Hostname: page-component-76d6cb85b7-s74w7 Total loading time: 0 Render date: 2026-07-21T21:41:19.646Z Has data issue: false hasContentIssue false
  • English
  • Français

Competitive displacement between two invasive whiteflies: insecticide application and host plant effects

Published online by Cambridge University Press:  05 March 2013

Di-Bing Sun ,
Yin-Quan Liu ,
Li Qin ,
Jing Xu ,
Fang-Fang Li  and
Shu-Sheng Liu
Di-Bing Sun
Affiliation:
Ministry of Agriculture Key Laboratory of Agricultural Entomology, Institute of Insect Sciences, Zhejiang University, 866 Yuhangtang Road, Hangzhou 310058, People's Republic of China
Yin-Quan Liu
Affiliation:
Ministry of Agriculture Key Laboratory of Agricultural Entomology, Institute of Insect Sciences, Zhejiang University, 866 Yuhangtang Road, Hangzhou 310058, People's Republic of China
Li Qin
Affiliation:
Ministry of Agriculture Key Laboratory of Agricultural Entomology, Institute of Insect Sciences, Zhejiang University, 866 Yuhangtang Road, Hangzhou 310058, People's Republic of China
Jing Xu
Affiliation:
Ministry of Agriculture Key Laboratory of Agricultural Entomology, Institute of Insect Sciences, Zhejiang University, 866 Yuhangtang Road, Hangzhou 310058, People's Republic of China
Fang-Fang Li
Affiliation:
Ministry of Agriculture Key Laboratory of Agricultural Entomology, Institute of Insect Sciences, Zhejiang University, 866 Yuhangtang Road, Hangzhou 310058, People's Republic of China
Shu-Sheng Liu*
Affiliation:
Ministry of Agriculture Key Laboratory of Agricultural Entomology, Institute of Insect Sciences, Zhejiang University, 866 Yuhangtang Road, Hangzhou 310058, People's Republic of China
*
* Author for correspondence Phone: +86 571 88982505 Fax: +86 571 88982355 E-mail: shshliu@zju.edu.cn
Get access Rights & Permissions [Opens in a new window]

Abstract

The cryptic species Middle East-Asia Minor 1 (MEAM1), formerly referred to as ‘B biotype’, of the whitefly Bemisia tabaci complex entered China in the mid 1990s, and the Mediterranean (MED) cryptic species, formerly referred to as ‘Q biotype’, of the same whitefly complex entered China around 2003. Field surveys in China after 2003 indicate that in many regions MED has been replacing the earlier invader MEAM1. The factors underlying this displacement are unclear. We conducted laboratory experiments and field sampling to examine the effects of insecticide application on the competitive interactions between MEAM1 and MED. In the laboratory, on cotton, a plant showing similar levels of suitability to both whitefly species, MEAM1 displaced MED in five generations when initial populations of the two species were equal and no insecticide was applied. In contrast, MED displaced MEAM1 in seven and two generations, respectively, when 12.5 and 50.0 mg l−1 imidacloprid was applied to the plants via soil drench. Field sampling indicated that in a single season MED displaced MEAM1 on crops heavily sprayed with neonicotinoid insecticides but the relative abundance of the two species changed little on crops without insecticide spray. We also examined the effects of host plants on the competitive interactions between the two species in the laboratory. When cohorts with equal abundance of MEAM1 and MED were set up on different host plants, MEAM1 displaced MED on cabbage and tomato in five and seven generations, respectively, but MED displaced MEAM1 on pepper in two generations. As field populations of MED have lower susceptibility than those of MEAM1 to nearly all commonly used insecticides including imidacloprid, insecticide application seems to have played a major role in shifting the species competitive interaction effects in favour of MED in the field across China. Host plants may also shape competition between the two species depending on the relative levels of plant suitability.

Keywords

whiteflycryptic speciesspecies exclusioninsecticide susceptibilityhost plant

Information

Type
Research Paper
Information
Bulletin of Entomological Research , Volume 103 , Issue 3 , June 2013 , pp. 344 - 353
Copyright
Copyright © Cambridge University Press 2013

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Article purchase

Temporarily unavailable

References

Amarasekare, P. (2003) Competitive coexistence in spatially structured environments: a synthesis. Ecology Letters 6, 1109–1122.Google Scholar
Chu, D., Zhang, Y.J., Cong, B., Xu, B.Y. & Wu, Q.J. (2005) Identification for Yunnan Q biotype Bemisia tabaci population. Chinese Bulletin of Entomology 42, 54–56 (in Chinese with English summary).Google Scholar
Chu, D., Wan, F.H., Zhang, Y.J. & Brown, J.K. (2010) Change in the biotype composition of Bemisia tabaci in Shandong province of China from 2005 to 2008. Environmental Entomology 39, 1028–1036.Google Scholar
Chu, D., Hu, X.S., Gao, C.S., Zhao, H.Y., Nichols, R.L. & Li, X.C. (2012a) Use of mitochondrial cytochrome oxidase I polymerase chain reaction–restriction fragment length polymorphism for identifying subclades of Bemisia tabaci Mediterranean group. Journal of Economic Entomology 105, 242–251.CrossRefGoogle ScholarPubMed
Chu, D., Tao, Y.L. & Chi, H. (2012b) Influence of plant combinations on population characteristics of Bemisia tabaci biotypes B and Q. Journal of Economic Entomology 105, 930–935.Google Scholar
Crowder, D.W., Horowitz, A.R., De Berro, P.J., Liu, S.S., Showalter, A.M., Kontsedalov, S., Khasdan, V., Shargal, A., Liu, J. & Carrière, Y. (2010a) Mating behaviour, life history and adaptation to insecticides determine species exclusion between whiteflies. Journal of Animal Ecology 79, 563–570.Google Scholar
Crowder, D.W., Sitvarin, M.I. & Carrière, Y. (2010b) Plasticity in mating behaviour drives asymmetric reproductive interference in whiteflies. Animal Behaviour 79, 579–586.Google Scholar
Crowder, D.W., Horowitz, A.R., Breslauer, H., Rippa, M., Kontsedalov, S., Ghanim, M. & Carrière, Y. (2011) Niche partitioning and stochastic processes shape community structure following whitefly invasions. Basic and Applied Ecology 12, 685–694.Google Scholar
De Barro, P.J. & Ahmed, M.Z. (2011) Genetic networking of the Bemisia tabaci cryptic species complex reveals pattern of biological invasions. PLoS ONE 6, e25579.Google Scholar
De Barro, P.J. & Driver, F. (1997) Use of RAPD PCR to distinguish the B biotype from other biotypes of Bemisia tabaci (Gennadius) (Hemiptera: Aleyrodidae). Australian Journal of Entomology 36, 149–152.Google Scholar
De Barro, P.J., Liu, S.S., Boykin, L.M. & Dinsdale, A. (2011) Bemisia tabaci: a statement of species status. Annual Review of Entomology 56, 1–19.Google Scholar
Dinsdale, A., Cook, L., Riginos, C., Buckley, Y.M. & De Barro, P.J. (2010) Refined global analysis of Bemisia tabaci (Gennadius) (Hemiptera: Sternorrhyncha: Aleyrodoidae: Aleyrodidea) mitochondrial cytochrome oxidase 1 to identify species level genetic boundaries. Annals of the Entomological Society of America 103, 196–208.CrossRefGoogle Scholar
Gao, Y.L., Reitz, S.R., Wei, Q.B., Yu, W.Y. & Lei, Z.R. (2012) Insecticide-mediated apparent displacement between two invasive species of leafminer fly. PLoS ONE 7, e36622.Google Scholar
Guo, X.J., Rao, Q., Luo, C., Zhang, H.Y. & Gao, X.W. (2012) Diversity and genetic differentiation of the whitefly Bemisia tabaci species complex in China based on mtDNA CO1 and cDNA-AFLP analysis. Journal of Integrative Agriculture 11, 206–214.Google Scholar
Horowitz, A.R., Gorman, K., Ross, G. & Denholm, I. (2003) Inheritance of pyriproxyfen resistance in the whitefly, Bemisia tabaci (Q biotype). Achieves of Insect Biochemistry and Physiology 54, 177–186.Google Scholar
Horowitz, A.R., Kontsedalov, S., Khasdan, V. & Ishaaya, I. (2005) Biotypes B and Q of Bemisia tabaci and their relevance to neonicotinoid and pyriproxyfen resistance. Achieves of Insect Biochemistry and Physiology 58, 216–225.Google Scholar
Hu, J., De Barro, P., Zhao, H., Wang, J., Nardi, F. & Liu, S.S. (2011a) An extensive field survey combined with phylogenetic analysis reveals rapid and widespread invasion of two alien whiteflies in China. PLoS ONE 6, e16061.Google Scholar
Hu, X.S., Dennehy, T.J., Ni, X.Z., Zhao, H.Y., Nichols, R.L. & Li, X.C. (2011b) Potential adaptation of Q biotype whitefly populations from poinsettia to field crops. Insect Science 18, 719–728.CrossRefGoogle Scholar
Iida, H., Kitamura, T. & Honda, K.I. (2009) Comparison of egg-hatching rate, survival rate and development time of the immature stage between B- and Q-biotypes of Bemisia tabaci (Gennadius) (Homoptera: Aleyrodidae) on various agricultural crops. Applied Entomology and Zoology 44, 267–273.Google Scholar
Khasdan, V., Levin, I., Rosner, A., Morin, S., Kontsedalov, S., Maslenin, L. & Horowitz, A.R. (2005) DNA markers for identifying biotypes B and Q of Bemisia tabaci (Hemiptera: Aleyrodidae) and studying population dynamics. Bulletin of Entomological Research 95, 605–613.Google Scholar
Liu, B.M., Yan, F.M., Chu, D., Pan, H.P., Jiao, X.G., Xie, W., Wu, Q.J., Wang, S.L., Xu, B.Y., Zhou, X.G. & Zhang, Y.J. (2012a) Differences in feeding behaviors of two invasive whiteflies on plants with differential suitability: implication for competitive displacement. International Journal of Biological Sciences 8, 697–706.Google Scholar
Liu, S.S., De Barro, P.J., Xu, J., Luan, J.B., Zang, L.S., Ruan, Y.M. & Wan, F.H. (2007) Asymmetric mating interactions drive widespread invasion and displacement in a whitefly. Science 318, 1769–1772.Google Scholar
Liu, S.S., Colvin, J. & De Barro, P.J. (2012b) Species concepts as applied to the whitefly Bemisia tabaci systematics: how many species are there? Journal of Integrative Agriculture 11, 176–186.CrossRefGoogle Scholar
Luan, J.B., Ruan, Y.M., Zang, L. &. Liu, S.S. (2008) Pre-copulation intervals, copulation frequencies, and initial progeny sex ratios in two biotypes of whitefly, Bemisia tabaci . Entomologia Experimentalis et Applicata 129, 316–324.Google Scholar
Luan, J.B., Xu, J., Lin, K.K., Zalucki, M.P. & Liu, S.S. (2012) Species exclusion between an invasive and an indigenous whitefly on host plants with differential levels of suitability. Journal of Integrative Agriculture 11, 215–224.Google Scholar
Luo, C., Yao, Y., Wang, R.J., Yan, F.M., Hu, D.X. & Zang, Z.L. (2002) The use of mitochondrial cytochrome oxidase I (mtCOI) gene sequences for the identification of biotype of Bemisia tabaci (Gennadius) in China. Acta Entomologica Sinica 45, 759–763 (in Chinese with English summary).Google Scholar
Luo, C., Jones, C.M., Devone, G., Zhang, F., Denholm, I. & Gorman, K. (2010) Insecticide-resistance in Bemisia tabaci biotype-Q from China. Crop Protection 29, 429–434.Google Scholar
McKenzie, C.L., Bethke, J.A., Byrne, F.J., Chamberlin, J.R., Dennehy, T.J., Dickey, A.M., Gilrein, D., Hall, P.M., Ludwig, S., Oetting, R.D., Osborne, L.S., Schmale, L. & Shatters, R.G. Jr. (2012) Distribution of Bemisia tabaci (Hemiptera: Aleyrodidae) biotypes in North America after the Q invasion. Journal of Economic Entomology 105, 753–766.Google Scholar
Moya, A., Guirao, P., Cifuentes, D., Beitia, F. & Cenis, J.L. (2001) Genetic diversity of Iberian populations of Bemisia tabaci (Hemiptera: Aleyrodidae) based on random amplified polymorphic DNA-polymerase chain reaction. Molecular Ecology 10, 891–897.CrossRefGoogle ScholarPubMed
Muniz, M., Nombela, G. & Barrios, L. (2002) Within-plant distribution and infestation pattern of the B- and Q-biotypes of the whitely, Bemisia tabaci, on tomato and pepper. Entomologia Experimentalis et Applicata 104, 369–373.Google Scholar
Naranjo, S.E., Castle, S.J., De Barro, P.J. & Liu, S.S. (2010) Population dynamics demography, dispersal and spread of Bemisia tabaci . pp. 185–226 in Stansly, P.A. & Naranjo, S.E. (Eds) Bemisia: Bionomics and Management of a Global Pest. Springer, Dordrecht.Google Scholar
Pan, H.P., Chu, D., Ge, D.Q., Wang, S.L., Wu, Q.J., Xie, W., Jiao, X.G., Liu, B.M., Yang, X., Yang, N., Su, Q., Xu, B.Y. & Zhang, Y.J. (2011) Further spread of and domination by Bemisia tabaci (Hemiptera: Aleyrodidae) biotype Q on field crops in China. Journal of Economic Entomology 104, 978–985.Google Scholar
Papayiannis, L.C., Brown, J.K., , Seraphides, N.A., Hadjistylli, M., Ioannou, N. & Katis, N.I. (2009) A real-time PCR assay to differentiate the B and Q biotypes of the Bemisia tabaci complex in Cyprus. Bulletin of Entomological Research 99, 573–582.Google Scholar
Pascual, S. (2006) Mechanisms in competition, under laboratory conditions, between Spanish biotypes B and Q of Bemisia tabaci Gennadius. Spanish Journal of Agricultural Research 44, 351–354.Google Scholar
Pascual, S. & Callejas, C. (2004) Intra- and interspecific competition between biotypes B and Q of Bemisia tabaci (Hemiptera: Aleyrodidae) from Spain. Bulletin of Entomological Research 94, 369–375.Google Scholar
Rao, Q., Luo, C., Zhang, H.Y., Guo, X.J. & Devine, J.G. (2011) Distribution and dynamics of Bemisia tabaci invasive biotypes in central China. Bulletin of Entomological Research 101, 81–88.Google Scholar
Rao, Q., Xu, Y.H., Luo, C., Zhang, H.Y., Jones, C.M., Devine, G.J., Gorman, K. & Denholm, I. (2012) Characterisation of neonicotinoid and pymetrozine resistance in strains of Bemisia tabaci (Hemiptera: Aleyrodidae) from China. Journal of Integrative Agriculture 11, 321–326.Google Scholar
Reitz, S.R. & Trumble, J.T. (2002) Competitive displacement among insects and arachnids. Annual Review of Entomology 47, 435–65.Google Scholar
Saleh, D., Laarif, A., Clouet, C. & Gauthier, N. (2012) Spatial and host-plant partitioning between coexisting Bemisia tabaci cryptic species in Tunisia. Population Ecology 54, 261–274.Google Scholar
Shen, Y., Du, Y.Z., Ren, S.X. & Qiu, B.L. (2011) Preliminary study of succession of Bemisia tabaci biotypes in Jiangsu Province, China. Chinese Journal of Applied Entomology 48, 16–21 (in Chinese with English summary).Google Scholar
Simon, B., Cenis, J.L. & De La Rúa, P. (2007) Distribution patterns of the Q and B biotypes of Bemisia tabaci in the Mediterranean Basin based on microsatellite variation. Entomologia Experimentalis et Applicata 124, 327–336.Google Scholar
Sun, D.B. (2011) Behavioural mechanisms underlying the competitive displacement between two invasive cryptic species of the whitefly Bemisia tabaci . MSc Thesis, Zhejiang University, China.Google Scholar
Sun, D.B., Xu, J., Luan, J.B. & Liu, S.S. (2011) Reproductive incompatibility between the B and Q biotypes of the whitefly Bemisia tabaci in China: genetic and behavioural evidence. Bulletin of Entomological Research 101, 211–220.Google Scholar
Tsueda, H. & Tsuchida, K. (2011) Reproductive differences between Q and B whiteflies, Bemisia tabaci, on three host plants and negative interactions in mixed cohorts. Entomologia Experimentalis et Applicata 141, 197–207.Google Scholar
Vassiliou, V.A., Jagge, C., Grispou, M., Pietrantonio, P.V. & Tsagkarakou, A. (2008) Biotype status of Bemisia tabaci from various crops in Cyprus. Phytoparasitica 36, 400–404.CrossRefGoogle Scholar
Wang, Z.Y., Yan, H.F., Yang, Y.H. & Wu, Y.D. (2010) Biotype and insecticide resistance status of the whitefly Bemisia tabaci from China. Pest Management Science 66, 1360–1366.Google Scholar
Wang, X.W., Luan, J.B., Li, J.M., Su, Y.L., Xia, J. & Liu, S.S. (2011a) Transcriptome analysis and comparison reveal divergence between two invasive whitefly cryptic species. BMC Genomics 12, 458.Google Scholar
Wang, P., Sun, D.B., Qiu, B.L. & Liu, S.S. (2011b) The presence of six cryptic species of the whitefly Bemisia tabaci complex in China as revealed by crossing experiments. Insect Science 18, 67–77.Google Scholar
Xu, J. (2009) Studies on the invasion by alien Bemisia tabaci in Zhejiang and comparison of biological characteristics between biotypes of the whitefly. PhD Thesis, Zhejiang University, Hangzhou, China.Google Scholar
Xu, J., Wang, W.L. & Liu, S.S. (2006) The occurrence and infestation of Bemisia tabaci biotype Q in partial regions of Zhejiang province. Plant Protection 32, 121 (in Chinese).Google Scholar
Xu, J., De Barro, P.J. & Liu, S.S. (2010) Reproductive incompatibility among genetic groups of Bemisia tabaci supports the proposition that the whitefly is a cryptic species complex. Bulletin of Entomological Research 100, 359–366.Google Scholar
Xu, J., Lin, K.K. & Liu, S.S. (2011) Performance on different host plants of an alien and an indigenous Bemisia tabaci from China. Journal of Applied Entomology 135, 771–779.Google Scholar
Yuan, L.Z., Wang, S.L., Zhou, J.C., Du, Y.Z., Zhang, Y.J. & Wang, J.J. (2012) Status of insecticide resistance and associated mutations in Q-biotype of whitefly, Bemisia tabaci, from eastern China. Crop Protection 31, 67–71.Google Scholar
Zang, L.S., Liu, S.S., Liu, Y.Q., Ruan, Y.M. & Wan, F.H. (2005) Competition between the B biotype and a non-B biotype of the whitefly, Bemisia tabaci, (Homopterea, Aleyrodidae) in Zhejiang, China. Biodiversity Sciences 13, 181–187 (in Chinese with an English summary).CrossRefGoogle Scholar