Abstract
Reliable niche models are a cornerstone of pest risk analyses, informing biosecurity policies and the management of biological invasions. Because species can invade and establish in areas with climates that are different from those that are found in their native range, it is important to accurately capture the range-limiting mechanisms in models that project climate suitability. We examined a published niche model for the beet armyworm, Spodoptera exigua, to assess its suitability for bioeconomic analyses of its pest threat, and identified issues with the model that rendered it unreliable for this purpose. Consequently, we refitted the CLIMEX model, paying close attention to the biology underpinning the stress mechanisms. This highlighted the necessity of carefully considering how the different stress mechanisms operate, and to select mechanisms which align with knowledge on the species’ biology. We also identified the important role of irrigation in modifying habitat suitability. The refitted model accords with both distribution data and our understanding of the biology of this species, including its seasonal range dynamics. The new model identifies establishment risks to South America, Africa, the Middle East and Asia, and highlights that under current climate, Europe is only climatically suitable during warm seasons when crops are available. The modelling exercise reinforced the importance of understanding the meaning of a location record (e.g. persistent versus ephemeral populations) and of carefully exploring the role of habitat-modifying factors, such as irrigation, in allowing species to persist in otherwise inclement localities.
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References
Adamczyk J Jr, Williams M, Reed J, Hubbard D, Hardee D (2003) Spatial and temporal occurrence of beet armyworm (Lepidoptera: Noctuidae) moths in Mississippi. Fla Entomol 86:229–232
ALA Atlas of Living Australia. http://bie.ala.org.au/species/urn:lsid:biodiversity.org.au:afd.taxon:94bb2aff-6dcc-4040-8d23-ac3c5cf59875. Accessed 6 Dec 2013
Ali A, Gaylor M (1992) Effects of temperature and larval diet on development of the beet armyworm (Lepidoptera: Noctuidae). Environ Entomol 21:780–786
Atapour M, Moharramipour S (2014) Cold hardiness process of beet armyworm larvae, Spodoptera exigua (Lepidoptera: Noctuidae). J Crop Prot 3:147–158
Baker R, Sansford C, Jarvis C, Cannon R, MacLeod A, Walters K (2000) The role of climatic mapping in predicting the potential geographical distribution of non-indigenous pests under current and future climates. Agr Ecosyst Environ 82:57–71
Butler GD Jr (1966) Development of the beet armyworm and its parasite Chelonus texanus in relation to temperature. J Econ Entomol 59:1324–1327
Carlson E (2010) Spodoptera exigua. Center for Invasive Species and Ecosystem Health. http://wiki.bugwood.org/Archive:GATop50/Spodoptera_exigua. Accessed 16 June 2016
Chamberlin TC (1965) The method of multiple working hypotheses. Science 148:754–759. https://doi.org/10.1126/science.148.3671.754
De Villiers M, Hattingh V, Kriticos D (2013) Combining field phenological observations with distribution data to model the potential distribution of the fruit fly Ceratitis rosa Karsch (Diptera: Tephritidae). Bull Ent Res 103:60–73
De Villiers M, Hattingh V, Kriticos DJ, Brunel S, Vayssières J-F, Sinzogan A, Billah M, Mohamed S, Mwatawala M, Abdelgader H (2016) The potential distribution of Bactrocera dorsalis: considering phenology and irrigation patterns. Bull Ent Res 106:19–33. https://doi.org/10.1017/S0007485315000693
Eghtedar E (1989) Some biological researches on beet army worm (Spodoptera exigua Hb) in Shiraz region [Iran]. Entomol Phytopathol Appl (Iran) 56:57–63
Elith J, Simpson J, Hirsch M, Burgman M (2013) Taxonomic uncertainty and decision making for biosecurity: spatial models for myrtle/guava rust. Australas Plant Pathol 42:43–51
El-Refai S, Degheele D (1988) Development time of the beet armyworm, Spodoptera exigua (Hübner) and the tobacco budworm, Heliothis virescens (F.) (Lepidoptera, Noctuidae) in function of temperature. Mededelingen van de Faculteit Landbouwwetenschappen Rijksuniversiteit Gent (Belgium)
Ezumah H, Knight A (1978) Some notes on the mealybug, Phenacoccus manihoti Mat. Ferr. incidence on manioc (Manihot esculenta) in Bas-Zaïre. In: Proceedings of the international workshop on the cassava mealybug, Phenacoccus manihoti Mat. Ferr, pp 26–29
FAO (2006) International standards for phytosanitary measures: 1 to 24. Secretariat of the International Plant Protection Convention, Rome
Farahani S, Talebi AA, Fathipour Y (2012) Life table of Spodoptera exigua (Lepidoptera: Noctuidae) on five soybean cultivars. Psyche (Camb Mass), p 7. https://doi.org/10.1155/2012/513824
Feng H-Q, Wu K-M, Cheng D-F, Guo Y-Y (2003) Radar observations of the autumn migration of the beet armyworm Spodoptera exigua (Lepidoptera: Noctuidae) and other moths in northern China. Bull Ent Res 93:115–124
French R (1969) Migration of Laphygma exigua Hübner (Lepidoptera: Noctuidae) to the British Isles in relation to large-scale weather systems. J Anim Ecol 38:199–210
Fye R (1978) Pupation preferences of bollworms, tobacco budworms, and beet armyworms and impact on mortality resulting from cultivation of irrigated cotton. J Econ Entomol 71:570–572
Fye R, Carranza R (1973) Cotton pests: overwintering of three lepidopterous species in Arizona. J Econ Entomol 66:657–660
GBIF Global Biodiversity Information Facility. Free and open access to biodiversity data. http://www.gbif.org/occurrence/search?TAXON_KEY=5109890. Accessed 6 Dec 2013
Greenberg S, Sappington T, Legaspi B, Liu T, Setamou M (2001) Feeding and life history of Spodoptera exigua (Lepidoptera: Noctuidae) on different host plants. Ann Entomol Soc Am 94:566–575
Guerra A, Ouye M (1968) Hatch, larval development, and adult longevity of four lepidopterous species after thermal treatment of eggs. J Econ Entomol 61:14–16
Hall M, Wall R (1995) Myiasis of humans and domestic animals. Adv Parasit 35:257–334
Han L, Zhai B, Zhang X (2002) Life table of the laboratory population of Spodoptera exigua (Hübner) at different temperatures. Acta Entomol Sin 46:184–189
Herren HR, Neuenschwander P (1991) Biological control of cassava pests in Africa. Annu Rev Entomol 36:257–283. https://doi.org/10.1146/annurev.en.36.010191.001353
Hogg DB, Gutierrez AP (1980) A model of the flight phenology of the beet armyworm (Lepidoptera: Noctuidae) in central California. Hilgardia 48:1–36
Hutchinson M, Xu T, Houlder D, Nix H, McMahon J (2009) ANUCLIM 6.0 user’s guide. Australian National University, Fenner School of Environment and Society, Canberra
Jiang X-F, Luo L-Z, Li K-B, Zhao T-C, Hu Y (2001) A study on the cold hardiness of the beet armyworm, Spodoptera exigua. Acta Ecol Sin 21:1576–1583
Jiang X, Zhai H, Wang L, Luo L, Sappington TW, Zhang L (2011) Cloning of the heat shock protein 90 and 70 genes from the beet armyworm, Spodoptera exigua, and expression characteristics in relation to thermal stress and development. Cell Stress Chaperon 17:67–80
Karimi-Malati A, Fathipour Y, Talebi A, Bazoubandi M (2012) Comparative life table parameters of beet armyworm, Spodoptera exigua (Lep.: Noctuidae), on four commercial sugar beet cultivars. J Entomol Soc Iran 32:109–124
Karimi-Malati A, Fathipour Y, Talebi AA (2014a) Development response of Spodoptera exigua to eight constant temperatures: linear and nonlinear modeling. J Asia Pac Entomol 17:349–354. https://doi.org/10.1016/j.aspen.2014.03.002
Karimi-Malati A, Fathipour Y, Talebi AA, Bazoubandi M (2014b) Life table parameters and survivorship of Spodoptera exigua (Lepidoptera: Noctuidae) at constant temperatures. Environ Entomol 43:795–803
Kim Y, Kim N (1997) Cold hardiness in Spodoptera exigua (Lepidoptera: Noctuidae). Environ Entomol 26:1117–1123
Kriticos DJ (2016) CLIMEX publications up until April 2015. CSIRO, Canberra, p 37
Kriticos DJ, Leriche A (2010) The effects of climate data precision on fitting and projecting species niche models. Ecography 33:115–127. https://doi.org/10.1111/j.1600-0587.2009.06042.x
Kriticos D, Sutherst R, Brown J, Adkins S, Maywald G (2003a) Climate change and biotic invasions: a case history of a tropical woody vine. Biol Invasions 5:147–165
Kriticos D, Sutherst R, Brown J, Adkins S, Maywald G (2003b) Climate change and the potential distribution of an invasive alien plant: Acacia nilotica ssp. indica in Australia. J Appl Ecol 40:111–124
Kriticos D, Yonow T, McFadyen R (2005) The potential distribution of Chromolaena odorata (Siam weed) in relation to climate. Weed Res 45:246–254
Kriticos DJ, Potter KJ, Alexander NS, Gibb AR, Suckling D (2007) Using a pheromone lure survey to establish the native and potential distribution of an invasive Lepidopteran, Uraba lugens. J Appl Ecol 44:853–863
Kriticos DJ, Webber BL, Leriche A, Ota N, Macadam I, Bathols J, Scott JK (2012) CliMond: global high-resolution historical and future scenario climate surfaces for bioclimatic modelling. Methods Ecol Evol 3:53–64
Kriticos DJ, Jarošik V, Ota N (2014) Extending the suite of bioclim variables: a proposed registry system and case study using principal components analysis. Methods Ecol Evol 5:956–960
Kriticos DJ, Maywald GF, Yonow T, Zurcher EJ, Herrmann NI, Sutherst RW (2015a) CLIMEX version 4: exploring the effects of climate on plants, animals and diseases. CSIRO, Canberra
Kriticos DJ, Ota N, Hutchison WD, Beddow J, Walsh T, Tay WT, Borchert DM, Paula-Moreas 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:e0119618
Kurdov M (1986) Prognosis of massive multiplication of the small ground moth Spodoptera exigua Hbn. (Laphygma exigua Hbn.) in Turkmenistan. (Prognoz massovogo razmnozheniya maloj nazemnoj sovki Spodoptera exigua (Laphygma exigua Hbn.) v Turkmenistane) Isvestiia Akademii Nauk Turkmenskoi SSR Seriia biologicheskikh nauk 1:25–28
Lawson BE, Day MD, Bowen M, van Klinken RD, Zalucki MP (2010) The effect of data sources and quality on the predictive capacity of CLIMEX models: an assessment of Teleonemia scrupulosa and Octotoma scabripennis for the biocontrol of Lantana camara in Australia. Biol Control 52:68–76
Lee S, Ahn S, Cho W, Choi K (1991) Effects of temperature on the development of beet armyworm, Spodoptera exigua Hübner (Lepidoptera: Noctuidae). Res Rep Rural Dev Adm (Crop Prot) 33:58–62
Mikkola K (1970) The interpretation of long-range migrations of Spodoptera exigua Hb. (Lepidoptera: Noctuidae). J Anim Ecol 39:593–598
Mitchell E (1979) Migration by Spodoptera exigua and S. frugiperda, North American style. In: Rabb R, Kennedy G (eds) Movement of highly mobile insects: concepts and methodology in research. North Carolina State University, Raleigh, pp 386–393
Portmann FT, Siebert S, Döll P (2010) MIRCA2000—global monthly irrigated and rainfed crop areas around the year 2000: a new high-resolution data set for agricultural and hydrological modeling. Glob Biogeochem Cycles 24:24. https://doi.org/10.1029/2008GB003435
Rodda GH, Jarnevich CS, Reed RN (2009) What parts of the US mainland are climatically suitable for invasive alien pythons spreading from Everglades National Park? Biol Invasions 11:241–252
Shelford VE (1963) The ecology of North America. University of Illinois Press, Urbana
Singh T (1982) The mealybug problem and its control. In: Root crops in Eastern Africa. Proceedings of a workshop held in Kigali, Rwanda, 23–27 November 1980. International Development Research Centre, Ottowa, pp 70–72
Sparks JA, Riley DG (2015) Beet armyworm. University of Georgia College of Agricultural and Environmental Sciences. http://www.ent.uga.edu/veg/solanaceous/beetarmyworm.htm. Accessed 16 June 2016
Sutherst RW (2003) Prediction of species geographical ranges. J Biogeogr 30:805–816
Sutherst RW (2014) Pest species distribution modelling: origins and lessons from history. Biol Invasions 16:239–256
Sutherst R, Bourne A (2009) Modelling non-equilibrium distributions of invasive species: a tale of two modelling paradigms. Biol Invasions 11:1231–1237
Sutherst RW, Maywald GF (1985) A computerised system for matching climates in ecology. Agr Ecosyst Environ 13:281–299
Trumble JT, Baker TC (1984) Flight phenology and pheromone trapping of Spodoptera exigua (Hübner) (Lepidoptera: Noctuidae) in southern coastal California. Environ Entomol 13:1278–1282
van der Ploeg RR, Kirkham M (1999) On the origin of the theory of mineral nutrition of plants and the law of the minimum. Soil Sci Soc Am J 63:1055–1062
Van Klinken RD, Lawson BE, Zalucki MP (2009) Predicting invasions in Australia by a Neotropical shrub under climate change: the challenge of novel climates and parameter estimation. Glob Ecol Biogeogr 18:688–700
Venette RC, Kriticos DJ, Magarey R, Koch F, Baker RHA, Worner S, Gómez Raboteaux NN, McKenney D, Dobesberger E, Yemshanov D, De Barro P, Hutchison WD, Fowler G, Kalaris T, Pedlar J (2010) Pest risk maps for invasive alien species: a roadmap for improvement. Bioscience 80:349–362
Webber BL, Yates CJ, Le Maitre DC, Scott JK, Kriticos DJ, Ota N, McNeill A, Le Roux JJ, Midgley GF (2011) Modelling horses for novel climate courses: insights from projecting potential distributions of native and alien Australian acacias with correlative and mechanistic models. Divers Distrib 17:978–1000
Weedon GP, Balsamo G, Bellouin N, Gomes S, Best MJ, Viterbo P (2014) The WFDEI meteorological forcing data set: WATCH forcing data methodology applied to ERA-interim reanalysis data. Water Resour Res 50:7505–7514
Wilson J (1932) Notes on the biology of Laphygma exigua Hübner. Fla Entomol 16:33–39
Xu J, Zhipeng H, Yueping Y, Xiong G (1998) The bionomics and control effects of chemical insecticides for Spodoptera exigua. J Fujian Agric Univ (Nat Sci) 1:73–77
Xu J, Xiong G, Zhipeng H, Yueping Y (1999) Effects of temperature on development of experimental beet armyworm population. Acta Phytophylacica Sin 26:20–24
Yonow T, Sutherst RW (1998) The geographical distribution of the Queensland fruit fly, Bactrocera (Dacus) tryoni, in relation to climate. Aust J Agric Res 49:935–953
Yonow T, Hattingh V, de Villiers M (2013) CLIMEX modelling of the potential global distribution of the citrus black spot disease caused by Guignardia citricarpa and the risk posed to Europe. Crop Prot 44:18–28
Yonow T, Kriticos DJ, Ota N, Van Den Berg J, Hutchison WD (2017) The potential global distribution of Chilo partellus, including consideration of irrigation and cropping patterns. J Pest Sci 90:459–477
Zheng X-L, Cong X-P, Wang X-P, Lei C-L (2011a) A review of geographic distribution, overwintering and migration in Spodoptera exigua Hübner (Lepidoptera: Noctuidae). J Ent Res Soc 13:39–48
Zheng X, Cheng W, Wang X, Lei C (2011b) Enhancement of supercooling capacity and survival by cold acclimation, rapid cold and heat hardening in Spodoptera exigua. Cryobiology 63:164–169
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
Zheng X-L, Wang P, Lei C-L, Lu W, Xian Z-H, Wang X-P (2013) Effect of soil moisture on overwintering pupae in Spodoptera exigua (Lepidoptera: Noctuidae). Appl Entomol Zool 48:365–371
Zhu G, Bu W, Gao Y, Liu G (2012) Potential geographic distribution of brown marmorated stink bug invasion (Halyomorpha halys). PLoS ONE 7:e31246
Acknowledgements
This work was led by InSTePP (International Science and Technology Practice and Policy), University of Minnesota, and CSIRO (Commonwealth Scientific and Industrial Research Organization, Australia), and was funded by the Bill and Melinda Gates Foundation by way of the HarvestChoice Project. Thanks are due to Philip Pardey and Jason Beddow for supporting the work, and to Matt Hill and Dean Paini for comments on the draft manuscript.
Funding
Work on this Project was funded by the Bill and Melinda Gates Foundation. Award No. 2010X446.UMN. Award title: HarvestChoice: Supporting Strategic Investment Choices in Agricultural Technology Development and Adoption.
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Yonow, T., Kriticos, D.J., Kirichenko, N. et al. Considering biology when inferring range-limiting stress mechanisms for agricultural pests: a case study of the beet armyworm. J Pest Sci 91, 523–538 (2018). https://doi.org/10.1007/s10340-017-0938-9
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DOI: https://doi.org/10.1007/s10340-017-0938-9