 (S1 File). This includes northern Western Australia, much of the Northern Territory, and north-western Queensland (S1 File). We note, however, that climate scenarios beyond 2030 frequently contain novel con- ditions across the northern regions of Australian, highlighting uncertainty in Maxent projec- tions within these areas (S1 File). Key horticultural crops for B. aquilonis are Mangifera indica (mango), Citrus × paradisi (grapefruit), Malus domestica (apple), Prunus persica (peach) and Citrus sp. (citrus) (S1 File). The major regions where these crops are currently grown include the Northern Territory and north-east Western Australia. These regions may remain suitable for B. aquilonis until at least

2070. Similarly, fruit growing regions in the Wet Tropics (north-east Queensland) are likely to increase in suitability in the future. Other major host-plant growing regions in the south and east of the continent will likely remain unsuitable (S1 File). Bactrocera bryoniae. Suitable habitat for B. bryoniae during the baseline period is pro- jected to have occurred along the northern and eastern coastlines (S1 File). Temperature annual range and precipitation of the driest month contributed the most to the model for this species (42.2% and 27.4%, respectively) (S1 File). By 2070, suitable habitat is projected to increase under all scenarios except GFDL-ESM2M (which projects a hot, very dry future) (S1 File), expanding to the southern coastlines of 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 6 / 19

Victoria and Western Australia. Under 1–3 scenarios, suitable habitat is projected to shift inland in Queensland and NSW. However, the amount of habitat projected to be suitable under all six scenarios remains relatively stable from 2030–2070 (S1 File). Beyond 2030, novel conditions are primarily restricted to the north-western regions (S1 File). The major horticultural host for B. bryoniae is Capsicum annuum (chilli) (S1 File). Our model indicates that key growing regions for this crop in Queensland contained suitable habi- tat for B. bryoniae during the baseline period, and this will continue to be the case until at least 2070 (S1 File). Bactrocera frauenfeldi. Climatically suitable habitat for the baseline period is projected to have been mostly confined to Cape York Peninsula and the Wet Tropics, although small areas in northern Western Australia and the Northern Territory from which the species has not been recorded were also classified as suitable (S1 File). The most important variable in the model for B. frauenfeldi was precipitation of the wettest quarter (75.4%) (S1 File). As the century progresses, suitable habitat is projected to expand under all scenarios except CanESM2 (S1 File). This scenario projects a hot, very dry future, leading to loss of suitable habitat in northern Queensland by 2050. However, the extent of suitable habitat for this species is likely to remain small, relative to other species. In addition, the far north-east of Queensland contains novel conditions, decreasing confidence that this area will be suitable as the century

progresses. As with other species, the Wet Tropics is projected to remain suitable and is not a region in which the model is extrapolating. The major crops for B. frauenfeldi are Mangifera indica (mango) and Carcica papaya (paw- paw) (S1 File). Major production regions in north-western Northern Territory may remain suitable for this species until at least 2070, although there is substantial uncertainty across the climate scenarios. In contrast, it is very likely that the Wet Tropics will remain suitable until at least 2070, irrespective of the climate scenario (S1 File). Bactrocera halfordiae. Baseline climatically suitable habitat for B. halfordiae occurred in the Wet Tropics and subtropics, from north Queensland to eastern New South Wales (S1 File). Precipitation of the driest month (66.8%) and annual mean temperature (32.3%) con- tributed most to this model (S1 File). The geographic extent of suitable habitat is projected to vary considerably across the six cli- mate scenarios. As the century progresses, gains in new habitat may exceed losses under some scenarios (e.g. see ACCESS and MIROC5 in S1 File) while losses are projected under the CanESM2 scenario (which projects a hot future, drying across central regions and higher pre- cipitation in the north-east), mostly due to contractions in the south and east. Across the sce- narios there is consensus that lower elevation regions in the south-east will be suitable. Furthermore, MESS maps indicate little model extrapolation for this species (S1 File).

Crops in the Wet Tropics may continue to be at risk from this species, until at least 2070. However, only 1–2 scenarios project horticultural regions in southern Queensland to retain suitable climate (S1 File). Although horticultural regions along the NSW-Victorian border are projected to have been unsuitable for B. halfordiae in the baseline period, these areas may become suitable between 2050–2070 under some scenarios (S1 File). Bactrocera jarvisi. Suitable habitat for this species is projected to have been mostly con- fined to northern Western Australia, the Top End of the Northern Territory, and eastern Aus- tralia from Cape York to NSW during the baseline period (S1 File). Annual mean temperature (38.0%) and precipitation of driest month (37.2%) had the highest contributions to the model for this species (S1 File). There is substantial consensus across the six scenarios that regions currently suitable for B. jarvisi will remain so until at least 2070 (S1 File). In addition, across some models gains are 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 7 / 19

projected to occur in central Queensland, Western Australia, and the Northern Territory, although model extrapolation occurs under several climate scenarios (S1 File). Comparing the distribution of suitable habitat for this fly with that of its major host crops indicates that crops grown in the Top End of the Northern Territory, and in eastern Australia from Cape York to New South Wales, may continue to be at risk until at least 2070. Other major host-plant growing regions in the south and west of the continent will also remain suit- able for this species until 2070 (S1 File). Bactrocera kraussi. For the baseline period, suitable habitat for B. kraussi is projected to have occurred across the northern tip of Australia and northeast Queensland, as far south as Townsville (S1 File). Precipitation of the wettest quarter (75.19%) had the highest contribution to the model of B. kraussi (S1 File). There is consensus across the six scenarios that the geographic extent of climatically suitable habitat may increase slightly (S1 File), although this is still confined to the Wet Tropics and far north of the continent. In addition, little extrapolation to novel conditions occurs (S1 File). Horticultural production regions in northeast Queensland may remain suitable for this species by 2070, although production regions in the south are likely to remain unsuitable (S1 File). Bactrocera musae. For the baseline period, suitable habitat for B. musae extended from the Torres Strait Islands through to the Wet Tropics (S1 File). The most important variable in

the model for B. musae was precipitation of the wettest quarter (78.7%) (S1 File). Suitable habitat for this species is projected to remain restricted to the Wet Tropics and northern–most regions of the country under the climate scenarios. While there is consensus across the six climate scenarios, less confidence can be placed in projections to the north-west (S1 File). B. musae mainly attacks Musa × paradisiaca (banana), the production areas for which are located primarily in tropical and subtropical regions of the continent (S1 File). The major commercial growing region in the Wet Tropics is projected to remain climatically suitable for this species until at least 2070 (S1 File). Bactrocera neohumeralis. Suitable habitat for this species during the baseline is projected to have been mostly confined to the Torres Strait Islands, eastern Queensland, and north east- ern NSW south to Wollongong (S1 File). Precipitation of the wettest month (47.4%) contrib- uted most to the model for B. neohumeralis (S1 File). As the century progresses, considerable differences in suitable habitat are projected across the six scenarios. For example, under the CanESM2 scenario, ~ one quarter of current suitable habitat is projected to be lost by 2030, although by 2070, range expansions are projected to exceed losses (S1 File). Similarly, under the hot, very dry scenario simulated by GFDL-ESM2M, total range size may decline by 2030, mostly due to contractions in the south and east, although limited gains in habitat may occur in northern Australia (S1 File). There is

consensus in projections of suitability across the north tips of the continent, however MESS maps indicate that Maxent has extrapolated suitability in these regions. In contrast, greater confidence can be placed in projections of consensus along the east coast (S1 File). Production regions in eastern Queensland and north-eastern NSW will likely remain suit- able for this species until at least 2070, although there is substantial uncertainty across the cli- mate scenarios. In contrast, regions along the NSW-Victorian border and further south are projected to remain unsuitable for B. neohumeralis (S1 File). Bactrocera tryoni. Highly suitable habitat for B. tryoni is projected to have occurred in south-western Western Australia, south-eastern South Australia, Victoria, and eastern Austra- lia from Cape York to NSW in the baseline period (S1 File). Coastal zones in northern West- ern Australia, the Northern Territory and the eastern half of Tasmania have moderate 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 8 / 19

suitability (S1 File). Annual mean temperature (33.06%) and mean temperature of the coldest month (32.42%) had the highest contributions to the model for this species (S1 File). The geographic extent of suitable habitat varies across the six climate scenarios. As the cen- tury progresses, gains in new habitat may exceed losses under some scenarios (e.g. see ACCESS1.0, MIROC5 and NorESM1-M; S1 File), while substantial declines occur under oth- ers (e.g. GFDL-ESM2M S1 File), mostly due to contractions in the south and east. Areas of consensus occur along the coastline, although less confidence can be placed in these projec- tions for the Northern Territory and northern Western Australia due to model extrapolation (S1 File). Key regions for host crops in the Top End of Northern Territory, eastern Australia from Cape York to NSW, Victoria, and some parts of Tasmania, may remain suitable for B. tryoni until at least 2070. Major host-plant growing regions in South Australia may also remain suit- able for this species until 2070 (S1 File). Ceratitis capitata. Our model suggests that suitable habitat for C. capitata for the baseline occurred throughout Western Australia, the Northern Territory, the east coast of Queensland to NSW and South Australia (S1 File). We note that scattered records within inland regions of Western Australia are projected as having had low suitability. Annual mean temperature (47.2%) and mean temperature of the coldest month (46.2%) contributed most to the model for this species (S1 File).

Under the future climate scenarios, the geographic extent of suitable habitat is projected to increase and expand inland (S1 File) with much of Victoria and Tasmania likely to be suitable. There is considerable consensus in the distribution of suitable habitat, although consensus declines in New South Wales as the time horizon increases (S1 File). As with other species, MESS maps indicate extrapolation across the northern regions under scenarios from 2050 onwards (S1 File). However, there is high consensus in suitability across the major host plant regions in Queensland, Victoria, and Western Australia. Zeugodacus cucumis. For the baseline period, suitable habitat for Z. cucumis is projected along the northern region of Western Australia and the Northern Territory, north-east Queensland, and south along the east coast to NSW (S1 File). Precipitation of the driest quar- ter (54.3%) and mean temperature of the coldest quarter (36.2%) had the highest permutation importance in the model for this species (S1 File). Under future climate scenarios, the geographic extent of suitable habitat may increase, expanding southward and inland, with most areas that are currently suitable projected to remain so until at least 2070 (S1 File). There is considerable variation among projections for inland regions, likely due to differences in precipitation patterns, indicating higher uncertainty about the future suitability of these regions. There is high consensus in suitability along the east coast, and while consensus is also high in the north MESS maps identify this as a region of

extrapolation. There is little agreement on the suitability of inland regions of New South Wales and Queensland (S1 File). Major commercial growing regions for host crops in Queensland and the Northern Terri- tory are projected to remain climatically suitable for this species until at least 2070 (S1 File). Other major host-plant growing regions in the south and west of the continent will likely remain unsuitable under the time periods considered in this study (S1 File). Future hotspots of pest fruit flies For each time period, we stacked climate suitability maps for all species, to identify regions most likely to contain suitable climate conditions for multiple pest species (i.e. hotspots). As the century progresses, the geographic extent of climatically suitable habitat for most of the 11 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 9 / 19

species is projected to expand and shift south regardless of whether novel environments are included or excluded (Figs 1 and 2 and Table 2). When regions containing novel climate are included, 31.6% of Australia (i.e. ~2,400,800 km2) is projected to have been suitable in the baseline period for at least one of the 11 species, increasing to more than half of the continent by 2070 (Table 2). However, only Queensland’s Wet Tropics is likely to be suitable for all 11 species into the future. When novel environments are excluded from maps, less than 30% of Australia is projected to be suitable for at least one of the species by 2070 (Table 2). Hence, exclusion of novel envi- ronments substantially impacts the size of suitable habitat (i.e., projections of suitable habitat frequently occur in areas with novel climatic conditions). However, extrapolation primarily occurs in northern regions of Western Australia, Northern Territory and the Cape York Pen- insula, decreasing confidence in projections across these regions. From the Wet Tropics and southward, little extrapolation occurs. As such, the Wet Tropics bioregion is projected to remain suitable for 10–11 species, indicating that the major commercial host plants within this bioregion may continue to be at risk of invasion by most or all of these high priority species. Major commercial host plant regions along the coastal strip of south-east Queensland and north-east NSW are likely to have areas that are suitable under all future scenarios for B. bryo-

niae, B. jarvisi, C. capitata and Z. cucumis (S1 File). Under some scenarios, these regions may also be suitable for B. halfordiae, B. neohumeralis and B. tryoni (S1 File). Some major commer- cial host plant regions in southern NSW and Victoria are also projected to be suitable for B. jarvisi, B. tryoni and C. capitata under all scenarios (S1 File) and for B. halfordiae, B. neohu- meralis and Z. cucumis under a limited number of scenarios (S1 File). Horticultural regions in Tasmania are projected as suitable for B. jarvisi, B. tryoni and C. capitata (S1 File). In south-west Western Australia, major horticulture regions are likely to remain suitable for B. jarvisi, B. tryoni and C. capitata, although the latter species is currently not found in this region (S1 File). Commercial horticulture regions in northern region of the Northern Terri- tory are also likely to be suitable for B. jarvisi, B. kraussi, B. musae, B. tryoni and Z. cucumis under all scenarios, and B. frauenfeldi under some climate scenarios. Discussion Our study suggests that the Wet Tropics bioregion has climatically suitable habitat for the larg- est number of high priorities tephritid pest species under both baseline conditions (1960– 1990) and as a result of climate changes projected to occur through to 2070. Cape York Penin- sula and the Northern Territory are also likely to be vulnerable, although novel climates are projected to occur in these regions, and the extrapolation of SDMs to these conditions may be

unreliable. The east coast of Australia is also likely to remain suitable for multiple species until at least 2070. As such, major horticulture regions in north-western Australia, the Northern Territory, southern-central regions of NSW, southern Victoria and north Tasmania may become increasingly suitable to high priority fruit flies. Two species, B. tryoni (Qfly) and C. capitata (Medfly), are projected to have suitable conditions in all states and territories of Aus- tralia, under all considered climate change scenarios, until at least 2070. Over the past 30 years, numerous studies have modelled suitable habitat for Qfly using CLI- MEX and Maxent, at various spatial resolutions [8, 40, 58, 59] and extents. While generally giv- ing similar projections, a key difference is that our model projects Tasmania to have been suitable in the baseline period (1960–1990), whereas fine scale modelling using CLIMEX indi- cates that it is unlikely to become suitable prior the mid-21st century [59]. Our models for both Qfly and Medfly were driven primarily by temperature parameters, rather than precipitation. Previous studies have identified climatic constraints on the 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 10 / 19

distribution of Qfly. For example, it has been reported that Qfly pupae do not survive in the winter months in Melbourne and near Sydney [60], and adults fail to emerge later than mid- April [61]. Further, many subtropical sites in Queensland are marginal in winter for Qfly breeding and general activity [8, 61]. As such, slight temperature increases associated with cli- mate change are projected to substantially elevate the threat that this species poses to horticul- tural industries [62]. For instance, using data from the late 1990s, it was estimated that annual control costs for apple growers around Adelaide may increase by between $346,000 and $1.3 million with a 0.5–2˚C increase in temperature [62]. With the exception of Western Australia, all Australian states and territories are currently free from Medfly, with market access protocols inhibiting movement into other states [21], and incursions met with immediate eradication programs [13]. Our model of baseline habitat indicates suitable conditions for Medfly around most of Australia’s coastal regions. In addition to identifying suitability in the subtropical coastal fringe of Queensland, our model suggested that much of the low-altitude regions in the south-east, including parts of Tasmania, are also Fig 1. Hotspot maps of habitat suitability for the 11 fruit fly species under climate change, when novel environments are included. Hotspot maps of baseline (1960–1990) and future habitat suitability for 11 fruit flies. Suitability was modelled with Maxent, and

thresholded using the 10th percentile of suitability at training presence localities. These maps include projections under novel environments (see S1 File for individual species maps with novel environments included). Colours indicate the number of species for which habitat is projected to be suitable under the majority (� 4) future climate scenarios. Figure was created in R version 3.3.3 [57] (https://www.R-project.org/). https://doi.org/10.1371/journal.pone.0213820.g001 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 11 / 19

suitable. While our result for Medfly is similar to that obtained from CLIMEX and Principle Components Analysis [25, 58], the model GARP projected a far broader potential distribution in Australia for this species [58], while Szyniszewska and Tatem’s [63] Maxent model sug- gested more of Queensland may be suitable, compared to our analysis. Competition with Qfly may be responsible for exclusion of Medfly from much of Queensland [25], and similar biotic interactions may suppress the species elsewhere [13]. However, Medfly may be more tolerant to low temperatures and dry summers than Qfly [4], rendering Medfly the stronger competitor in areas with these conditions. Medfly was recorded in Tasmania in the 1920s but reportedly failed to survive an unseasonably hot and dry summer [4]. Due to their age, these records were not used to calibrate our model, yet our projections indicate that Tasmania continues to have conditions suitable for this species. Allwood and Angeles [64] reported that B. jarvisi is recognized as a pest in north-western Australia, infesting mango, guava and pomegranates (as reported in [65]). Dominiak and Fig 2. Hotspot maps of habitat suitability for the 11 fruit fly species under climate change, when novel environments are excluded. Hotspot maps of baseline (1960–1990) and future habitat suitability for 11 fruit flies. Suitability was modelled with Maxent, and thresholded using the 10th percentile at training presence localities. These maps exclude regions containing novel environments (see S1

File for individual species maps with novel environments excluded). Colours indicate the number of species for which habitat is projected to be suitable under the majority (� 4) future climate scenarios. Figure was created in R version 3.3.3 [57] (https://www.R- project.org/). https://doi.org/10.1371/journal.pone.0213820.g002 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 12 / 19

Worsley [9] concluded that the current south-eastern range limit lies north of the Queensland- NSW border (~25.5˚ south), while the south-western limit lies at approximately 18˚ south. However, previous analysis suggested that this species’ current climatic range could extend into the cooler temperate areas of southern NSW, and eastern and northern Victoria [4]. Our models partly agree, indicating that suitable conditions along the east coast of Victoria in the baseline period. This species can also withstand very warm conditions, with eggs known to be more heat tolerant than those of the sympatric Qfly, surviving temperatures of 48.2˚C [65]. Given that these species infest many of the same hosts, competition is likely, hence eradication of Qfly may result in the competitive release of B. jarvisi, increasing the threat it poses to horti- culture [4, 65]. Further, as the cultivation of B. jarvisi host plants expands geographically, this species may increase in abundance and extend its range, potentially becoming a major pest in north-western Australia [6, 36]. However, across north-western Australia, and to a lesser extent the far north-east, models for most species were projected onto novel conditions, decreasing confidence in suitability estimates for these regions. In contrast, MESS maps dem- onstrated that extrapolation rarely occurred across eastern and southern regions, although novel interactions between climate variables cannot be ruled out. While widespread throughout Queensland, Z. cucumis currently has a restricted distribu-

tion in the Northern Territory, although there is a disputed single record from northern West- ern Australia [66]. Both Fitt [67] and the Horticultural Policy Council [4] reported that if the cucurbit industry expands in the Northern Territory, the pest status of Z. cucumis may increase. However, while the species has been trapped frequently in the Northern Territory, it has not been found on cucurbits growing in this region [6]. In NSW, Z. cucumis appears to be currently limited to regions close to the Queensland border, with rare detection as far south as Sydney [66]. It has not been detected in the (former) Fruit Fly Exclusion Zone in southern NSW [37]. Our model also estimates the southern limit of suitable climate for this species to be around Sydney. However, with climate change this may extend further southward, with parts Table 2. Percentage (%) of Australia projected to be suitable for the 11 fruit fly species considered in this study, under baseline (1960–1990) and future climates. Suitable area (% of Australia) Count Baseline (Novel masked) 2030 2050 2070 0 68.4% (68.5%) 67.5% (70.2%) 59.5% (73.6%) 47.0% (72.0%) 1 11.0% (11.1%) 9.6% (9.4%) 11.6% (9.6%) 14.6% (10.0%) 2 11.1% (11.0%) 10.5% (9.7%) 14.8% (8.8%) 17.5% (10.3%) 3 2.3% (2.3%) 3.4% (4.1%) 3.0% (3.0%) 6.5% (3.4%) 4 1.2% (1.2%) 1.9% (2.2%) 3.2% (1.6%) 4.8% (1.2%) 5 1.6% (1.8%) 2.6% (2.8%) 2.9% (1.9%) 3.9% (1.6%) 6 1.2% (1.5%) 1.9% (0.8%) 1.8% (0.6%) 2.3% (0.7%) 7 1.3% (1.3%) 0.6% (0.4%) 1.0% (0.5%) 1.2% (0.5%) 8 0.4% (0.7%) 0.4% (0.2%) 0.5% (0.2%) 0.6% (0.1%)

9 0.8% (0.3%) 1.3% (0.2%) 1.4% (0.1%) 1.4% (0.1%) 10 0.6% (0.4%) 0.3% (0.1%) 0.1% (0.1%) 0.1% (0.1%) 11 0.0% (1.3E-05%) 0.1% (0.0%) 0.1% (0.0%) 0.1% (0.0%) This is a summary of the ‘consensus’ maps for each species. Values in brackets represent results when novel environments have been excluded. Each row of the table indicates the percentage of Australia projected to be suitable in the baseline period (1960–1990), in 2030, 2050, and 2070, for n species, where n is given in the “Count” column. Thus, the first row (with Count = 0) gives the area projected to be unsuitable for all 11 species under four or more of the climate scenarios, the row with Count = 1 gives the area projected to be suitable for any one of the 11 species in at least four of the climate scenarios, and the row with Count = 11 gives the area projected to be suitable for all 11 species in at least four of the climate scenarios. Note that the number of 1 km2 grid cells spanning Australia is 7,667,790. https://doi.org/10.1371/journal.pone.0213820.t002 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 13 / 19

of Victoria projected to become increasingly suitable over time, depending on the climate change scenario. Bactrocera neohumeralis presently occurs from the western Cape York Peninsula, Queens- land, south to Sydney, NSW [3, 7, 37]. Our model suggests that as climate changes, the range of this species may extend southward and, under some scenarios, into parts of Victoria. Previ- ous climatic analysis also suggested that this species is well adapted to conditions on the east coast of Queensland, with large populations occurring in areas north of Townsville [4]. Similar ecological characteristics are shared by B. neohumeralis and Qfly [68], yet while Qfly is preva- lent in sub-tropical and temperate areas of Queensland and NSW, B. neohumeralis is more prevalent in northern wet tropical areas [4, 5, 69]. The reason for this difference between the geographical ranges of these species is unclear, as both are polyphagous and use similar host fruits for their larval development [68, 69]. Our model for B. aquilonis indicates suitable conditions for this species in northern Queensland under baseline conditions, although it is presently only known from north-west- ern Australia [5]. The hosts of this species now include 40 commercial crops [6]. Expansion of the range of this species, or the growth of host plant industries in north-western Australia may necessitate the development of new monitoring, control and disinfestation procedures [65]. In addition, it has been argued that if B. aquilonis hybridises with Qfly, the resulting strain may

have greater potential for spread than B. aquilonis [4]. This, in turn, would require that disin- festation procedures be developed for the hybrids [65]. The distribution of B. bryoniae ranges from the Torres Strait Islands, across northern Aus- tralia, and along the east coast to north of Sydney, NSW. Our results indicate that suitable cli- mate may exist in Victoria, south of the species’ known range. However, previous studies have demonstrated that populations in northern NSW experience a marked decline in abundance through November–January [37]. This may be explained by a decline in the fruiting and flow- ering of native host trees, or seasonal climatic constraints that are not reflected in our model [37], which may also explain their absence in Victoria. Northern Queensland has the highest diversity of fruit flies in Australia, and some species with significant economic impacts are found only in this region [7]. The distribution of B. kraussi, B. musae and B. frauenfeldi is limited to north Queensland [3, 70], with recent trap data suggesting that these species do not occur south of Townsville [7]. Royer et al. [35] pre- dicted that B. frauenfeldi has suitable habitat in the Northern Territory and northern Western Australia, which is also suggested by our model. This species has expanded its range in north- ern Queensland due to continued planting of hosts, such as mango and guava [35]. Further increases within these horticulture industries in northern Queensland may increase the pest status of this fly [70]. Model errors and uncertainties