Abstract:

The objective of this work was to outline the potential distribution and economic impact of Drosophila suzukii (Diptera: Drosophilidae), a recent invasive pest, in Brazil. Two maps of the potential establishment of the species were drawn based on the ecoclimatic index (EI), which uses the following thermal requirements for the species: with thermal stress, most restrictive scenario for spread; and without thermal stress. The EI was classified into four ranges: unfavorable, ≤25%; less favorable, >25 to ≤50%; favorable, >50 to ≤75%; and highly favorable, >75%. Economic losses were estimated based on the most restrictive map. The highly favorable areas were overlapped with those of the maps of production data for each possible host (apple, grape, peach, persimmon, fig, and pear). Considering these six hosts, the overlap between the highly favorable and the production areas varied from 45.5% (grape) to 98.3% (apple). However, the monetary estimation of the potential losses in the worst case scenario (no control measures) was possible only for figs and peaches. Southern Brazil is the most climatically favorable area for D. suzukii development and where potential economic losses are expected to be the greatest. Maximum average temperatures (>30°C) are the main ecological factor to limit D. suzukii spread in Brazil.

Index terms:
adaptation, biogeography; bioinvasion; exotic species; spotted wing drosophila.

Resumo:

O objetivo deste trabalho foi delinear a distribuição e o impacto econômico potenciais de Drosophila suzukii (Diptera: Drosophilidae), recente praga invasora, no Brasil. Foram feitos dois mapas de potencial de estabelecimento da espécie baseados no índice ecoclimático (EI), que utiliza as seguintes exigências termicas da espécie: com estresse de temperatura, cenário mais restrito para a expansão; e sem estresse de temperatura. O EI foi classificado em quatro faixas: não favorável, ≤25%; pouco favorável, >25 a ≤50%; favorável, >50 a ≤75%; e altamente favorável, >75%. As perdas econômicas foram estimadas a partir do mapa com a distribuição mais restritiva. As áreas consideradas altamente favoráveis foram sobrepostas às dos mapas de produção de cada hospedeiro possível (maçã, uva, pêssego, caqui, figo e pera). Ao se considerar esses seis hospedeiros, a sobreposição das áreas altamente favorável e de produção variou de 45,5% (uva) a 98,3% (maçã). No entanto, a estimativa monetária de perdas potenciais no pior cenário possível (sem medidas de controle) foi possível apenas para figo e pêssego. O Sul do Brasil é a área climaticamente mais favorável para o desenvolvimento de D. suzukii e onde as perdas econômicas potenciais podem ser máximas. As temperaturas médias máximas (>30°C) são o principal fator para restringir a dispersão de D. suzukii no Brasil.

Termos para indexação:
adaptação; biogeografia; bioinvasão; espécies exóticas; drosófila-da-asa-manchada.

Introduction

The dipterans of the Drosophilidae family encompass more than 4,000 species (Yassin, 2013YASSIN, A. Phylogenetic classification of the Drosophilidae Rondani (Diptera): the role of morphology in the postgenomic era. Systematic Entomology, v.38, p.349-364, 2013. DOI: 10.1111/j.1365-3113.2012.00665.x.
https://doi.org/10.1111/j.1365-3113.2012... ). These flies breed on rotten fruit and other organic matter; however, the majority of them are not of economic importance. Only Zaprionus indianus (Gupta, 1970), the African fig fly, and Drosophila suzukii (Matsumura, 1931) (Diptera: Drosophilidae), are considered pests of economic relevance, because they are able to attack fruit suitable for human consumption prior to harvest (Van Timmeren & Isaacs, 2014VAN TIMMEREN, S.; ISAACS, R. Drosophila suzukii in Michigan vineyards, and the first report of Zaprionus indianus from this region. Journal of Applied Entomology, v.138, p.529-537, 2014. DOI: 10.1111/jen.12113.
https://doi.org/10.1111/jen.12113.... ).

Drosophila suzukii became invasive in the second half of the 20^th century. It was first described in 1931 by Matsumura in Japan (Hauser, 2011HAUSER, M. A historic account of the invasion of Drosophila suzukii (Matsumura) (Diptera: Drosophilidae) in the continental United States, with remarks on their identification. Pest Management Science, v.67, p.1352-1357, 2011. DOI: 10.1002/ps.2265.
https://doi.org/10.1002/ps.2265.... ). In the United States, it was collected in Hawaii in 1980, then in California in 2008 (Hauser, 2011HAUSER, M. A historic account of the invasion of Drosophila suzukii (Matsumura) (Diptera: Drosophilidae) in the continental United States, with remarks on their identification. Pest Management Science, v.67, p.1352-1357, 2011. DOI: 10.1002/ps.2265.
https://doi.org/10.1002/ps.2265.... ), spreading across the western and eastern coasts of the country and of Canada. The species was also discovered in Spain in 2008, and in France in 2009, then spread to Central Europe and other countries on the Mediterranean coast, such as Slovenia and Croatia (Cini et al., 2014CINI, A.; ANFORA, G.; ESCUDERO-COLOMAR, L.A.; GRASSI, A.; SANTOSUOSSO, U.; SELJAK, G.; PAPINI, A. Tracking the invasion of the alien fruit pest Drosophila suzukii in Europe. Journal of Pest Science, v.87, p.559-566, 2014. DOI: 10.1007/s10340-014-0617-z.
https://doi.org/10.1007/s10340-014-0617-... ).

In Brazil, D. suzukii was reported for the first time in the subtropical forests of the southern region (Deprá et al., 2014DEPRÁ, M.; POPPE, J.L.; SCHMITZ, H.J.; DE TONI, D.C.; VALENTE, V.L.S. The first records of the invasive pest Drosophila suzukii in the South American continent. Journal of Pest Science, v.87, p.379-383, 2014. DOI: 10.1007/s10340-014-0591-5.
https://doi.org/10.1007/s10340-014-0591-... ), where it damaged strawberries in the municipality of Vacaria, in the state of Rio Grande do Sul (Santos, 2014SANTOS, R.S.S. dos. Ocorrência de Drosophila suzukii (Matsumura, 1931) (Diptera: Drosophilidae) atacando frutos de morango no Brasil. Bento Gonçalves: Embrapa Uva e Vinho, 2014. 4p. (Embrapa Uva e Vinho. Comunicado técnico, 159).). In the state of São Paulo, in the southeastern region, D. suzukii was found in fruits traded in a fruits and vegetable wholesale center (Vilela & Mori, 2014VILELA, C.R.; MORI, L. The invasive spotted-wing Drosophila (Diptera, Drosophilidae) has been found in the city of São Paulo (Brazil). Revista Brasileira de Entomologia, v.58, p.371-375, 2014. DOI: 10.1590/S0085-56262014000400004.
https://doi.org/10.1590/S0085-5626201400... ). In addition, specimens of D. suzukii were collected in the Brazilian Cerrado (savannah-like vegetation), in Brasília, DF (Paula et al., 2014PAULA, M.A.; LOPES, P.H.S.; TIDON, R. First record of Drosophila suzukii in the Brazilian Savanna. Drosophila Information Service, v.97, p.113-115, 2014.). This finding confirms that D. suzukii is able to spread until 1,400 km per year (Calabria et al., 2012CALABRIA, G.; MÁCA, J.; BÄLICH, G.; SERRA, L.; PASCUAL, M. First records of the potential pest species Drosophila suzukii (Diptera: Drosophilidae) in Europe. Journal of Applied Entomology, v.136, p.139-147, 2012. DOI: 10.1111/j.1439-0418.2010.01583.x.
https://doi.org/10.1111/j.1439-0418.2010... ).

Mathematical models for species distribution have been used to estimate the probability of an invasive species establishing itself in areas where it has not yet been found. Climex is one of the most used models to predict the potential geographic distribution of invasive species, such as Helicoverpa armigera (Lepidoptera: Noctuidae) in the United States (Kriticos et al., 2015KRITICOS, D.J.; OTA, N.; HUTCHISON, W.D.; BEDDOW, J.; WALSH, T.; TAY, W.T.; BORCHERT, D.M.; PAULA-MORAES, S.V.; CZEPAK, C.; ZALUCKI, M.P. The potential distribution of invading Helicoverpa armigera in North America: is it just a matter of time? PLoS One, v.10, p.1-24, 2015. DOI: 10.1371/journal.pone.0119618.
https://doi.org/10.1371/journal.pone.011... ) and Ceutorhynchus obstrictus (Coleoptera: Curculionidae), Meligethes viridescens (Coleoptera: Nitidulidae), and Oulema melanopus (Coleoptera: Chrysomelidae) in Canada (Olfert & Weiss, 2006OLFERT, O.; WEISS, R.M. Impact of climate change on potential distributions and relative abundances of Oulema melanopus, Meligethes viridescens and Ceutorhynchus obstrictus in Canada. Agriculture, Ecosystems and Environment, v.113, p.295-301, 2006. DOI: 10.1016/j.agee.2005.10.017.
https://doi.org/10.1016/j.agee.2005.10.0... ).

The potential spread of D. suzukii in Brazil is very significant, because more than 80% of the production areas of most of its hosts are located in climatically highly favorable areas. Restricting fruit trade in the internal market is a measure adopted to avoid the spread of this pest; however, it is not very effective due to the species' high natural spreading capability. This restriction could be more effective in unfavorable areas, such as important grape-production areas in the Northeast region of the country. It should be noted that economic evaluations are still necessary for any quarantine restriction.

The economic impact of D. suzukii has been described in the United States (Bolda et al., 2010BOLDA, M.P.; GOODHUE, R.E.; ZALOM, F.G. Spotted wing drosophila: potential economic impact of newly established pest. Giannini Foundation of Agricultural Economics, v.13, p.5-8, 2010.; Goodhue et al., 2011GOODHUE, R.E.; BOLDA, M.; FARNSWORTH, D.; WILLIAMS, J.C.; ZALOM, F.G. Spotted wing drosophila infestation of California strawberries and raspberries: economic analysis of potential revenue losses and control costs. Pest Management Science, v.67, p.1396-1402, 2011. DOI: 10.1002/ps.2259.
https://doi.org/10.1002/ps.2259.... ) and in Italy (De Ros et al., 2013DE ROS, G.; ANFORA, G.; GRASSI, A.; IORIATTI, C. The potential economic impact of Drosophila suzukii on small fruits production in Trentino (Italy). Integrated Protection of Fruit Crops, v.91, p.317-321, 2013.). The damaged fruits are considered unmarketable, and chemical control can result in the rejection of fruits for export and consumption due to insecticide residues (Haviland & Beers, 2012HAVILAND, D.R.; BEERS, E.H. Chemical control programs for Drosophila suzukii that comply with international limitations on pesticide residues for exported sweet cherries. Journal of Integrated Pest Management, v.3, p.F1-F6, 2012. DOI: 10.1603/IPM11034.
https://doi.org/10.1603/IPM11034.... ). However, there is a lack of estimates of the economic losses caused by this pest around the world, which limits the analysis of costs and benefits for phytosanitary measures (Kehlenbeck et al., 2012KEHLENBECK, H.; ROBINET, C.; WERF, W. VAN DER; KRITICOS, D.; REYNAUD, P.; BAKER, R. Modelling and mapping spread in pest risk analysis: a generic approach. EPPO Bulletin, v.42, p.74-80, 2012. DOI: 10.1111/j.1365-2338.2012.02550.x.
https://doi.org/10.1111/j.1365-2338.2012... ).

The objective of this work was to outline the potential distribution and economic impact of D. suzukii, a recent invasive pest, in Brazil.

Materials and Methods

The simulated map of D. suzukii establishment was drawn using the Climex model (Hearne Software, Melbourne, Australia), which is based on information of the ecoclimate index (EI) on temperature thresholds for the development of a species. The index was determined by EI = GI × SI, in which GI is the growth index and SI is the stress index (Sutherst, 1991SUTHERST, R.W. Predicting the survival of immigrant insect pests in new environments. Crop Protection, v.10, p.331-333, 1991. DOI: 10.1016/S0261-2194(06)80020-7.
https://doi.org/10.1016/S0261-2194(06)80... ; Sutherst et al., 1999SUTHERST, R.W.; MAYWALD, G.F.; YONOW, T.; STEVENS, P.M. Climex: predicting the effects of climate on plants and animals: user guide. Collingwood: Commonwealth Scientific and Industrial Research Organisation, 1999. 88p.). Considering insects are poikilothermic and their development is mainly determined by temperature variation, it was assumed that GI = TI, in which TI is the temperature index, defined by the temperature limits (DV parameters) of the Climex model. For D. suzukii, the DV parameters considered were: limiting low temperature (DV0) of 7.2ºC; lower optimal temperature (DV1) of 13.4ºC; upper optimal temperature (DV2) of 28.1ºC; and limiting high temperature (DV3) of 30ºC. All temperature limits were based on data from Tochen et al. (2014)TOCHEN, S.; DALTON, D.T.; WIMAN, N.; HAMM, C; SHEARER, P.W.; WALTON, V.M. Temperature-related development and population parameters for Drosophila suzukii (Diptera: Drosophilidae) on cherry and blueberry. Environmental Entomology, v.43, p.501-510, 2014. DOI: 10.1603/EN13200.
https://doi.org/10.1603/EN13200.... . The number of degree-days for complete development is 208 (Table 1), i.e., the thermal constant k in positive degree-days (PDD) (Tochen et al., 2014TOCHEN, S.; DALTON, D.T.; WIMAN, N.; HAMM, C; SHEARER, P.W.; WALTON, V.M. Temperature-related development and population parameters for Drosophila suzukii (Diptera: Drosophilidae) on cherry and blueberry. Environmental Entomology, v.43, p.501-510, 2014. DOI: 10.1603/EN13200.
https://doi.org/10.1603/EN13200.... ).

In the model, when the average temperature is between DV1 and DV2, the value of the base temperature is subtracted from the average temperature in order to obtain degree-days. When the accumulated degree-days are positive (PDD), the model considers that one development cycle was completed. Calculations of the number of generations per year were performed based on the thermal constant k (PDD).

Two environmental stress factors were considered for the SI: cold stress (THCS) and heat stress (THHS). For THCS, a temperature below 5°C is the limit for adult activity (Kanzawa, 1936KANZAWA, T. Studies on Drosophila suzukii Mats. Journal of Plant Protection, Tokyo, v.23, p.66-70, 1936.); however, adults can survive in the winter with negative temperatures. For THHS, 30°C is the limit for larval eclosion and development (Kinjo et al., 2014KINJO, H.; KUNIMI, Y.; NAKAI, M. Effects of temperature on the reproduction and development of Drosophila suzukii (Diptera: Drosophilidae). Applied Entomology and Zoology, v.49, p.297-304, 2014. DOI: 10.1007/s13355-014-0249-z.
https://doi.org/10.1007/s13355-014-0249-... ). These two stress parameters were adjusted according to the Mediterranean template of Climex (Sutherst et al., 1999SUTHERST, R.W.; MAYWALD, G.F.; YONOW, T.; STEVENS, P.M. Climex: predicting the effects of climate on plants and animals: user guide. Collingwood: Commonwealth Scientific and Industrial Research Organisation, 1999. 88p.). When the minimum temperature is lower than the THCS value or the maximum temperature is higher than the THHS, the rhythm of organism development is decelerated at a rate provided by the model.

The Climex model uses a matrix of 61,076 terrestrial points, with distances of 0.5 degree among them. For each one of them there is data on minimum, average, and maximum temperatures, based on normal climatological variables between 1961 and 1990 (New et al., 2002NEW, M.; LISTER, D.; HULME, M.; MAKIN, I. A high-resolution data set of surface climate over global land areas. Climate Research, v.21, p.1-25, 2002. DOI: 10.3354/cr021001.
https://doi.org/10.3354/cr021001.... ). The EI was calculated combining TI and SI, and the maps were generated by the Dymex simulator software, using the "Compare Locations" function for one species of Climex, version 3.00.009 (Hearne Software, Melbourne, Australia).

For the species establishment maps, two scenarios were considered for Brazil: one with heat and cold stress, and the other without heat and cold stress. The EI was classified into four classes of favorability: unfavorable, ≤25%, less than 3 months climatically favorable per year; less favorable, >25 to ≤50%, between 3 to 6 months climatically favorable per year; favorable, >50 to ≤75%, between 6 to 9 months climatically favorable per year; and highly favorable, >75%, more than 9 months climatically favorable per year.

Six D. suzukii hosts were evaluated: apple (Malus domestica Borkh.), fig (Ficus carica L.), grape (Vitis vinifera L.), peach [Prunus persica (L.) Batsch], pear (Pyrus communis L.), and persimmon (Diospyros kaki Thunb.).

Another map was drawn, showing the distribution of the production per municipality of the following D. suzukii hosts: apple, grape, peach, and persimmon. The data about these hosts were obtained from the statistics on production per municipality, "Produção Agrícola Municipal" (Instituto Brasileiro de Geografia e Estatística, 2013INSTITUTO BRASILEIRO DE GEOGRAFIA E ESTATÍSTICA. Produção agrícola municipal. 2013. Disponível em: <Disponível em: http://downloads.ibge.gov.br/downloads_estatisticas.htm >. Acesso em: 8 jul. 2014.
http://downloads.ibge.gov.br/downloads_e... ), and all the information was classified according to the fruit species and to production value. The two simulated maps - of D. suzukii potential distribution and of host production - were overlapped in order to observe regions with high phytosanitary risk (EI for D. suzukii >75%).

A partial budgeting method was used to estimate the potential economic impact of D. suzukii, employing a scenario without control measures (Soliman et al., 2010SOLIMAN, T.; MOURITS, M.C.M.; OUDE LANSINK, A.G.J.M.; WERF, W. van der. Economic impact assessment in pest risk analysis. Crop Protection, v.29, p.517-524, 2010. DOI: 10.1016/j.cropro.2009.12.014.
https://doi.org/10.1016/j.cropro.2009.12... ). The potential economic losses in monetary terms (values in US$) were obtained through the equation: L_($) = PV_(hfa) × L_(r), in which L_($) is the potential economic losses in monetary terms; PV(_hfa) is the crop production value of the highly favorable area (EI >75%); and L_(r) is the maximum production loss reported without control measures (%).

Results and Discussion

The Climex parameters resulted in simulated distribution maps that are very similar to the real distribution of D. suzukii around the world, especially in North America, Europe, and Japan (Figure 1). In the United States, both the east and west coasts are suitable for the establishment of D. suzukii. This is similar to the information that was reported by Walsh et al. (2011)WALSH, D.B.; BOLDA, M.P.; GOODHUE, R.E.; DREVES, A.J.; LEE, J.; BRUCK, D.J.; WALTON, V.M.; O'NEAL, S.D.; SALOM, F.G. Drosophila suzukii (Diptera: Drosophilidae): invasive pest of ripening soft fruit expanding its geographic range and damage potential. Journal of Integrated Pest Management, v.106, p.289-295, 2011. DOI: 10.1603/ipm10010.
https://doi.org/10.1603/ipm10010.... . The obtained world map is also in alignment with current D. suzukii distribution across Europe (Cini et al., 2012CINI, A.; IORIATTI, C.; ANFORA, G. A review of the invasion of Drosophila suzukii in Europe and a draft research agenda for integrated pest management. Bulletin of Insectology, v.65, p.149-160, 2012.) and Japan (Mitsui et al., 2010MITSUI, H.; BEPPU, K.; KIMURA, M.T. Seasonal life cycles and resource uses of flower- and fruit-feeding drosophilid flies (Diptera: Drosophilidae) in central Japan. Entomological Science, v.13, p.60-67, 2010. DOI: 10.1111/j.1479-8298.2010.00372.x.
https://doi.org/10.1111/j.1479-8298.2010... ).

Figure 1:
Potential distribution of Drosophila suzukii around the world. Areas in circles are regions where D. suzukii occurred before it was registered in Brazil. USA, according to Walsh et al. (2011)WALSH, D.B.; BOLDA, M.P.; GOODHUE, R.E.; DREVES, A.J.; LEE, J.; BRUCK, D.J.; WALTON, V.M.; O'NEAL, S.D.; SALOM, F.G. Drosophila suzukii (Diptera: Drosophilidae): invasive pest of ripening soft fruit expanding its geographic range and damage potential. Journal of Integrated Pest Management, v.106, p.289-295, 2011. DOI: 10.1603/ipm10010.
https://doi.org/10.1603/ipm10010.... ; Europe, Cini et al. (2012)CINI, A.; IORIATTI, C.; ANFORA, G. A review of the invasion of Drosophila suzukii in Europe and a draft research agenda for integrated pest management. Bulletin of Insectology, v.65, p.149-160, 2012.; and Japan, Mitsui et al. (2010)MITSUI, H.; BEPPU, K.; KIMURA, M.T. Seasonal life cycles and resource uses of flower- and fruit-feeding drosophilid flies (Diptera: Drosophilidae) in central Japan. Entomological Science, v.13, p.60-67, 2010. DOI: 10.1111/j.1479-8298.2010.00372.x.
https://doi.org/10.1111/j.1479-8298.2010... .

Most of Brazil is not favorable for the establishment of D. suzukii (EI <25%) (Figure 1 and Table 2). However, states in the southern region are located in climatic areas that are considered favorable to highly favorable for D. suzukii establishment. The southeastern region, including the states of São Paulo and Minas Gerais, has more than 50% of its area classified as favorable or highly favorable. The average temperature of these areas is about 25°C, which is favorable for the establishment of invasive species (Shi et al., 2010SHI, J.; LUO, Y.-Q.; ZHOU, F.; HE, P. The relationship between invasive alien species and main climatic zones. Biodiversity and Conservation, v.19, p.2485-2500, 2010. DOI: 10.1007/s10531-010-9855-4.
https://doi.org/10.1007/s10531-010-9855-... ).

The two simulated maps, with temperature stress and without temperature stress, of predicted favorability in Brazil show some similarities and differences. In the scenario without stress, the spread of D. suzukii throughout Brazil would not be more extensive than that of the stress-restrictive scenario (Figures 2 and 3). The main difference between the scenarios is that the areas with intermediate favorability (EI >25% to <75%) are predicted to be more extensive than those in the restrictive scenario. Therefore, the potential distribution of D. suzukii can occur somewhere between the two simulated scenarios.

Figure 2:
Map of predicted climatic favorability for Drosophila suzukii establishment in Brazil in a scenario without temperature stress. Probability ranges are temperature intervals of the ecoclimatic index from Climex (Hearne Software, Melbourne, Australia). The darkest areas are highly favorable for D. suzukii establishment.

Figure 3:
Map of predicted climatic favorability for Drosophila suzukii establishment in Brazil in a scenario with temperature stress. Probability ranges are the temperature intervals of the ecoclimatic index from Climex (Hearne Software, Melbourne, Australia). The darkest areas are highly favorable for D. suzukii establishment.

The distribution limits of D. suzukii will be governed by the occurrence of average maximum temperatures above 30°C. However, despite this temperature limit, the adaptation of D. suzukii to new environments and ecological niches might occur, although this process is not fast (Broennimann et al., 2007BROENNIMANN, O.; TREIER, U.A.; MÜLLER-SCHÄRER, H.; THUILLER, W.; PETERSON, A.T.; GUISAN, A. Evidence of climatic niche shift during biological invasion. Ecology Letters, v.10, p.701-709, 2007. DOI: 10.1111/j.1461-0248.2007.01060.x.
https://doi.org/10.1111/j.1461-0248.2007... ). Overall, the states of Rio Grande do Sul, Santa Catarina, Paraná, São Paulo, and Minas Gerais are located in regions that show a high probability of economic losses due to D. suzukii. These states are the main producers of grapes, apples, peaches, and persimmons (Figure 4). Other D. suzukii hosts, such as strawberry (Fragaria vesca L.), raspberry (Rubus idaeus L.), and mulberry (Morus sp.), were not considered in the economic impact study because there is no data available concerning production per municipality (Instituto Brasileiro de Geografia e Estatística, 2013INSTITUTO BRASILEIRO DE GEOGRAFIA E ESTATÍSTICA. Produção agrícola municipal. 2013. Disponível em: <Disponível em: http://downloads.ibge.gov.br/downloads_estatisticas.htm >. Acesso em: 8 jul. 2014.
http://downloads.ibge.gov.br/downloads_e... ). However, these hosts are still important. In 2013, for example, 9,708 Mg of strawberry were marketed by the fruits and vegetable wholesale center "Companhia de Entrepostos e Armazéns Gerais de São Paulo" (Ceagesp) at the price of R$ 10.00 per kilogram (Agrianual..., 2015AGRIANUAL 2015: anuário da agricultura brasileira. 20.ed. São Paulo: FNP, 2015. 472p.), indicating losses of 30% in production (Santos, 2014SANTOS, R.S.S. dos. Ocorrência de Drosophila suzukii (Matsumura, 1931) (Diptera: Drosophilidae) atacando frutos de morango no Brasil. Bento Gonçalves: Embrapa Uva e Vinho, 2014. 4p. (Embrapa Uva e Vinho. Comunicado técnico, 159).), which would mean R$ 29 million or US$ 11.5 million. The potential economic losses of peaches and figs were 20 and 30% according to data from Lies (2009)LIES, M. New fruit pest triggers concerns. Capital Press Agricultural News, 26 Sept. 2009. Available at: <Available at: http://www.capitalpress.com/content/ml-vinegar-fly-092509-art# >. Accessed on: 25 Mar. 2014.
http://www.capitalpress.com/content/ml-v... and from Berry (2012)BERRY, J.A. Pest risk assessment: Drosophila suzukii: spotted wing drosophila (Diptera: Drosophilidae) on fresh fruit from the USA.Wellington: Ministry for Primary Industries, 2012. 46p. Final: MPI Technical paper n.º 2012/05. , respectively, representing a Figure of about US$ 29.2 million or R$ 75.9 million as maximum potential economics losses caused by D. suzukii in Brazil (Table 3). It should be highlighted that yield losses estimated in 20% must be considered only an average benchmark (Bolda et al., 2010BOLDA, M.P.; GOODHUE, R.E.; ZALOM, F.G. Spotted wing drosophila: potential economic impact of newly established pest. Giannini Foundation of Agricultural Economics, v.13, p.5-8, 2010.), which is a critical simplifying assumption (Goodhue et al., 2011GOODHUE, R.E.; BOLDA, M.; FARNSWORTH, D.; WILLIAMS, J.C.; ZALOM, F.G. Spotted wing drosophila infestation of California strawberries and raspberries: economic analysis of potential revenue losses and control costs. Pest Management Science, v.67, p.1396-1402, 2011. DOI: 10.1002/ps.2259.
https://doi.org/10.1002/ps.2259.... ). An analysis based on price response reduces estimated losses, but the inclusion of managing costs on market prices is not possible due to the lack of identification of suitable control approaches (Goodhue et al., 2011GOODHUE, R.E.; BOLDA, M.; FARNSWORTH, D.; WILLIAMS, J.C.; ZALOM, F.G. Spotted wing drosophila infestation of California strawberries and raspberries: economic analysis of potential revenue losses and control costs. Pest Management Science, v.67, p.1396-1402, 2011. DOI: 10.1002/ps.2259.
https://doi.org/10.1002/ps.2259.... ). In this scenario, a powerful tool for economic analysis, such as partial equilibrium modeling (Soliman et al., 2010SOLIMAN, T.; MOURITS, M.C.M.; OUDE LANSINK, A.G.J.M.; WERF, W. van der. Economic impact assessment in pest risk analysis. Crop Protection, v.29, p.517-524, 2010. DOI: 10.1016/j.cropro.2009.12.014.
https://doi.org/10.1016/j.cropro.2009.12... ), cannot be used to estimate losses of D. suzukii in Brazil. Despite showing limitations for a precise estimation of losses, predicted monetary values for economic impact assessment of invasive pests are very useful for cost-benefit analysis of pest eradication programs (Miranda et al., 2015MIRANDA, S.H.G.; NASCIMENTO, A.M.; XIMENES, V.P. Potenciais impactos socioeconômicos da expansão da mosca-da-carambola. In: VILELA, E.F.; ZUCCHI, R.A. (Ed.). Pragas introduzidas no Brasil: insetos e ácaros. Piracicaba: FEALQ, 2015. p.132-149.).

Figure 4:
Aggregated production per municipality (Mg) of four D. suzukii hosts: grape (Vitis vinifera), apple (Malus domestica), peach (Prunus persica), and persimmon (Diospyros kaki). Source: Instituto Brasileiro de Geografia e Estatística (2013)INSTITUTO BRASILEIRO DE GEOGRAFIA E ESTATÍSTICA. Produção agrícola municipal. 2013. Disponível em: <Disponível em: http://downloads.ibge.gov.br/downloads_estatisticas.htm >. Acesso em: 8 jul. 2014.
http://downloads.ibge.gov.br/downloads_e... .

In spite of the available statistics for grape, apple, pear, and persimmon production in Brazil, there is no data about losses caused by D. suzukii around the world. It is probable that potential losses are lower than those reported for small fruits. The production value of these four fruits is of R$ 3.87 billion or US$ 1.49 billion (Instituto Brasileiro de Geografia e Estatística, 2014INSTITUTO BRASILEIRO DE GEOGRAFIA E ESTATÍSTICA. Produção agrícola municipal. 2014. Disponível em: <Disponível em: http://www.sidra.ibge.gov.br/bda/agric/ >. Acesso em: 3 nov. 2015.
http://www.sidra.ibge.gov.br/bda/agric/... ). Brazilian apple production is almost entirely located in highly favorable areas for D. suzukii establishment, whereas grape production is located in less than half of the highly favorable areas for D. suzukii (Table 2). However, highly favorable areas for D. suzukii account for 90% of the grape production area in South Brazil, mainly in the states of Rio Grande do Sul, Santa Catarina, and Paraná, and for 45% of the grape production area in the state of São Paulo. The São Francisco Valley, the most important area of grape production in the states of Bahia and Pernambuco, in Northeast Brazil, is a climatically unsuitable area for D. suzukii, even in simulated scenarios without temperature stress.

Considering a hypothetical "worst case scenario" - D. suzukii spreads to all climatically suitable areas in Brazil and no control measures are adopted -, fruit production in the state of Rio Grande do Sul would experience the greatest economic impact. Southeastern and northeastern Rio Grande de Sul are areas that concentrate the majority of preferential hosts for D. suzukii. This impact could be expected based on the fact that, in the United States, D. suzukii is adding a cost between US$ 250 to US$ 350 per acre (Werts & Green, 2014WERTS, P.; GREEN, T. Spotted wing drosophila: adding cost to fruit production. Crops and Soils, v.47, p.36-38, 2014. ). Producers of small fruits have been the most affected in economic terms. Before D. suzukii invasion, small fruit growers from Oregon spent US$ 1 million on pest management, and, after the invasion, this aggregated cost increased to US$ 15 million in 2013 (Werts & Green, 2014WERTS, P.; GREEN, T. Spotted wing drosophila: adding cost to fruit production. Crops and Soils, v.47, p.36-38, 2014. ). One of the aspects that has relevance in order to quantify the impact of D. suzukii is that the species is broadening its host range in new environments. This adaptation to new hosts is inferred based on the first records of D. suzukii in Brazil in forest reserves (Santos, 2014SANTOS, R.S.S. dos. Ocorrência de Drosophila suzukii (Matsumura, 1931) (Diptera: Drosophilidae) atacando frutos de morango no Brasil. Bento Gonçalves: Embrapa Uva e Vinho, 2014. 4p. (Embrapa Uva e Vinho. Comunicado técnico, 159).). The population dynamics of D. suzukii may be affected by the fructification patterns of wild hosts. Moreover, the abundance of D. suzukii in orchards will depend on how well the food resources provided by the wild hosts can sustain populations in natural areas. Expected adaptation to new hosts (cultivated and native) in short term may allow D. suzukii to spread in all areas favorable for its development, in which its population might be forming a continuum (Hauser, 2011HAUSER, M. A historic account of the invasion of Drosophila suzukii (Matsumura) (Diptera: Drosophilidae) in the continental United States, with remarks on their identification. Pest Management Science, v.67, p.1352-1357, 2011. DOI: 10.1002/ps.2265.
https://doi.org/10.1002/ps.2265.... ; Maier, 2012MAIER, C.T. First detection and widespread distribution of the spotted wing drosophila, Drosophila suzukii (Matsumura) (Diptera: Drosophilidae), in Connecticut in 2011. Proceedings of the Entomological Society of Washington, v.114, p.329-337, 2012. DOI: 10.4289/0013-8797.114.3.329.
https://doi.org/10.4289/0013-8797.114.3.... ). As a parallel example, the invasive drosophilid Z. indianus is undergoing niche shift after colonization of new areas around the world (Mata et al., 2010MATA, R.A. da; TIDON, R.; CÔRTES, L.G.; DE MARCO JR., P.; DINIZ-FILHO, J.A.F. Invasive and flexible: niche shift in the drosophilid Zaprionus indianus (Insecta, Diptera). Biological Invasions, v.12, p.1231-1241, 2010. DOI: 10.1007/s10530-009-9542-0.
https://doi.org/10.1007/s10530-009-9542-... ). In this case, potential distribution areas can be inferred based on the new locations in which the organism establishes itself.

Considering that the population fluctuation of D. suzukii depends on food resources and temperatures, an inference may be made using population data from other drosophilids. Some vinegar flies, such as Drosophila melanogaster, Drosophila nigricuria, and Drosophila cardinoides, are found in the Pampas region of the state of Rio Grande do Sul. These species are more abundant between June and September, when minimum and maximum average temperatures are between 10 and 25°C (Poppe et al., 2013POPPE, J.L.; VALENTE, V.L.S.; SCHMITZ, H.J. Population dynamics of drosophilids in the Pampa biome in response to temperature. Neotropical Entomology, v.42, p.269-277, 2013. DOI: 10.1007/s13744-013-0125-5.
https://doi.org/10.1007/s13744-013-0125-... ). These temperatures are close to the temperature limits, and these four months will probably be the most favorable. Therefore, this short season of most favorable conditions may decrease the potential economic impact of D. suzukii.

In general, it will be necessary to develop some management options in order to control D. suzukii, with constant surveillance and monitoring during some years. Control measures can be applied based on solid scientific information in the case of phytosanitary emergencies caused by D. suzukii.

Conclusions

References

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History