Theoretical and Applied Climatology

, Volume 135, Issue 1–2, pp 409–424 | Cite as

Suitable areas of Phakopsora pachyrhizi, Spodoptera exigua, and their host plant Phaseolus vulgaris are projected to reduce and shift due to climate change

  • Nadiezhda Yakovleva Zitz Ramirez-CabralEmail author
  • Lalit Kumar
  • Farzin Shabani
Original Paper


Worldwide, crop pests (CPs) such as pathogens and insects affect agricultural production detrimentally. Species distribution models can be used for projecting current and future suitability of CPs and host crop localities. Our study overlays the distribution of two CPs (Asian soybean rust and beet armyworm) and common bean, a potential host of them, in order to determine their current and future levels of coexistence. This kind of modeling approach has rarely been performed previously in climate change studies. The soybean rust and beet armyworm model projections herein show a reduction of the worldwide area with high and medium suitability of both CPs and a movement of them away from the Equator, in 2100 more pronounced than in 2050. Most likely, heat and dry stress will be responsible for these changes. Heat and dry stress will greatly reduce and shift the future suitable cultivation area of common bean as well, in a similar manner. The most relevant findings of this study were the reduction of the suitable areas for the CPs, the reduction of the risk under future scenarios, and the similarity of trends for the CPs and host. The current results highlight the relation between and the coevolution of host and pathogens.


Food security Climate change Asiatic soybean rust Beet armyworm Common bean Suitability Abiotic stresses 


  1. Agrios GN (2004) Plant pathology, Elsevier Academic PressGoogle Scholar
  2. ALA. (2014). Atlas of Living Australia. 2014, from
  3. Aluja M, Guillén L, Rull J, Höhn H, Frey J, Graf B, Samietz J (2011) Is the alpine divide becoming more permeable to biological invasions?–Insights on the invasion and establishment of the walnut husk fly, Rhagoletis completa (Diptera: Tephritidae) in Switzerland. Bull Entomol Res 101(04):451–465. CrossRefGoogle Scholar
  4. Amaya OS, Restrepo OD, Argüelles J, Garramuño EA (2009) Evaluación del comportamiento del complejo Spodoptera con la introducción de algodón transgénico al Tolima, Colombia. Revista Corpoica-Ciencia y Tecnología Agropecuaria 10(1):24–32. CrossRefGoogle Scholar
  5. Babu SC, Rajasekaran B (1989) Dynamic economic injury levels of soybean rust-a dynamic programming model. Soybean Rust Newsletter 9:10–14Google Scholar
  6. Bandyopadhyay R, Ojiambo P, Twizeyimana M, Asafo-Adjei B, Frederick R, Pedley K, Stone C, Hartman G (2007) First report of soybean rust caused by Phakopsora pachyrhizi in Ghana. Plant Dis 91(8):1057–1057. CrossRefGoogle Scholar
  7. Battisti DS, Naylor RL (2009) Historical warnings of future food insecurity with unprecedented seasonal heat. Science 323(5911):240–244. CrossRefGoogle Scholar
  8. Baysal-Gurel F, Ivey MLL, Dorrance A, Luster D, Frederick R, Czarnecki J, Boehm M, Miller SA (2008) An immunofluorescence assay to detect urediniospores of Phakopsora pachyrhizi. Plant Dis 92(10):1387–1393. CrossRefGoogle Scholar
  9. Bebber DP (2015) Range-expanding pests and pathogens in a warming world. Annu Rev Phytopathol 53(1):335–356. CrossRefGoogle Scholar
  10. Bebber DP, Holmes T, Smith D, Gurr SJ (2014) Economic and physical determinants of the global distributions of crop pests and pathogens. New Phytol 202(3):901–910. CrossRefGoogle Scholar
  11. Berzitis EA, Minigan JN, Hallett RH, Newman JA (2014) Climate and host plant availability impact the future distribution of the bean leaf beetle (Cerotoma Trifurcata). Glob Chang Biol 20(9):2778–2792. CrossRefGoogle Scholar
  12. Bonde M, Berner D, Nester S, Frederick R (2007) Effects of temperature on urediniospore germination, germ tube growth, and initiation of infection in soybean by Phakopsora isolates. Phytopathology 97(8):997–1003. CrossRefGoogle Scholar
  13. Bregaglio S, Cappelli G, Donatelli M (2012) Evaluating the suitability of a generic fungal infection model for pest risk assessment studies. Ecol Model 247:58–63. CrossRefGoogle Scholar
  14. Broughton W, Hernandez G, Blair M, Beebe S, Gepts P, Vanderleyden J (2003) Beans (Phaseolus spp.)—model food legumes. Plant Soil 252(1):55–128. CrossRefGoogle Scholar
  15. Capinera JL (2008) Encyclopedia of entomology, Springer Science & Business Media, DOI:
  16. Capinera JL (2014) Beet armyworm, Spodoptera exigua (Hübner)(Insecta: Lepidoptera: Noctuidae), University of Florida Cooperative Extension Service. Institute of Food and Agricultural Sciences, EDISGoogle Scholar
  17. Cárcamo Rodríguez A, Rios JA, Hernández J (2006) First report of Asian soybean rust caused by Phakopsora pachyrhizi from Mexico. Plant Dis 90(9):1260–1260. CrossRefGoogle Scholar
  18. Cassman KG (1999) Ecological intensification of cereal production systems: yield potential, soil quality, and precision agriculture. Proc Natl Acad Sci 96(11):5952–5959. CrossRefGoogle Scholar
  19. Chakraborty S (2013) Migrate or evolve: options for plant pathogens under climate change. Glob Chang Biol 19(7):1985–2000. CrossRefGoogle Scholar
  20. Chakraborty S, Datta S (2003) How will plant pathogens adapt to host plant resistance at elevated CO2 under a changing climate? New Phytol 159(3):733–742. CrossRefGoogle Scholar
  21. Chakraborty S, Newton AC (2011) Climate change, plant diseases and food security: an overview. Plant Pathol 60(1):2–14. CrossRefGoogle Scholar
  22. Chen I-C, Hill JK, Ohlemüller R, Roy DB, Thomas CD (2011) Rapid range shifts of species associated with high levels of climate warming. Science 333(6045):1024–1026. CrossRefGoogle Scholar
  23. Constenla M (1988) El uso de plaguicidas en America Latina: tendencias e implicaciones ambientales. International symposium on changing perspectives in agrochemicals: isotopic techniques for the study of food and environmental implications, Neuherberg (Germany, FR), pp 24–27Google Scholar
  24. Cook WC (1931) Notes on predicting the probable future distribution of introduced insects. Ecology 12(2):245–247. CrossRefGoogle Scholar
  25. Cortez-Mondaca E, J Pérez-Márquez, E Sifuentes-Ibarra, C Garcia-Gutierrez, Valenzuela-Escoboza FA and JR Camacho-Baez (2014). Impacto del cambio climático sobre insectos en Sinaloa; el caso palomilla de la papa Phthorimaea operculella Zeller 1873 (Lepidoptera: Gelechiidae). En Sinaloa y el cambio climático global. L. M. Flores-Campana, R. E. Moran-Angulo and C. Karam-Quiniones: 219–235Google Scholar
  26. Crisp MD, Arroyo MT, Cook LG, Gandolfo MA, Jordan GJ, McGlone MS, Weston PH, Westoby M, Wilf P, Linder HP (2009) Phylogenetic biome conservatism on a global scale. Nature 458(7239):754–756. CrossRefGoogle Scholar
  27. Del Ponte EM, Esker PD (2008) Meteorological factors and Asian soybean rust epidemics: a systems approach and implications for risk assessment. Sci Agric 65(SPE):88–97CrossRefGoogle Scholar
  28. Demirel MC, Moradkhani H (2016) Assessing the impact of CMIP5 climate multi-modeling on estimating the precipitation seasonality and timing. Clim Chang 135(2):357–372. CrossRefGoogle Scholar
  29. Desborough P (1984) Selection of soybean cultivar and sowing date as a strategy for avoidance of rust (Phakopsora pachyrhizi Syd.) losses in coastal New South Wales. Anim Prod Sci 24(126):433–439. CrossRefGoogle Scholar
  30. Diaz BME (2004) Computarización de la Colección Nacional de insectos Dr. Alfredo Barrera Marín del Museo de Historia Natural de la Ciudad de México. Base Lepidoptera Consejo Internacional para la Preservación de las Aves-Sección Mexicana.. SNIB-CONABIO, México, D.FGoogle Scholar
  31. Dormann CF, Schymanski SJ, Cabral J, Chuine I, Graham C, Hartig F, Kearney M, Morin X, Römermann C, Schröder B (2012) Correlation and process in species distribution models: bridging a dichotomy. J Biogeogr 39(12):2119–2131. CrossRefGoogle Scholar
  32. EPPO (2009). Alert list: Phakopsora pachyrhizi (Asian soybean rust), EPPOGoogle Scholar
  33. Fisher MC, Henk DA, Briggs CJ, Brownstein JS, Madoff LC, McCraw SL, Gurr SJ (2012) Emerging fungal threats to animal, plant and ecosystem health. Nature 484(7393):186–194. CrossRefGoogle Scholar
  34. GBIF. (2015). the global biodiversity information facility. 2014, from
  35. Grafton RQ, Daugbjerg C, Qureshi ME (2015) Towards food security by 2050. Food Security 7(2):179–183. CrossRefGoogle Scholar
  36. Grapputo A, Boman S, Lindstrom L, Lyytinen A, Mappes J (2005) The voyage of an invasive species across continents: genetic diversity of North American and European Colorado potato beetle populations. Mol Ecol 14(14):4207–4219. CrossRefGoogle Scholar
  37. Grewal PS, Gaugler R, Lewis EE (1993) Host recognition behavior by entomopathogenic nematodes during contact with insect gut contents. J Parasitol 79(4):495–503. CrossRefGoogle Scholar
  38. Guo H, Sun Y, Li Y, Tong B, Harris M, Zhu-Salzman K, Ge F (2013) Pea aphid promotes amino acid metabolism both in Medicago truncatula and bacteriocytes to favor aphid population growth under elevated CO2. Glob Chang Biol 19(10):3210–3223. CrossRefGoogle Scholar
  39. Hanssen K (1970) Production of seed beans for export. Rhod Agric J 67:45–50Google Scholar
  40. Harmon PF, Momol MT, Marois J, Dankers H, Harmon CL (2005) Asian soybean rust caused by Phakopsora pachyrhizi on soybean and kudzu in Florida. Plant Health Progress 2005:1–4Google Scholar
  41. Hershman D, Bachi P, Harmon C, Harmon P, Palm M, McKemy J, Zeller K, Levy L (2006) First report of soybean rust caused by Phakopsora pachyrhizi on Kudzu (Pueraria montana var. lobata) in Kentucky. Plant Dis 90(6):834–834. CrossRefGoogle Scholar
  42. Hovmoller MS, Yahyaoui AH, Milus EA, Justesen AF (2008) Rapid global spread of two aggressive strains of a wheat rust fungus. Mol Ecol 17(17):3818–3826. CrossRefGoogle Scholar
  43. IPCC (2007). Climate change 2007: the physical science basis. Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change. S. Solomon, D. Qin, M. Manning et al., Cambridge University press, Cambridge: 996Google Scholar
  44. Isakeit T, Miller M, Saldana R, Barnes L, McKemy J, Palm M, Zeller K, DeVries-Paterson R, Levy L (2006) First report of rust caused by Phakopsora pachyrhizi on soybean and kudzu in Texas. Plant Dis 90(7):971–971. CrossRefGoogle Scholar
  45. Ivancovich A, Botta G, Rivadaneira M, Saieg E, Erazzu L, Guillin E (2007) First report of soybean rust caused by Phakopsora pachyrhizi on Phaseolus spp. in Argentina. Plant Dis 91(1):111–111. CrossRefGoogle Scholar
  46. Jarvie JA (2009) A review of soybean rust from a South African perspective. S Afr J Sci 105(3–4):103–108Google Scholar
  47. Juroszek P, von Tiedemann A (2015) Linking plant disease models to climate change scenarios to project future risks of crop diseases: a review. J Plant Dis Protect 122(1):3–15. CrossRefGoogle Scholar
  48. Karimi-Malati A, Fathipour Y, Talebi AA (2014) Development response of Spodoptera Exigua to eight constant temperatures: linear and nonlinear modeling. J Asia Pac Entomol 17(3):349–354. CrossRefGoogle Scholar
  49. Kim K, Wang T, Yang X (2005) Simulation of apparent infection rate to predict severity of soybean rust using a fuzzy logic system. Phytopathology 95(10):1122–1131. CrossRefGoogle Scholar
  50. Kochman J (1979) The effect of temperature on development of soybean rust (Phakopsora pachyrhizi). Crop and Pasture Sci 30(2):273–277. CrossRefGoogle Scholar
  51. Koenning S, Moore A, Creswell T, Abad G, Palm M, McKemy J, Hernández J, Levy L, DeVries-Paterson R (2006) First report of soybean rust caused by Phakopsora pachyrhizi in North Carolina. Plant Dis 90(7):973–973. CrossRefGoogle Scholar
  52. Kriticos DJ, Webber BL, Leriche A, Ota N, Macadam I, Bathols J, Scott JK (2011) CliMond: global high-resolution historical and future scenario climate surfaces for bioclimatic modelling. Methods Ecol Evol 3(1):53–64CrossRefGoogle Scholar
  53. Kriticos DJ, Reynaud P, Baker RHA, Eyre D (2012) Estimating the global area of potential establishment for the western corn rootworm (Diabrotica virgifera virgifera) under rain-fed and irrigated agriculture. OEPP/EPPO Bull 42(1):56–64. CrossRefGoogle Scholar
  54. Kriticos D, Maywald G, Yonow T, Zurcher E, Herrmann N, Sutherst R (2015a) CLIMEX version 4: exploring the effects of climate on plants, animals and diseases. CSIRO, Canberra, ACTGoogle Scholar
  55. Kriticos DJ, Ota N, Hutchison WD, Beddow J, Walsh T, Tay WT, Borchert DM, Paula-Moraes SV, Czepak C, Zalucki MP (2015b) The potential distribution of invading Helicoverpa armigera in North America: is it just a matter of time? PLoS One 10(7)Google Scholar
  56. Kumar S, Verma R (1985) Soyabean rust in NE hills of India: further observations. Soybean Rust Newsletter 7:17–19Google Scholar
  57. Lamichhane JR, Barzman M, Booij K, Boonekamp P, Desneux N, Huber L, Kudsk P, Langrell SRH, Ratnadass A, Ricci P, Sarah J-L, Messéan A (2015) Robust cropping systems to tackle pests under climate change. A review. Agron Sustain Dev 35(2):443–459CrossRefGoogle Scholar
  58. Leach MC, Hobbs SL (2013) Plantwise knowledge bank: delivering plant health information to developing country users. Learn Publ 26(3):180–185Google Scholar
  59. Lenz HD, Bartha B, Straßer L, Lemme H (2016) Development of ash dieback in south-eastern Germany and the increasing occurrence of secondary pathogens. Forests 7(2):41. CrossRefGoogle Scholar
  60. Logan JA, Powell JA (2001) Ghost forests, global warming, and the mountain pine beetle (Coleoptera: Scolytidae). Am Entomol 47(3):160–173. CrossRefGoogle Scholar
  61. Lynch T, Marois J, Wright D, Harmon P, Harmon C, Miles M, Hartman G (2006) First report of soybean rust caused by Phakopsora pachyrhizi on Phaseolus spp. in the United States. Plant Dis 90(7):970–970. CrossRefGoogle Scholar
  62. Mahdian K, Vantornhout I, Tirry L, De Clercq P (2006) Effects of temperature on predation by the stinkbugs Picromerus bidens and Podisus maculiventris (Heteroptera: Pentatomidae) on noctuid caterpillars. Bull Entomol Res 96(05):489–496Google Scholar
  63. Marchetti M, Melching J, Bromfield K (1976) The effects of temperature and dew period on germination and infection by uredospores of Phakopsora pachyrhizi. Phytopathology 66(4):461–463. CrossRefGoogle Scholar
  64. Melching J, Dowler W, Koogle D, Royer M (1989) Effects of duration, frequency, and temperature of leaf wetness periods on soybean rust. Plant Dis 73(2):117–122. CrossRefGoogle Scholar
  65. Mendelsohn R, Dinar A (1999) Climate change, agriculture, and developing countries: does adaptation matter? World Bank Res Observer 14(2):277–293. CrossRefGoogle Scholar
  66. Mullen J, Sikora E, McKemy J, Palm M, Levy L, DeVries-Paterson R (2006) First report of Asian soybean rust caused by Phakopsora pachyrhizi on soybean in Alabama. Plant Dis 90(1):112–112. CrossRefGoogle Scholar
  67. Murillo-Williams A, Esker P, Allen T, Stone C, Frederick R (2015) First report of Phakopsora pachyrhizi on soybean in Costa Rica. Plant Dis 99(3):418–418. CrossRefGoogle Scholar
  68. Murithi H, Beed F, Soko M, Haudenshield J, Hartman G (2015) First report of Phakopsora pachyrhizi causing rust on soybean in Malawi. Phytopathology 105(7):905–916CrossRefGoogle Scholar
  69. Murithi H, Beed F, Tukamuhabwa P, Thomma B, Joosten M (2016) Soybean production in eastern and southern Africa and threat of yield loss due to soybean rust caused by Phakopsora pachyrhizi. Plant Pathol 65(2):176–188. CrossRefGoogle Scholar
  70. Nakicenovic N and R Swart (2000). Special report on emissions scenarios. Special Report on Emissions Scenarios, Edited by Nebojsa Nakicenovic and Robert Swart, pp. 612. ISBN 0521804930. Cambridge, UK: Cambridge University Press, July 2000. 1 Google Scholar
  71. Nunkumar A, Caldwell P, Pretorius Z (2008) Alternative hosts of Asian soybean rust (Phakopsora pachyrhizi) in South Africa. S Afr J Plant and Soil 25(1):62–63. CrossRefGoogle Scholar
  72. Oerke E-C (2006) Crop losses to pests. J Agric Sci 144(01):31–43. CrossRefGoogle Scholar
  73. Parmesan C (2006) Ecological and evolutionary responses to recent climate change. Annu Rev Ecol Evol Syst 37(1):637–669. CrossRefGoogle Scholar
  74. Pivonia S, Yang X (2004) Assessment of the potential year-round establishment of soybean rust throughout the world. Plant Dis 88(5):523–529. CrossRefGoogle Scholar
  75. Ploper L, González V, Gálvez M, de Ramallo N, Zamorano M, García G, Castagnaro A (2005) Detection of soybean rust caused by Phakopsora pachyrhizi in Northwestern Argentina. Plant Dis 89(7):774–774. CrossRefGoogle Scholar
  76. Porch TG, Beaver JS, Debouck DG, Jackson S, Kelly JD, Dempewolf H (2013) Use of Wild Relatives and Closely Related Species to Adapt Common Bean to Climate Change. Agronomy 3(2):433–461.
  77. Pyšek P, Richardson DM, Pergl J, Jarošík V, Sixtová Z, Weber E (2008) Geographical and taxonomic biases in invasion ecology. Trends Ecol Evol 23(5):237–244. CrossRefGoogle Scholar
  78. Ram H, Rashid A, Zhang W, Duarte A, Phattarakul N, Simunji S, Kalayci M, Freitas R, Rerkasem B, Bal R (2016) Biofortification of wheat, rice and common bean by applying foliar zinc fertilizer along with pesticides in seven countries. Plant Soil:1–13Google Scholar
  79. Ramírez OA, Mumford JD (2008) Formulación de políticas fitosanitarias en América Central1. Manejo integrado de plagas en Mesoamerica 40:399Google Scholar
  80. Ramirez-Cabral NYZ, Kumar L, Taylor S (2016) Crop niche modeling projects major shifts in common bean growing areas. Agric For Meteorol 218:102–113CrossRefGoogle Scholar
  81. Ramirez-Villegas J, Challinor AJ, Thornton PK, Jarvis A (2013) Implications of regional improvement in global climate models for agricultural impact research. Environ. Res Lett 8, 024018 p 12.
  82. Rao V, Raut V, Patil V (1995) Out-break of soybean rust in Maharashtra. J Maharashtra Agri Univ 20(3):479–480Google Scholar
  83. Romero NJ (1998) Catálogo de insectos de la colección del Centro de Entomología. Colegio de Postgraduados. Instituto de Fitosanidad. SNIB-CONABIO, México, D.FGoogle Scholar
  84. Sabburg R, Obanor F, Aitken E, Chakraborty S (2015) Changing fitness of a necrotrophic plant pathogen under increasing temperature. Glob Chang Biol 21(8):3126–3137. CrossRefGoogle Scholar
  85. Santana Torres Y, Martínez de la Parte E, Pérez Vicente L, Rodríguez Bustamante E, Sánchez Marín R (2012) Alternative hosts of Phakopsora pachyrhizi in soybeans fields (Glycine max) of Ciego de Ávila province, Cuba. Fitosanidad 16(2):69–72Google Scholar
  86. Schoonhoven LM, Van Loon JJ, Dicke M (2005) Insect-plant biology. Press on Demand, Oxford UniversityGoogle Scholar
  87. Sconyers L, Kemerait Jr R, Brock J, Gitaitis R, Sanders F, Phillips D, Jost P (2006) First report of Phakopsora pachyrhizi, the causal agent of Asian soybean rust, on Florida beggarweed in the United States. Plant Dis 90(7):972–972. CrossRefGoogle Scholar
  88. Shabani F, Kumar L (2013) Risk levels of invasive Fusarium oxysporum f. sp. in areas suitable for date palm (Phoenix dactylifera) cultivation under various climate change projections. PLoS One 8(12):e83404. CrossRefGoogle Scholar
  89. Shabani F, Kumar L (2014) Sensitivity analysis of CLIMEX parameters in modeling potential distribution of Phoenix dactylifera L. PLoS One 9(4):e94867. CrossRefGoogle Scholar
  90. Shabani F, Kumar L (2015) Should species distribution models use only native or exotic records of existence or both? Ecol Inform 29:57–65. CrossRefGoogle Scholar
  91. Shabani F, Kumar L, Taylor S (2012) Climate change impacts on the future distribution of date palms: a modeling exercise using CLIMEX. PLoS One 7(10):1–12CrossRefGoogle Scholar
  92. Shabani F, Kumar L, Taylor S (2013) Suitable regions for date palm cultivation in Iran are predicted to increase substantially under future climate change scenarios. J Agric Sci 152(04):543–557CrossRefGoogle Scholar
  93. Shabani F, Kumar L, Nojoumian AH, Esmaeili A, Toghyani M (2016) Projected future distribution of date palm and its potential use in alleviating micronutrient deficiency. J Sci Food Agric 96(4):1132–1140. CrossRefGoogle Scholar
  94. da Silva RS, L Kumar, F Shabani and MC Picanço (2016). Potential risk levels of invasive Neoleucinodes elegantalis (small tomato borer) in areas optimal for open field Solanum lycopersicum (tomato) cultivation in the present and under predicted climate change. Pest Manag SciGoogle Scholar
  95. Singh RP, Hodson DP, Huerta-Espino J, Jin Y, Bhavani S, Njau P, Herrera-Foessel S, Singh PK, Singh S, Govindan V (2011) The emergence of Ug99 races of the stem rust fungus is a threat to world wheat production. Annu Rev Phytopathol 49(1):465–481. CrossRefGoogle Scholar
  96. Slaminko T, Miles M, Frederick R, Bonde M, Hartman G (2008) New legume hosts of Phakopsora pachyrhizi based on greenhouse evaluations. Plant Dis 92(5):767–771. CrossRefGoogle Scholar
  97. Sturrock R, Frankel S, Brown A, Hennon P, Kliejunas J, Lewis K, Worrall J, Woods A (2011) Climate change and forest diseases. Plant Pathol 60(1):133–149. CrossRefGoogle Scholar
  98. Sutherst RW (2014) Pest species distribution modelling: origins and lessons from history. Biol Invasions 16(2):239–256. CrossRefGoogle Scholar
  99. Sutherst R, Maywald G (1985) A computerised system for matching climates in ecology. Agric Ecosyst Environ 13(3):281–299. CrossRefGoogle Scholar
  100. Sutherst R, Maywald G, Bourne A (2007a) Including species interactions in risk assessments for global change. Glob Chang Biol 13(9):1843–1859. CrossRefGoogle Scholar
  101. Sutherst R, G Maywald and D Kriticos (2007b) CLIMEX version 3: user’s guide. Hearne Scientific Software Pty Ltd.Google Scholar
  102. Tschanz A, T Wang and B Tsai (1983) Recent advances in soybean rust research. International Symposium on Soybean in Tropical and Sub-tropical Cropping SystemsGoogle Scholar
  103. Twizeyimana M, Ojiambo P, Ikotun T, Ladipo J, Hartman G, Bandyopadhyay R (2008) Evaluation of soybean germplasm for resistance to soybean rust (Phakopsora pachyrhizi) in Nigeria. Plant Dis 92(6):947–952. CrossRefGoogle Scholar
  104. Václavík T, Meentemeyer RK (2009) Invasive species distribution modeling (iSDM): are absence data and dispersal constraints needed to predict actual distributions? Ecol Model 220(23):3248–3258. CrossRefGoogle Scholar
  105. Vasseur DA, DeLong JP, Gilbert B, Greig HS, Harley CD, McCann KS, Savage V, Tunney TD, O'Connor MI (2014) Increased temperature variation poses a greater risk to species than climate warming. Proc R Soc Lond B Biol Sci 281(1779):20132612. CrossRefGoogle Scholar
  106. Wang T, Hartman G (1992) Epidemiology of soybean rust and breeding for host resistance. Plant Protect Bull (Taipei) 34(2):109–124Google Scholar
  107. Wilson J (1932) Notes on the biology of Laphygma exigua Hübner. Florida Entomol 16(3):33–39. CrossRefGoogle Scholar
  108. Yañez-Lopez R, Hernández-Zul MI, Quijano-Carranza JÁ, Terán-Vargas AP, Pérez-Moreno L, Díaz-Padilla G, Rico-García E (2015) Potential distribution zones for soybean rust (Phakopsora pachyrhizi) in Mexico. Ecosistemas y Recursos Agropecuarios 2(6):291–302Google Scholar
  109. Yeh C, Sinclair J, Tschanz A (1982) Phakopsora pachyrhizi: Uredial development, urediospore production and factors affecting teliospore formation on soybeans. Crop and Pasture Sci 33(1):25–31. CrossRefGoogle Scholar
  110. Zheng X-L, Cong X-P, Wang X-P, Lei C-L (2011) Pupation behaviour, depth, and site of Spodoptera Exigua. Bull Insectol 64:209–214Google Scholar
  111. Zheng X-L, Wang P, Cheng W-J, Wang X-P, Lei C-L (2012) Projecting overwintering regions of the beet armyworm, Spodoptera exigua in China using the CLIMEX model. J Insect Sci 12(13):1–13. CrossRefGoogle Scholar
  112. Zheng X-L, Huang Q-C, Cao W-Z, Lu W, Wang G-Q, Yu S-Z, Yang Z-D, Wang X-P (2015) Modeling climate change impacts on overwintering of Spodoptera exigua Hübner in regions of China. Chilean J Agr Res 75(3):328–333. CrossRefGoogle Scholar

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© Springer-Verlag GmbH Austria, part of Springer Nature 2018

Authors and Affiliations

  • Nadiezhda Yakovleva Zitz Ramirez-Cabral
    • 1
    • 2
    Email author
  • Lalit Kumar
    • 1
  • Farzin Shabani
    • 1
  1. 1.Ecosystem Management, School of Environmental and Rural ScienceUniversity of New EnglandArmidaleAustralia
  2. 2.INIFAP, Campo Experimental ZacatecasZacatecasMexico

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