Assessing the Global Risk of Establishment of Cydia pomonella (Lepidoptera: Tortricidae) Using CLIMEX and MaxEnt Niche Models

ABSTRACT Accurate assessment of insect pest establishment risk is needed by national plant protection organizations to negotiate international trade of horticultural commodities that can potentially carry the pests and result in inadvertent introductions in the importing countries. We used mechanistic and correlative niche models to quantify and map the global patterns of the potential for establishment of codling moth (Cydia pomonella L.), a major pest of apples, peaches, pears, and other pome and stone fruits, and a quarantine pest in countries where it currently does not occur. The mechanistic model CLIMEX was calibrated using species-specific physiological tolerance thresholds, whereas the correlative model MaxEnt used species occurrences and climatic spatial data. Projected potential distribution from both models conformed well to the current known distribution of codling moth. None of the models predicted suitable environmental conditions in countries located between 20°N and 20°S potentially because of shorter photoperiod, and lack of chilling requirement (<60 d at ≤10°C) in these areas for codling moth to break diapause. Models predicted suitable conditions in South Korea and Japan where codling moth currently does not occur but where its preferred host species (i.e., apple) is present. Average annual temperature and latitude were the main environmental variables associated with codling moth distribution at global level. The predictive models developed in this study present the global risk of establishment of codling moth, and can be used for monitoring potential introductions of codling moth in different countries and by policy makers and trade negotiators in making science-based decisions.

[1]  C. Spirig,et al.  Impact of Climate Change on Voltinism and Prospective Diapause Induction of a Global Pest Insect – Cydia pomonella (L.) , 2012, PloS one.

[2]  P. Geier Population dynamics of codling moth, cydia pomonella (L) (Tortricidae), in the Australian Capital Territory. , 1964 .

[3]  D. Kriticos,et al.  Estimating the global area of potential establishment for the western corn rootworm (Diabrotica virgiferavirgifera) under rain‐fed and irrigated agriculture* , 2012 .

[4]  L. Kumar,et al.  Sensitivity Analysis of CLIMEX Parameters in Modelling Potential Distribution of Lantana camara L. , 2012, PloS one.

[5]  Pulling Out the Evil by the Root: the Codling Moth Cydia pomonella Eradication Programme in Brazil , 2007 .

[6]  J. H. Porter,et al.  The potential effects of climatic change on agricultural insect pests , 1991 .

[7]  G. Anfora,et al.  Electrophysiological responses of Cydia pomonella to codlemone and pear ester ethyl (E,Z)-2,4-decadienoate: peripheral interactions in their perception and evidences for cells responding to both compounds , 2004 .

[8]  M. Kearney,et al.  Correlation and process in species distribution models: bridging a dichotomy , 2012 .

[9]  U. Koch,et al.  Behavioral observations of codling moth, Cydia pomonella, in orchards permeated with synthetic pheromone , 1999, BioControl.

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

[11]  Sunil Kumar,et al.  Assessing the Potential for Establishment of Western Cherry Fruit Fly using Ecological Niche Modeling , 2014, Journal of economic entomology.

[12]  V. Bus,et al.  Apple Volatiles Synergize the Response of Codling Moth to Pear Ester , 2013, Journal of Chemical Ecology.

[13]  Trevor Hastie,et al.  A statistical explanation of MaxEnt for ecologists , 2011 .

[14]  G. Anfora,et al.  Effect of anti‐hail nets on Cydia pomonella behavior in apple orchards , 2008 .

[15]  Steve W. Adkins,et al.  Climate change and the potential distribution of an invasive alien plant: Acacia nilotica ssp. indica in Australia , 2003 .

[16]  P. Calanca,et al.  Quarantine arthropod invasions in Europe: the role of climate, hosts and propagule pressure , 2014 .

[17]  W. W. Coates,et al.  Predicting the emergence of the codling moth, Cydia pomonella (Lepidoptera: Tortricidae), on a degree-day scale in North America. , 2013, Pest management science.

[18]  M. Bosch,et al.  Studies on the Codling Moth (Lepidoptera: Tortricidae) Response to Different Codlemone Release Rates , 2013, Environmental entomology.

[19]  Bruce L. Webber,et al.  Modelling horses for novel climate courses: insights from projecting potential distributions of native and alien Australian acacias with correlative and mechanistic models , 2011 .

[20]  V. Kil’ PCR analysis of codling moth (Cydia pomonella) populations using SSR markers , 2011, Russian Agricultural Sciences.

[21]  E. Mani,et al.  The dispersal of male codling moths (Laspeyresia pomonella L.) in the Upper Rhine Valley , 2009 .

[22]  M De Meyer,et al.  Ecological niche and potential geographic distribution of the invasive fruit fly Bactrocera invadens (Diptera, Tephritidae) , 2009, Bulletin of Entomological Research.

[23]  B. Sauphanor,et al.  Deltamethrin resistance in the codling moth (Lepidoptera: Tortricidae): inheritance and number of genes involved , 2001, Heredity.

[24]  Robert P. Anderson,et al.  Maximum entropy modeling of species geographic distributions , 2006 .

[25]  E. Beers,et al.  Orchard Pest Management: A Resource Book for the Pacific Northwest , 1993 .

[26]  Sam Veloz,et al.  Spatially autocorrelated sampling falsely inflates measures of accuracy for presence‐only niche models , 2009 .

[27]  Steven J. Phillips Transferability, sample selection bias and background data in presence‐only modelling: a response to Peterson et al. (2007) , 2008 .

[28]  M. Barzegar,et al.  Cold tolerance and trehalose accumulation in overwintering larvae of the codling moth, Cydia pomonella (Lepidoptera: Tortricidae) , 2007 .

[29]  Sunil Kumar,et al.  Evaluating correlative and mechanistic niche models for assessing the risk of pest establishment , 2014 .

[30]  Karl J. Niklas,et al.  Invariant scaling relations across tree-dominated communities , 2001, Nature.

[31]  R. W. Sutherst,et al.  A computerised system for matching climates in ecology , 1985 .

[32]  R. Senoussi,et al.  Spatial distribution of an arthropod community in a pear orchard (southern France): Identification of a hedge effect , 2008 .

[33]  V. Košťál,et al.  Overwintering Strategy and Mechanisms of Cold Tolerance in the Codling Moth (Cydia pomonella) , 2013, PloS one.

[34]  Peter-Tobias Stoll,et al.  Agreement on the Application of Sanitary and Phytosanitary Measures , 2007 .

[35]  B. Croft,et al.  THE EFFECTS OF PHOTOPERIOD AND EFFECTIVE TEMPERATURES ON THE SEASONAL PHENOLOGY OF THE CODLING MOTH (LEPIDOPTERA: TORTRICIDAE) , 1978, The Canadian Entomologist.

[36]  A. Townsend Peterson,et al.  Constraints on interpretation of ecological niche models by limited environmental ranges on calibration areas , 2012 .

[37]  M. Parry,et al.  Distribution, Damage and Biology of Codling Moth, Cydia Pomanella (L) , 1981 .

[38]  Jake F. Weltzin,et al.  The biogeography of prediction error: why does the introduced range of the fire ant over-predict its native range? , 2006 .

[39]  J. Lobo,et al.  Species distribution models that do not incorporate global data misrepresent potential distributions: a case study using Iberian diving beetles , 2011 .

[40]  L. Neven Fate of Codling Moth (Lepidoptera: Tortricidae) in Harvested Apples Held Under Short Photoperiod , 2012, Journal of economic entomology.

[41]  J. L. Parra,et al.  Very high resolution interpolated climate surfaces for global land areas , 2005 .

[42]  M. Solomon Predation of overwintering larvae of codling moth (Cydia pomonella (L.) by birds , 1976 .

[43]  K. Kiritani Predicting impacts of global warming on population dynamics and distribution of arthropods in Japan , 2005, Population Ecology.

[44]  G. Anfora,et al.  Mating disruption of codling moth with a continuous adhesive tape carrying high densities of pheromone dispensers , 2009 .

[45]  Jun Ma,et al.  Potential Geographical Distributions of the Fruit Flies Ceratitis capitata, Ceratitis cosyra, and Ceratitis rosa in China , 2009, Journal of economic entomology.

[46]  V. Markó,et al.  Flowers for better pest control? Effects of apple orchard groundcover management on mites (Acari), leafminers (Lepidoptera, Scitellidae), and fruit pests , 2012 .

[47]  Steven J. Phillips,et al.  WHAT MATTERS FOR PREDICTING THE OCCURRENCES OF TREES: TECHNIQUES, DATA, OR SPECIES' CHARACTERISTICS? , 2007 .

[48]  R. Senoussi,et al.  Spatial analyses of ecological count data: a density map comparison approach. , 2010 .

[49]  J. Giliomee,et al.  Effect of Temperature on the Oviposition, Longevity and Mating of Codling Moth, Cydia pomonella (L.) (Lepidoptera: Tortricidae) , 2011 .

[50]  S. U. Karaağaç INSECTICIDE resistance. , 1958, Canadian Medical Association journal.

[51]  J. Avilla,et al.  Comparison of Lures Loaded with Codlemone and Pear Ester for Capturing Codling Moths, Cydia pomonella, in Apple and Pear Orchards using Mating Disruption , 2010, Journal of insect science.

[52]  A. Sarafrazi,et al.  Population variation of codling moth Cydia pomonella (Lep.; Tortricidae) based on molecular data from northwestern Iran , 2011, Turkish Journal of Zoology.

[53]  T. Rafoss,et al.  Spatial and temporal distribution of bioclimatic potential for the Codling moth and the Colorado potato beetle in Norway: model predictions versus climate and field data from the 1990s , 2003 .

[54]  Ç. Şekercioğlu,et al.  The Worldwide Variation in Avian Clutch Size across Species and Space , 2008, PLoS biology.

[55]  M. Saethre,et al.  Distribution of the Codling Moth, Cydia pomonella L. (Lepidoptera: Tortricidae) in Southern Norway , 2001 .

[56]  Damaris Zurell,et al.  Collinearity: a review of methods to deal with it and a simulation study evaluating their performance , 2013 .

[57]  M. F. Malik,et al.  Scouting and Control of Helicoverpa armigera by Synthetic Pheromone Technology in Apple , 2002 .

[58]  K. Pringle,et al.  Field observations on oviposition of codling moth, Cydia pomonella (Linnaeus) (Lepidoptera: Olethreutidae), in an unsprayed apple orchard in South Africa , 1997 .

[59]  K. Abromeit Music Received , 2023, Notes.

[60]  D. Kriticos,et al.  Combining Inferential and Deductive Approaches to Estimate the Potential Geographical Range of the Invasive Plant Pathogen, Phytophthora ramorum , 2013, PloS one.

[61]  L. Neven Effects of Short Photoperiod on Codling Moth Diapause and Survival , 2013, Journal of economic entomology.

[62]  J. Jehle,et al.  Field resistance of codling moth against Cydia pomonella granulovirus (CpGV) is autosomal and incompletely dominant inherited. , 2006, Journal of invertebrate pathology.

[63]  Remigiusz W. Olszak,et al.  Controlling the codling moth [Cydioa pomonella L.} with the 'attract and kill' agent Appeal 04 PA , 2006 .

[64]  Robert P. Anderson,et al.  Estimating optimal complexity for ecological niche models: A jackknife approach for species with small sample sizes , 2013 .

[65]  Jennifer A. Miller,et al.  Mapping Species Distributions: Spatial Inference and Prediction , 2010 .

[66]  C. Wearing Integrated control of apple pests in New Zealand , 1975 .

[67]  Brad Vogus LibGuides: Government Documents - Executive Branch - Department of Agriculture: Animal and Plant Health Inspection Service , 2012 .

[68]  Amanda M. West,et al.  Using district-level occurrences in MaxEnt for predicting the invasion potential of an exotic insect pest in India , 2014 .

[69]  M. Sæthre,et al.  Effect of Temperature on Oviposition Behavior, Fecundity, and Fertility in Two Northern European Populations of the Codling Moth (Lepidoptera: Tortricidae) , 2002 .

[70]  Charles E. Miller,et al.  The Occurrence of Codling Moth in Low Latitude Countries: Validation of Pest Distribution Reports , 2009 .

[71]  Robert P. Anderson,et al.  A framework for using niche models to estimate impacts of climate change on species distributions , 2013, Annals of the New York Academy of Sciences.

[72]  A. Sarafrazi,et al.  An analysis of seasonal dimorphism in codling moths, Cydia pomonella, from Iran using geometric morphometrics , 2014 .

[73]  Matthew J. Smith,et al.  The Effects of Sampling Bias and Model Complexity on the Predictive Performance of MaxEnt Species Distribution Models , 2013, PloS one.

[74]  Bruce L. Webber,et al.  CliMond: global high‐resolution historical and future scenario climate surfaces for bioclimatic modelling , 2012 .

[75]  Sunil Kumar,et al.  Assessing Forest Vulnerability and the Potential Distribution of Pine Beetles Under Current and Future Climate Scenarios in the Interior West of the US , 2011 .

[76]  Jane Elith,et al.  What do we gain from simplicity versus complexity in species distribution models , 2014 .

[77]  N. Mills,et al.  Predicting the potential invasive range of light brown apple moth (Epiphyas postvittana) using biologically informed and correlative species distribution models , 2011, Biological Invasions.

[78]  A. Knight,et al.  An evaluation of orange and clear traps with pear ester to monitor codling moth (Lepidoptera: Tortricidae) in apple orchards , 2013 .

[79]  R. Prokopy,et al.  Ecology and management of apple arthropod pests. , 2003 .

[80]  T. Itioka,et al.  Climatic and intertrophic effects detected in 10-year population dynamics of biological control of the arrowhead scale by two parasitoids in southwestern Japan , 2005, Population Ecology.

[81]  M. Proverbs,et al.  Effect of Heat on the Fertility of the Codling Moth, Carpocapsa pomonella (L.) (Lepidoptera: Olethreutidae) , 1962, The Canadian Entomologist.

[82]  L. Neven,et al.  Physiological Development Time and Zero Development Temperature of the Codling Moth (Lepidoptera: Tortricidae) , 2000 .

[83]  K. Saikkonen,et al.  Climate change-driven species' range shifts filtered by photoperiodism , 2012 .

[84]  X. Basagaña,et al.  Measurement errors in the assessment of exposure to solar ultraviolet radiation and its impact on risk estimates in epidemiological studies , 2011, Photochemical & photobiological sciences : Official journal of the European Photochemistry Association and the European Society for Photobiology.

[85]  L. Anshelevich,et al.  Control of the codling moth (cydia pomonella) in apple and pear orchards in Israel by mating disruption , 1995, Phytoparasitica.

[86]  A. Peterson,et al.  The crucial role of the accessible area in ecological niche modeling and species distribution modeling , 2011 .

[87]  J. Samietz,et al.  Mating disruption of codling moth, Cydia pomonella (L.), using Isomate C plus dispensers in apple orchards of Bulgaria. , 2009 .

[88]  Jason L. Brown SDMtoolbox: a python‐based GIS toolkit for landscape genetic, biogeographic and species distribution model analyses , 2014 .

[89]  D. Roberts,et al.  The WTO Agreement on the Application of Sanitary and Phytosanitary Measures: a catalyst for regulatory reform? , 2001 .

[90]  T. Tuovinen,et al.  'Candidatus Phytoplasma mali' infected Cacopsylla picta found in apple orchards in south-western Finland. , 2011 .

[91]  Miroslav Dudík,et al.  Modeling of species distributions with Maxent: new extensions and a comprehensive evaluation , 2008 .

[92]  S. Applebaum,et al.  Diapause induction in field populations of the codling moth,Cydia Pomonella, in Northern Israel , 1988, Phytoparasitica.

[93]  A. Peterson,et al.  INTERPRETATION OF MODELS OF FUNDAMENTAL ECOLOGICAL NICHES AND SPECIES' DISTRIBUTIONAL AREAS , 2005 .

[94]  Robert A. Boria,et al.  Spatial filtering to reduce sampling bias can improve the performance of ecological niche models , 2014 .

[95]  K. Mody,et al.  Influence of Canopy Aspect and Height on Codling Moth (Lepidoptera: Tortricidae) Larval Infestation in Apple, and Relationship between Infestation and Fruit Size , 2008, Journal of economic entomology.

[96]  J. Elith,et al.  Sensitivity of predictive species distribution models to change in grain size , 2007 .

[97]  D. Briese,et al.  THE DEMOGRAPHIC PERFORMANCE OF A LABORATORY STRAIN OF CODLING MOTH, CYDIA POMONELLA (LEPIDOPTERA: TORTRICIDAE) , 1978 .

[98]  K. Stahl,et al.  Climate change could alter the distribution of mountain pine beetle outbreaks in western Canada , 2012 .

[99]  A. Knight Codling Moth Areawide Integrated Pest Management , 2008 .

[100]  D. Pimentel,et al.  Environmental and Economic Costs of Nonindigenous Species in the United States , 2000 .

[101]  A. Peterson,et al.  Evidence of climatic niche shift during biological invasion. , 2007, Ecology letters.

[102]  Lael Parrott,et al.  Viewing forests through the lens of complex systems science , 2014 .

[103]  Michael A. Rodriguez,et al.  Susceptibility to Organophosphate Insecticides and Activity of Detoxifying Enzymes in Spanish Populations of Cydia pomonella (Lepidoptera: Tortricidae) , 2010, Journal of economic entomology.

[104]  P. L. Shaffer,et al.  Developmental Rates of Codling Moth (Lepidoptera: Olethreutidae) Reared on Apple at Four Constant Temperatures , 1983 .

[105]  D. Richardson,et al.  Niche‐based modelling as a tool for predicting the risk of alien plant invasions at a global scale , 2005, Global change biology.

[106]  Richard E. Glor,et al.  ENMTools: a toolbox for comparative studies of environmental niche models , 2010 .

[107]  Darren J. Kriticos,et al.  CLIMEX Version 3: User's Guide , 2007 .

[108]  B. Sauphanor,et al.  Genetic architecture in codling moth populations: comparison between microsatellite and insecticide resistance markers , 2007, Molecular ecology.

[109]  David G. Williams,et al.  Dual pheromone dispenser for combined control of codling moth Cydia pomonella L. and oriental fruit moth Grapholita molesta (Busck) (Lep., Tortricidae) in pears , 2007 .