The risk of Xylella fastidiosa outbreaks will decrease in the Mediterranean olive-producing regions

The bacterium Xylella fastidiosa (Xf) is a worldwide distributed invasive insect-borne plant pathogen, which causes lethal diseases to many economically-important crops including olives, citrus, almonds and grapes as well as numerous forest, ornamental, and uncultivated plants. The Mediterranean basin is the top supplier of olive oil with 93% of the world production and is consequently highly concerned about the recent invasion of Xf in Europe. Recently, bioeconomic models estimated putative losses induced by the spread of Xf across the European olive-producing area ranging from 1.9 to 5.2 billion euros over 50 years; however, such models did not take into account the insect vectors, which constitute a key driver of Xf spread. In the present study, we used bioclimatic species distribution models to predict the current and future climate suitability of the Mediterranean area for the main efficient or putative transmitters of Xf to olive (i.e. Philaenus spumarius, Neophilaenus campestris and Aphrophora alni). An important part of the total extent of the Mediterranean olive-producing area, mainly situated in southern Spain, Turkey and Greece, is predicted as currently poorly suitable for these vector species. Moreover, models forecast that nearly the totality of the Mediterranean olive-producing regions will likely become climatically little suitable for these vectors by 2050 due to climate change. In Europe, Xf outbreaks have occurred so far only in localities predicted as climatically suitable for these main vector species (e.g. the Apulia region of Italy) while the areas predicted as poorly suitable are still apparently Xf-free, which suggests that climate tolerances of vectors might play a main role in shaping Xf outbreaks patterns. This pattern highlights the crucial necessity of accounting for vectors when assessing risk of Xf outbreaks, and when considering vector-borne diseases in general. The risk maps presented here will have important practical application for the optimization of current and future strategies to control Xf in the Mediterranean region.

[1]  F. Porcelli,et al.  No evidence for cicadas’ implication in Xylella fastidiosa epidemiology , 2020 .

[2]  A. Oude Lansink,et al.  Impact of Xylella fastidiosa subspecies pauca in European olives , 2020, Proceedings of the National Academy of Sciences.

[3]  G. Gilioli,et al.  Spittlebugs of Mediterranean Olive Groves: Host-Plant Exploitation throughout the Year , 2020, Insects.

[4]  D. Papachristos,et al.  Presence of Cicadomorpha in olive orchards of Greece with special reference to Xylella fastidiosa vectors , 2020, Journal of Applied Entomology.

[5]  R. Redak,et al.  An overview on the worldwide vectors of Xylella fastidiosa , 2019 .

[6]  R. Waldman,et al.  Evaluation of CNRM Earth System Model, CNRM‐ESM2‐1: Role of Earth System Processes in Present‐Day and Future Climate , 2019, Journal of Advances in Modeling Earth Systems.

[7]  D. Bosco,et al.  Transmission of Xylella fastidiosa Subspecies Pauca Sequence Type 53 by Different Insect Species , 2019, Insects.

[8]  N. Gillett,et al.  The Canadian Earth System Model version 5 (CanESM5.0.3) , 2019, Geoscientific Model Development.

[9]  A. Cruaud,et al.  Xylella fastidiosa: climate suitability of European continent , 2019, Scientific Reports.

[10]  M. Scharf,et al.  Rapid evolutionary responses to insecticide resistance management interventions by the German cockroach (Blattella germanica L.) , 2019, Scientific Reports.

[11]  D. Makowski,et al.  Effectiveness of in planta control measures for Xylella fastidiosa , 2019, EFSA journal. European Food Safety Authority.

[12]  L. Marini,et al.  Landscape composition predicts the distribution of Philaenus spumarius, vector of Xylella fastidiosa, in olive groves , 2019, Journal of Pest Science.

[13]  D. Boscia,et al.  Xylella fastidiosa in Olive in Apulia: Where We Stand. , 2019, Phytopathology.

[14]  M. Pautasso,et al.  A New Resource for Research and Risk Analysis: The Updated European Food Safety Authority Database of Xylella spp. Host Plant Species. , 2019, Phytopathology.

[15]  J. Pereira,et al.  Distribution and Relative Abundance of Insect Vectors of Xylella fastidiosa in Olive Groves of the Iberian Peninsula , 2018, Insects.

[16]  D. Bosco,et al.  Plant Selection and Population Trend of Spittlebug Immatures (Hemiptera: Aphrophoridae) in Olive Groves of the Apulia Region of Italy , 2018, Journal of Economic Entomology.

[17]  R. Karban,et al.  Decline of meadow spittlebugs, a previously abundant insect, along the California coast. , 2018, Ecology.

[18]  S. Soubeyrand,et al.  Inferring pathogen dynamics from temporal count data: the emergence of Xylella fastidiosa in France is probably not recent , 2018, The New phytologist.

[19]  D. Bosco,et al.  Philaenus spumarius: when an old acquaintance becomes a new threat to European agriculture , 2018, Journal of Pest Science.

[20]  J. Tiihonen,et al.  Amygdala-orbitofrontal structural and functional connectivity in females with anxiety disorders, with and without a history of conduct disorder , 2018, Scientific Reports.

[21]  S. Nidelet,et al.  Using insects to detect, monitor and predict the distribution of Xylella fastidiosa: a case study in Corsica , 2018, Scientific Reports.

[22]  Stephen E. Fick,et al.  WorldClim 2: new 1‐km spatial resolution climate surfaces for global land areas , 2017 .

[23]  Pascal O. Title,et al.  ENVIREM: An expanded set of bioclimatic and topographic variables increases flexibility and improves performance of ecological niche modeling , 2016, bioRxiv.

[24]  F. Porcelli,et al.  Spittlebugs as vectors of Xylella fastidiosa in olive orchards in Italy , 2016, Journal of Pest Science.

[25]  Robert P. Anderson,et al.  Environmental filters reduce the effects of sampling bias and improve predictions of ecological niche models , 2014 .

[26]  P. Pliscoff,et al.  Effects of alternative sets of climatic predictors on species distribution models and associated estimates of extinction risk: A test with plants in an arid environment , 2014 .

[27]  J. Lopes,et al.  A survey of potential insect vectors of the plant pathogenic bacterium Xylella fastidiosa in three regions of Spain: short communication , 2014 .

[28]  Luigi Ponti,et al.  Fine-scale ecological and economic assessment of climate change on olive in the Mediterranean Basin reveals winners and losers , 2014, Proceedings of the National Academy of Sciences.

[29]  G. P. Martelli,et al.  IDENTIFICATION OF DNA SEQUENCES RELATED TO XYLELLA FASTIDIOSA IN OLEANDER, ALMOND AND OLIVE TREES EXHIBITING LEAF SCORCH SYMPTOMS IN APULIA (SOUTHERN ITALY) , 2013 .

[30]  M. White,et al.  Selecting thresholds for the prediction of species occurrence with presence‐only data , 2013 .

[31]  F. Jiguet,et al.  Selecting pseudo‐absences for species distribution models: how, where and how many? , 2012 .

[32]  Robert P. Anderson,et al.  Ecological Niches and Geographic Distributions , 2011 .

[33]  Robert P. Anderson,et al.  Ecological Niches and Geographic Distributions (MPB-49) , 2011 .

[34]  S. Emori,et al.  MIROC-ESM 2010: model description and basic results of CMIP5-20c3m experiments , 2011 .

[35]  D. Kriticos,et al.  Pest Risk Maps for Invasive Alien Species: A Roadmap for Improvement , 2010 .

[36]  Alberto Jiménez-Valverde,et al.  The uncertain nature of absences and their importance in species distribution modelling , 2010 .

[37]  A. Peterson,et al.  ENVIRONMENTAL CORRELATION STRUCTURE AND ECOLOGICAL NICHE MODEL PROJECTIONS , 2009 .

[38]  M. Daugherty,et al.  Estimating Xylella fastidiosa transmission parameters: decoupling sharpshooter number and feeding period , 2009 .

[39]  Omri Allouche,et al.  Assessing the accuracy of species distribution models: prevalence, kappa and the true skill statistic (TSS) , 2006 .

[40]  C. Parmesan.  Ecological and Evolutionary Responses to Recent Climate Change , 2006 .

[41]  M. Zappa,et al.  Are niche‐based species distribution models transferable in space? , 2006 .

[42]  R. Karban,et al.  Physiological tolerance, climate change, and a northward range shift in the spittlebug, Philaenus spumarius , 2004 .

[43]  A. Purcell,et al.  Temperature-Dependent Growth and Survival of Xylella fastidiosa in Vitro and in Potted Grapevines. , 2001, Plant disease.

[44]  John Bell,et al.  A review of methods for the assessment of prediction errors in conservation presence/absence models , 1997, Environmental Conservation.

[45]  藤木 幸夫,et al.  THE COLD SPRING HARBOR SYMPOSIUM ON QUANTITATIVE BIOLOGY. , 1996, Science.

[46]  A. Purcell.  Almond Leaf Scorch: Leafhopper and Spittlebug Vectors , 1980 .

[47]  J. Whittaker.  Population Changes in Neophilaenus lineatus (L.) (Homoptera: Cercopidae) in Different Parts of its Range , 1971 .

[48]  M. Torres.  Resultados de las prospecciones realizadas de vectores de "Xylella fastidiosa" , 2020 .

[49]  J. M. D. Alvaro.  Observaciones sobre Philaenus spumarius, vector potencial de Xylella fastidiosa, en el olivar de Sevilla , 2018 .

[50]  M. Plaza,et al.  Vectores de Xylella fastidiosa en la comarca de Guadalest (Alicante) , 2018 .

[51]  Kabir P. Tumber,et al.  Pierce's disease costs California $104 million per year , 2014 .

[52]  R Core Team,et al.  R: A language and environment for statistical computing. , 2014 .

[53]  Keywan Riahi,et al.  A new scenario framework for climate change research: the concept of shared climate policy assumptions , 2014, Climatic Change.

[54]  J. Whittaker,et al.  An altitudinal transect as an indicator of responses of a spittlebug (Auchenorrhyncha: Cercopidae) to climate change , 2013 .

[55]  Keywan Riahi,et al.  A new scenario framework for climate change research: the concept of shared socioeconomic pathways , 2013, Climatic Change.

[56]  Mark New,et al.  Ensemble forecasting of species distributions. , 2007, Trends in ecology & evolution.

[57]  J. Bové,et al.  Etiology of three recent diseases of citrus in São Paulo State: Sudden death, variegated chlorosis and huanglongbing , 2007, IUBMB life.

[58]  Valerio Mazzoni.  Contribution to the knowledge of the Auchenorrhyncha (Hemiptera Fulgoromorpha and Cicadomorpha) of Tuscany (Italy). , 2005 .

[59]  D. Hopkins.  Xylella Fastidiosa: Xylem-Limited Bacterial Pathogen of Plants , 1989 .

[60]  W. G. Ruesink,et al.  Vector intensity: a product of propensity and activity , 1986 .

[61]  W. G. Ruesink,et al.  Plant virus epidemics. Monitoring, modelling and predicting outbreaks. , 1986 .

[62]  A. Purcell.  Vector preference and inoculation efficiency as components of resistance to Pierce's disease in European grape cultivars. , 1981 .

[63]  D. R. King,et al.  Meadow spittlebug, Philaenus leucophthalmus (L.) , 1954 .