423
Views
6
CrossRef citations to date
0
Altmetric
Research Articles

Review of the biology and ecology of a ragweed leaf beetle, Ophraella communa (Coleoptera: Chrysomelidae), which is a biological control agent of an invasive common ragweed, Ambrosia artemisiifolia (Asterales: Asteraceae)

&
Pages 185-200 | Received 01 Jun 2018, Accepted 08 Oct 2018, Published online: 30 Oct 2018

References

  • Bassett, I. J., & Crompton, C. W. (1975). The biology of Canadian weeds.: 11. Ambrosia artemisiifolia L. and A. psilostachya DC. Canadian Journal of Plant Science, 55(2), 463–476. doi: 10.4141/cjps75-072
  • Bonini, M., Šikoparija, B., Prentović, M., Cislaghi, G., Colombo, P., Testoni, C., … Smith, M. (2015). Is the recent decrease in airborne Ambrosia pollen in the Milan area due to the accidental introduction of the ragweed leaf beetle Ophraella communa? Aerobiologia, 31(4), 499–513. doi: 10.1007/s10453-015-9380-8
  • Bonini, M., Šikoparija, B., Prentović, M., Cislaghi, G., Colombo, P., Testoni, C., … Smith, M. (2016). A follow-up study examining airborne Ambrosia pollen in the Milan area in 2014 in relation to the accidental introduction of the ragweed leaf beetle Ophraella communa. Aerobiologia, 32(2), 371–374. doi: 10.1007/s10453-015-9406-2
  • Bonini, M., Šikoparija, B., Skjøth, C. A., Cislaghi, G., Colombo, P., Testoni, C., & Smith, M. (2018). Ambrosia pollen source inventory for Italy: A multi-purpose tool to assess the impact of the ragweed leaf beetle (Ophraella communa LeSage) on populations of its host plant. International Journal of Biometeorology, 62(4), 597–608. doi: 10.1007/s00484-017-1469-z
  • Bosio, G., Massobrio, V., Chersi, C., Scavarda, G., & Clark, S. (2014). Spread of the ragweed leaf beetle, Ophraella communa LeSage, 1986 (Coleoptera Chrysomelidae), in Piedmont Region (northwestern Italy). Bollettino della Società Entomologica Italiana, 146(1), 17–30. doi: 10.4081/BollettinoSEI.2014.17
  • Bradshaw, C. J., Leroy, B., Bellard, C., Roiz, D., Albert, C., Fournier, A. … Courchamp, F. (2016). Massive yet grossly underestimated global costs of invasive insects. Nature Communications, 7, 12986. doi:10.1038/ncomms12986
  • Bullock, J., Chapman, D., Schaffer, S., Roy, D., Girardello, M., Haynes, T., … Tinch, R. (2012). Assessing and controlling the spread and the effects of common ragweed in Europe (ENV. B2/ETU/2010/0037). European Commission, Final Report.
  • Cao, Z., Wang, H., Meng, L., & Li, B. (2011). Risk to nontarget plants from Ophraella communa (Coleoptera: Chrysomelidae), a potential biological control agent of alien invasive weed Ambrosia artemisiifolia (Asteraceae) in China. Applied Entomology and Zoology, 46(3), 375–381. doi: 10.1007/s13355-011-0048-8
  • Cardarelli, E., Musacchio, A., Montagnani, C., Bogliani, G., Citterio, S., & Gentili, R. (2018). Ambrosia artemisiifolia control in agricultural areas: Effect of grassland seeding and herbivory by the exotic leaf beetle Ophraella communa. NeoBiota, 38, 1–22. doi: 10.3897/neobiota.38.23562
  • Chen, H. S., Zheng, X. W., Luo, M., Guo, J. Y., Luo, Y. H., Zhou, Z. S., & Wan, F. H. (2014). Effects of high temperature on body size and weight of Ophraella communa. Biocontrol Science and Technology, 24(8), 882–890. doi: 10.1080/09583157.2014.902426
  • Dernovici, S. (2003). Susceptibility of sunflower to Ophraella communa LeSage (Coleoptera: Chrysomelidae), a candidate for the biological control of common ragweed (Ambrosia artemisiifolia L.) (Doctoral dissertation). McGill University Libraries.
  • Dernovici, S. A., Teshler, M. P., & Watson, A. K. (2006). Is sunflower (Helianthus annuus) at risk to damage from Ophraella communa, a natural enemy of common ragweed (Ambrosia artemisiifolia)? Biocontrol Science and Technology, 16(7), 669–686. doi: 10.1080/09583150600699820
  • Emura, K. (1999). The ragweed beetle Ophraella communa LeSage (Coleoptera: Chrysomelidae) which injures harmful exotic plants. Plant Protect, 53, 138–141.
  • Emura, K. (2000). Recent topics and insect pest. Ragweed beetle, Ophraella communa. Agriculture and Horticulture, 75(1), 210–214.
  • Essl, F., Biró, K., Brandes, D., Broennimann, O., Bullock, J. M., Chapman, D. S., … Follak, S. (2015). Biological flora of the British Isles: Ambrosia artemisiifolia. Journal of Ecology, 103(4), 1069–1098. doi: 10.1111/1365-2745.12424
  • Fukano, Y., & Doi, H. (2013). Population abundance and host use pattern of Ophraella communa (Coleoptera: Chrysomelidae) in its native and introduced range. Biocontrol Science and Technology, 23(5), 595–601. doi: 10.1080/09583157.2013.775218
  • Fukano, Y., Doi, H., Thomas, C. E., Takata, M., Koyama, S., & Satoh, T. (2016). Contemporary evolution of host plant range expansion in an introduced herbivorous beetle Ophraella communa. Journal of Evolutionary Biology, 29(4), 757–765. doi: 10.1111/jeb.12824
  • Fukano, Y., Hirayama, H., & Tanaka, K. (2014). A herbivory-induced increase in the proportion of floating seeds in an invasive plant. Acta Oecologica, 56, 27–31. doi: 10.1016/j.actao.2014.02.001
  • Fukano, Y., Tanaka, K., & Yahara, T. (2013). Directional selection for early flowering is imposed by a re-associated herbivore-but no evidence of directional evolution. Basic and Applied Ecology, 14(5), 387–395. doi: 10.1016/j.baae.2013.05.009
  • Fukano, Y., & Yahara, T. (2012). Changes in defense of an alien plant Ambrosia artemisiifolia before and after the invasion of a native specialist enemy Ophraella communa. PloS one, 7(11), e49114. doi: 10.1371/journal.pone.0049114
  • Funk, D. J., Futuyma, D. J., Orti, G., & Meyer, A. (1995). A history of host associations and evolutionary diversification for Ophraella (Coleoptera: Chrysomelidae): New evidence from mitochondrial DNA. Evolution, 49(5), 1008–1017. doi: 10.1111/j.1558-5646.1995.tb02335.x
  • Futuyma, D. J. (1990). Observations on the taxonomy and natural history of Ophraella Wilcox (Coleoptera: Chrysomelidae), with a description of a new species. Journal of the New York Entomological Society, 98(2), 163–186.
  • Futuyma, D. J. (1991). A new species of Ophraella Wilcox (Coleoptera: Chrysomelidae) from the southeastern United States. Journal of the New York Entomological Society, 99(4), 643–653.
  • Futuyma, D. J., & McCafferty, S. S. (1990). Phylogeny and the evolution of host plant associations in the leaf beetle genus Ophraella (Coleoptera Chrysomelidae). Evolution, 44(8), 1885–1913. doi: 10.1111/j.1558-5646.1990.tb04298.x
  • Goeden, R. D., & Ricker, D. W. (1985). The life history of Ophraella notulata (F.) on western ragweed, Ambrosia psilostachya De Candolle, in southern California (Coleoptera: Chrysomelidae). Pan-Pacific Entomologist, 61(1), 32–37.
  • Guo, J. Y., Zhou, Z. S., Zheng, X. W., Chen, H. S., Wan, F. H., & Luo, Y. H. (2011). Control efficiency of leaf beetle, Ophraella communa, on the invasive common ragweed, Ambrosia artemisiifolia, at different growing stages. Biocontrol Science and Technology, 21(9), 1049–1063. doi: 10.1080/09583157.2011.603823
  • Hager, A., & Renner, K. (1994). Common ragweed (Ambrosia artemisiifolia) control in soybean (Glycine max) with bentazon as influenced by imazethapyr or thifensulfuron tank-mixes. Weed Technology, 8(4), 766–771. doi: 10.1017/S0890037X00028669
  • Hamaoui-Laguel, L., Vautard, R., Liu, L., Solmon, F., Viovy, N., Khvorostyanov, D. … Epstein, M. M. (2015). Effects of climate change and seed dispersal on airborne ragweed pollen loads in Europe. Nature Climate Change, 5(8), 766–771. doi: 10.1038/nclimate2652
  • Hilgendorf, J. H., & Goeden, R. D. (1981). Phytophagous insects reported from cultivated and weedy varieties of the sunflower, Helianthus annuus L., in North America. Bulletin of the ESA, 27(2), 102–109.
  • Igrc, J., DeLoach, C. J., & Zlof, V. (1995). Release and establishment of Zygogramma suturalis F (Coleoptera: Chrysomelidae) in Croatia for control of common ragweed (Ambrosia artemisiifolia L.). Biological Control, 5(2), 203–208. doi: 10.1006/bcon.1995.1025
  • Julien, M. H., & Griffiths, M. W. (1998). Biological control of weeds – A catalogue of agents and their target weeds (4th ed). Wallingford, NY: CABI.
  • Katz, D. S., & Carey, T. S. (2014). Heterogeneity in ragweed pollen exposure is determined by plant composition at small spatial scales. Science of the Total Environment, 485–486, 435–440. doi: 10.1016/j.scitotenv.2014.03.099
  • Kim, J.-W., Lee, I.-Y., & Lee, J. (2017). Distribution of invasive alien species in Korean croplands. Weed&Turfgrass Science, 6(2), 117–123.
  • Kim, S., Lee, J. K., Song, Y. J., Kang, S. C., Kim, B., Choi, I. J., & Lee, D. H. (2018). Evaluating natural compounds as potential insecticides against three economically important pests, Bemisia tabaci (Hemiptera: Aleyrodidae), Frankliniella occidentalis (Thysanoptera: Thripidae), and Myzus persicae (Hemiptera: Aphididae), on greenhouse sweet peppers. Applied Biological Chemistry, 61, 313–323. doi: 10.1007/s13765-018-0362-8
  • Kim, D.-S., Oh, K.-S., Lee, Y.-D., Lee, S.-Y., Lee, H., Kim, H.-J., & Kim, D.-E. (2017). The distribution of the exotic species, Ophraella communa LeSage (Coleoptera, Chrysomelidae) and their applicability for biological control against ragweed Ambrosia artemisiifolia L. on Jeju island. Environmental Biology Research, 35(4), 437–445. doi: 10.11626/KJEB.2017.35.4.437
  • Komives, T., Béres, I., Reisinger, P., Lehoczky, E., Berke, J., Tamás, J., … Mikulás, J. (2006). New strategy of the integrated protection against common ragweed (Ambrosia artemisiifolia L. Hungarian Weed Research and Technology, 6, 5–50.
  • Kong, L., Zhou, Z., Yue, L., Liu, Z., Wan, F., & Guo, J. (2016). Effect of daily temperatural fluctuation on population fitness of Ophraella communa in early spring in Langfang, Heibei Province. Acta Ecologica Sinica, 36(2), 57–61. doi: 10.1016/j.chnaes.2016.01.001
  • Kwon, Y. J., Seo, S. J., & Kim, J. A. (2001). A serviced report for planning and designing Taegu Eco-park, section insects. Research Service Entrusted From KIEM, Keimyung University, Daegu. (In Korean).
  • Lee, I. Y., Park, J. Y., Oh, S. M., Park, J. E., & Kwon, O. S. (2007). Selection of insects for potential biological control of Ambrosia trifida. Korean Journal of Weed Science, 27(4), 309–317.
  • LeSage, L. (1986). A taxonomic monograph of the Nearctic galerucine genus Ophraella Wilcox (Coleoptera: Chrysomelidae). Memoirs of the Entomological Society of Canada, 118(S133), 3–75. doi: 10.4039/entm118133fv
  • Lommen, S. T., Ciappetta, S., Ghiani, A., Asero, R., Gentili, R., Müller-Schärer, H., & Citterio, S. (2017). Defoliation of common ragweed by Ophraella communa beetle does not affect pollen allergenicity in controlled conditions. Plant Biosystems-An International Journal Dealing with all Aspects of Plant Biology, 151(6), 1094–1100. doi: 10.1080/11263504.2016.1244122
  • Lommen, S. T., Jolidon, E. F., Sun, Y., Eduardo, J. I. B., & Müller-Schärer, H. (2017). An early suitability assessment of two exotic Ophraella species (Coleoptera: Chrysomelidae) for biological control of invasive ragweed in Europe. European Journal of Entomology, 114, 160–169. doi: 10.14411/eje.2017.021
  • Makra, L., Matyasovszky, I., Hufnagel, L., & Tusnady, G. (2015). The history of ragweed in the world. Applied Ecology and Environmental Research, 13(2), 489–512.
  • Meng, L., & Li, B. P. (2005). Advances on biology and host specificity of the newly introduced beetle, Ophraella communa LeSage (Coleoptera: Chrysomelidae), attacking Ambrosia artemisiifolia (Compositae) in continent of China. Chinese Journal of Biological Control, 21(2), 65–69.
  • Miyatake, T., & Ohno, T. (2010). Seasonal abundance of exotic leaf beetle Orphraella communa LeSage (Coleoptera: Chrysomelidae) on two different host plants. Applied Entomology and Zoology, 45(2), 283–288. doi: 10.1303/aez.2010.283
  • Montagnani, C., Gentili, R., Smith, M., Guarino, M. F., & Citterio, S. (2017). The Worldwide Spread, Success, and Impact of Ragweed (Ambrosia spp.). Critical Reviews in Plant Sciences, 36(3), 139–178. doi: 10.1080/07352689.2017.1360112
  • Moriya, S. (1999). Successive rearing of ragweed beetle, Ophraella communa LeSage (Coleoptera: Chrysomelidae) in Japan. Annual Report of the Kanto-Tosan Plant Protection Society, 46, 115–117.
  • Moriya, S., & Shiyake, S. (2001). Spreading the distribution of an exotic ragweed beetle, Ophraella communa LeSage (Coleoptera: Chrysomelidae), in Japan. Japanese Journal of Entomology (New Series), 4(3), 99–102.
  • Moriya, S., Tanaka, K., Yamamura, K., Shimizu, T., & Shiyake, S. (2002). Expansion of the distribution range of the ragweed beetle, Ophraella communa LeSage, (Coleoptera: Chrysomelidae) and its natural enemies in Japan. Annual Report of the Kanto-Tosan Plant Protection Society, 49, 131–133.
  • Müller-Schärer, H., Lommen, S. T., Rossinelli, M., Bonini, M., Boriani, M., Bosio, G., & Schaffner, U. (2014). Ophraella communa, the ragweed leaf beetle, has successfully landed in Europe: Fortunate coincidence or threat? Weed Research, 54(2), 109–119. doi: 10.1111/wre.12072
  • Palmer, W. A., & Goeden, R. D. (1991). The host range of Ophraella communa LeSage (Coleoptera: Chrysomelidae). The Coleopterists’ Bulletin, 45(2), 115–120.
  • Pimentel, D., Zuniga, R., & Morrison, D. (2005). Update on the environmental and economic costs associated with alien-invasive species in the United States. Ecological Economics, 52(3), 273–288. doi: 10.1016/j.ecolecon.2004.10.002
  • Reinhardt, F., Herle, M., Bastiansen, F., & Streit, B. (2003). Economic impact of the spread of alien species in Germany. Berlin, Germany: Federal Environmental Agency (Umweltbundesamt).
  • Rich, T. C. G. (1994). Ragweeds (Ambrosia L.) in Britain. Grana, 33(1), 38–43. doi: 10.1080/00173139409427454
  • Sheppard, A. W., Shaw, R. H., & Sforza, R. (2006). Top 20 environmental weeds for classical biological control in Europe: A review of opportunities, regulations and other barriers to adoption. Weed Research, 46(2), 93–117. doi: 10.1111/j.1365-3180.2006.00497.x
  • Smith, M., Cecchi, L., Skjøth, C. A., Karrer, G., & Šikoparija, B. (2013). Common ragweed: A threat to environmental health in Europe. Environment International, 61, 115–126. doi: 10.1016/j.envint.2013.08.005
  • Sohn, J. C., An, S. L., Lee, J. E., & Park, K. T. (2002). Notes on exotic species, Ophraella communa LeSage (Coleoptera: Chrysomelidae) in Korea. Korean Journal of Applied Entomology, 41(2), 145–150.
  • Sun, Y., Brönnimann, O., Roderick, G. K., Poltavsky, A., Lommen, S. T., & Müller-Schärer, H. (2017). Climatic suitability ranking of biological control candidates: A biogeographic approach for ragweed management in Europe. Ecosphere, 8(4), e01731. doi:10.1002/ecs2.1731
  • Takizawa, H., Saito, A., Hirano, Y., & Ohno, M. (1999). Invading insect, Ophraella communa LeSage, 1986-range extension and life history in Kanto district, Japan. Gek-kan-mushi, 338, 26–31.
  • Tamura, Y., Hattori, M., Konno, K., Kono, Y., Honda, H., Ono, H., & Yoshida, M. (2004). Triterpenoid and caffeic acid derivatives in the leaves of ragweed, Ambrosia artemisiifolia L. (Asterales: Asteraceae), as feeding stimulants of Ophraella communa LeSage (Coleoptera: Chrysomelidae). Chemoecology, 14(2), 113–118. doi: 10.1007/s00049-004-0269-1
  • Tanaka, K., & Murata, K. (2016). Rapid evolution of photoperiodic response in a recently introduced insect Ophraella communa along geographic gradients. Entomological Science, 19(3), 207–214. doi: 10.1111/ens.12200
  • Tanaka, K., & Yamanaka, T. (2009). Factors affecting flight activity of Ophraella communa (Coleoptera: Chrysomelidae), an exotic insect in Japan. Environmental Entomology, 38(1), 235–241. doi: 10.1603/022.038.0129
  • Teshler, M. P., Dernovici, S. A., DiTommaso, A., Coderre, D., & Watson, A. K. (2004). A novel device for the collection, storage, transport, and delivery of beneficial insects, and its application to Ophraella communa (Coleoptera: Chrysomelidae). Biocontrol Science and Technology, 14(4), 347–357. doi: 10.1080/09583150410001665204
  • Wan, F. H., Liu, W. X., Ma, J., & Guo, J. Y. (2005). Ambrosia artemisiifolia and A. Trifida. In F. H. Wan, X. B. Zheng, & J. Y. Guo (Eds.), Biology and management of invasive alien species in agriculture and forestry (pp. 662–688). Beijing: Science Press.
  • Wang, C., & Chiang, M. (1998). New record of a fastidious chrysomelid, Ophraella communa LeSage (Coleoptera: Chrysomelidae), in Taiwan. Plant Protection Bulletin (Taipei), 40(2), 185–188.
  • Watanabe, M. (2000). Photoperiodic control of development and reproductive diapause in the leaf beetle Ophraella communa LeSage. Entomological Science, 3(2), 245–253.
  • Watanabe, M., & Hirai, Y. (2004). Host-use pattern of the ragweed beetle Ophraella communa LeSage (Coleoptera: Chrysomelidae) for overwintering and reproduction in Tsukuba. Applied Entomology and Zoology, 39(2), 249–254. doi: 10.1303/aez.2004.249
  • Welch, K. A. (1978). Biology of Ophraella notulata (Coleoptera: Chrysomelidae). Annals of the Entomological Society of America, 71(1), 134–136. doi: 10.1093/aesa/71.1.134
  • Wilcox, J. A. (1965). Synopsis of the North American Galerucinae (Coleoptera: Chrysomelidae).
  • Yamamura, K., Moriya, S., Tanaka, K., & Shimizu, T. (2007). Estimation of the potential speed of range expansion of an introduced species: characteristics and applicability of the gamma model. Population Ecology, 49(1), 51–62. doi: 10.1007/s10144-006-0001-9
  • Yamanaka, T., Tanaka, K., Otuka, A., & Bjørnstad, O. N. (2007). Detecting spatial interactions in the ragweed (Ambrosia artemissifolia L.) and the ragweed beetle (Ophraella communa LeSage) populations. Ecological Research, 22(2), 185–196. doi: 10.1007/s11284-006-0300-9
  • Zhang, L., Yang, X., Li, W., & Cui, J. (2005). A new record of Ophraella communa of mainland China. Chinese Bulletin of Entomology, 42(2), 227–228.
  • Zhao, C. C., Zheng, H. Y., Ma, C., Guo, J. Y., Wan, F. H., & Zhou, Z. S. (2017). Effects of age at mating of both sexes on female longevity and fecundity performance in Ophraella communa LeSage (Coleoptera: Chrysomelidae). Biocontrol Science and Technology, 27(10), 1145–1152. doi: 10.1080/09583157.2017.1387232
  • Zhou, Z. S., Chen, H. S., Zheng, X. W., Guo, J. Y., Guo, W., Li, M., … Wan, F. H. (2014). Control of the invasive weed Ambrosia artemisiifolia with Ophraella communa and Epiblema strenuana. Biocontrol Science and Technology, 24(8), 950–964. doi: 10.1080/09583157.2014.897305
  • Zhou, Z. S., Guo, J. Y., Chen, H. S., & Wan, F. H. (2010a). Effect of humidity on the development and fecundity of Ophraella communa (Coleoptera: Chrysomelidae). BioControl, 55(2), 313–319. doi: 10.1007/s10526-009-9242-9
  • Zhou, Z. S., Guo, J. Y., Chen, H. S., & Wan, F. H. (2010b). Effects of temperature on survival, development, longevity, and fecundity of Ophraella communa (Coleoptera: Chrysomelidae), a potential biological control agent against Ambrosia artemisiifolia (Asterales: Asteraceae). Environmental Entomology, 39(3), 1021–1027. doi: 10.1603/EN09176
  • Zhou, Z. S., Guo, J. Y., Guo, W., & Wan, F. H. (2011). Synergistic effects of olfactory and tactile cues in short-range mate finding of Ophraella communa. Entomologia Experimentalis et Applicata, 138(1), 48–54. doi: 10.1111/j.1570-7458.2010.01074.x
  • Zhou, Z. S., Guo, J. Y., Guo, W., Zheng, H. Y., & Wan, F. H. (2012). Effects of morphological traits, age and copulation experience on mate choice in Ophraella communa. Biocontrol Science and Technology, 22(1), 81–91. doi: 10.1080/09583157.2011.643225
  • Zhou, Z. S., Guo, J. Y., Li, M., Ai, H. M., & Wan, F. H. (2011). Seasonal changes in cold hardiness of Ophraella communa. Entomologia Experimentalis et Applicata, 140(1), 85–90. doi: 10.1111/j.1570-7458.2011.01128.x
  • Zhou, Z. S., Guo, J. Y., & Wan, F. H. (2009). Biological control of Ambrosia artemisiifolia with Epibleme strenuana and Ophraella communa. In F. H. Wan, J. Y. Guo, & F. Zhang (Eds.), Research on Biological Invasions in China (pp. 246–251). Beijing, People’s Republic of China: Science Press.
  • Zhou, Z. S., Guo, J. Y., Zheng, X. W., Luo, M., Chen, H. S., & Wan, F. H. (2011). Reevaluation of biosecurity of Ophraella communa against sunflower (Helianthus annuus). Biocontrol Science and Technology, 21(10), 1147–1160. doi: 10.1080/09583157.2011.606559
  • Zhou, Z. S., Luo, M., Guo, J. Y., Chen, H. S., & Wan, F. H. (2014). Effect of photoperiod on developmental fitness in Ophraella communa (Coleoptera: Chrysomelidae). Journal of Economic Entomology, 43(5), 1435–1442.
  • Zhou, Z. S., Luo, M., Guo, J. Y., Chen, H. S., & Wan, F. H. (2014). Food deprivation-dependent development and fecundity in Ophraella communa. Biocontrol Science and Technology, 24(11), 1217–1226. doi: 10.1080/09583157.2014.931352
  • Zhou, Z. S., Rasmann, S., Zheng, H. Y., Watson, A., Guo, J. Y., Wang, J. G., & Wan, F. H. (2015). Mating frequency positively associates with fitness in Ophraella communa. Ecological Entomology, 40(3), 292–298. doi: 10.1111/een.12184
  • Zhu, D. H., Zhu, J., Peng, Z. P., & Wan, F. H. (2012). Effects of photoperiod and temperature on reproductive diapause in Ophraella communa (Coleoptera: Chrysomelidae), a potential biocontrol agent against Ambrosia artemisiifolia. Insect Science, 19(3), 286–294. doi: 10.1111/j.1744-7917.2011.01455.x

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.