Hostname: page-component-77c89778f8-fv566 Total loading time: 0 Render date: 2024-07-16T18:12:23.778Z Has data issue: false hasContentIssue false
  • English
  • Français

Roles of mating behavioural interactions and life history traits in the competition between alien and indigenous whiteflies

Published online by Cambridge University Press:  01 March 2012

P. Wang ,
D.W. Crowder  and
S.-S. Liu
P. Wang
Affiliation:
Ministry of Agriculture Key Laboratory of Agricultural Entomology, Institute of Insect Sciences, Zhejiang University, 866 Yuhangtang Road, Hangzhou 310058, China
D.W. Crowder
Affiliation:
Department of Entomology, Washington State University, 166 FSHN Building, PO Box 646382, Pullman, WA 99164, USA
S.-S. Liu*
Affiliation:
Ministry of Agriculture Key Laboratory of Agricultural Entomology, Institute of Insect Sciences, Zhejiang University, 866 Yuhangtang Road, Hangzhou 310058, China
*
*Author for correspondence Fax: +86 571 88982355 E-mail: shshliu@zju.edu.cn
Get access Rights & Permissions [Opens in a new window]

Abstract

Interference competition between closely related alien and indigenous species often influences the outcome of biological invasions. The whitefly Bemisia tabaci species complex contains ≥28 putative species and two of them, Mediterranean (MED, formally referred to as the ‘Q biotype’) and Middle East-Asia Minor 1 (MEAM1, formally referred to as the ‘B biotype’), have recently spread to much of the world. In many invaded regions, these species have displaced closely related indigenous whitefly species. In this study, we integrated laboratory population experiments, behavioural observations and simulation modelling to investigate the capacity of MED to displace Asia II 1 (AII1, formally referred to as the ‘ZHJ2 biotype’), an indigenous whitefly widely distributed in Asia. Our results show that intensive mating interactions occur between MED and AII1, leading to reduced fecundity and progeny female ratio in AII1, as well as an increase in progeny female ratio in MED. In turn, our population cage experiments demonstrated that MED has the capacity to displace AII1 in a few generations. Using simulation models, we then show that both asymmetric mating interactions and differences in life history traits between the two species contribute substantially to the process of displacement. These findings would help explain the displacement of AII1 by MED in the field and, together with earlier studies on mating interactions between other species of the B. tabaci complex, indicate the widespread significance of asymmetric mating interactions in whitefly species exclusions.

Keywords

whiteflycryptic speciesinvasion biologybehavioural interactionspecies exclusionstochastic model
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 102 , Issue 4 , August 2012 , pp. 395 - 405
Copyright
Copyright © Cambridge University Press 2012

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.)

References

Byrne, D.N. & Bellows, T.S. (1991) Whitefly biology. Annual Review of Entomology 36, 431–457.CrossRefGoogle 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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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., Sitvarin, M.I. & Carrière, Y. (2010c) Mate discrimination in invasive whitefly species. Journal of Insect Behaviour 23, 364–380.CrossRefGoogle Scholar
De Barro, P.J. & Bourne, A. (2010) Ovipositional host choice by an invader accelerates displacement of its indigenous competitor. Biological Invasions 12, 3013–3023.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, 149–52.CrossRefGoogle Scholar
De Barro, P.J., Bourne, A., Khan, S.A. & Brancatini, V.A.L. (2006) Host plant and biotype density interactions – their role in the establishment of the invasive B biotype of Bemisia tabaci. Biological Invasions 8, 287–294.CrossRefGoogle Scholar
De Barro, P.J., Liu, S.S. & Bourne, A. (2010) Age-based differential host acceptability and human mediated disturbance prevent establishment of an invasive species and displacement of a native competitor. Biological Invasions 12, 3429–3438.CrossRefGoogle 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.CrossRefGoogle ScholarPubMed
Dinsdale, A., Cook, L., Riginos, C., Buckley, Y.M. & De Barro, P.J. (2010) Refined global analysis of Bemisia tabaci (Gennadius) (Hemiptera: Sternorrhyncha: Aleyrodoidea) mitochondrial CO1 to identify species level genetic boundaries. Annals of the Entomological Society of America 103, 196–208.CrossRefGoogle Scholar
Elbaz, M., Lahav, N. & Morin, S. (2010) Evidence for pre-zygotic reproductive barrier between the B and Q biotypes of Bemisia tabaci (Hemiptera: Aleyrodidae). Bulletin of Entomological Research 100, 581–590.CrossRefGoogle Scholar
Gröning, J. & Hochkirch, A. (2008) Reproductive interference between animal species. The Quarterly Review of Biology 83, 257–282.CrossRefGoogle ScholarPubMed
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., Denholm, I., Gorman, K., Cenis, J.L., Kontsedalov, S. & Ishaaya, I. (2003) Biotype Q of Bemisia tabaci identified in Israel. Phytoparasitica 31, 94–98.CrossRefGoogle Scholar
Hu, J., De Barro, P., Zhao, H., Wang, J., Nardi, F. & Liu, S.S. (2011) An extensive field survey combined with phylogenetic analysis reveals rapid and widespread invasion of two alien whiteflies in China. PLoS ONE 6, e16061.Google ScholarPubMed
Kishi, S., Nishida, T. & Tsubaki, Y. (2009) Reproductive interference determines persistence and exclusion in species interactions. Journal of Animal Ecology 78, 1043–1049.CrossRefGoogle ScholarPubMed
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. (2012) Species concepts as applied to the whitefly Bemisia tabaci systematics: how many species are there? Journal of Integrative Agriculture 11, 176–186.CrossRefGoogle Scholar
Lockwood, J.L., Hoopes, M.F. & Marchetti, M.P. (2007) Invasion Ecology. Oxford, UK, Blackwell Publishing.Google Scholar
Luan, J.B. & Liu, S.S.Differences in mating behaviour lead to asymmetric mating interactions and consequential changes in sex ratio between an invasive and an indigenous whitefly. Integrative Zoology, in press (doi: 10.1111/j.1749-4877.2011.00273.x).Google 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.CrossRefGoogle 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.CrossRefGoogle Scholar
Martinez-Carrillo, J.L. & Brown, J.K. (2007) First report of the Q biotype of Bemisia tabaci in southern Sonora, Mexico. Phytoparasitica 35, 282–284.CrossRefGoogle Scholar
McKenzie, C.L., Anderson, P.K. & Villarreal, N. (2004) An extensive survey of Bemisia tabaci (Homoptera: Aleyrodidae) in agricultural ecosystems in Florida. Florida Entomologist 87, 403–407.CrossRefGoogle Scholar
McKenzie, C.L., Hodges, G., Osborne, L.S., Byrne, F.J. & Shatters, R.G. (2009) Distribution of Bemisia tabaci (Hemiptera: Aleyrodidae) biotypes in Florida-investigating the Q invasion. Journal of Economic Entomology 102, 670–676.Google Scholar
Microsoft (2002) Microsoft Excel 2002. Microsoft, Seattle, WA, USA.Google Scholar
Nombela, G., Garzo, E.M., Duque, M. & Muñiz, M. (2009) Preinfestations of tomato plants by whiteflies (Bemisia tabaci) or aphids (Macrosiphum euphorbiae) induce variable resistance or susceptibility responses. Bulletin of Entomological Research 99, 183–191.CrossRefGoogle ScholarPubMed
Oliveira, M.R.V., Henneberry, T.J. & Anderson, P. (2001) History, current status, and collaborative research projects for Bemisia tabaci. Crop Protection 20, 709–723.CrossRefGoogle Scholar
Perring, T.M. (1996) Biological differences of two species of Bemisia that contribute to adaptive advantage. pp. 3–16 in Gerling, D. & Mayer, R.T. (Eds) Bemisia 1995: Taxonomy, Biology, Damage, Control and Management. Andover, Hants, UK, Intercept.Google Scholar
Perring, T.M. & Symmes, E.J. (2006) Courtship behaviour of Bemisia argentifolii (Hemiptera: Aleyrodidae) and whitefly mate recognition. Annals of the Entomological Socety America 99, 598–606.CrossRefGoogle Scholar
Perring, T.M., Copper, A.D., Rodriguez, R.J., Farrar, C.A. & Bellows, T.S. (1993) Identification of a whitefly species by genomic and behavioural studies. Science 259, 74–77.CrossRefGoogle 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.CrossRefGoogle ScholarPubMed
Reitz, S.R. & Trumble, J.T. (2002) Competitive displacement among insects and arachnids. Annual Review of Entomology 47, 435–65.CrossRefGoogle ScholarPubMed
Ruan, Y.M., Luan, J.B., Zang, L.S. & Liu, S.S. (2007) Observing and recording copulation events of whiteflies on plants using a video camera. Entomologia Experimentalis et Applicata 124, 229–233.CrossRefGoogle Scholar
StatSoft Inc. (2003) STATISTICSA (data analysis software system), version 6.1. Available online at www.statsoft.com.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.CrossRefGoogle Scholar
Ueda, S. & Brown, J.K. (2006) First report of the Q biotype of Bemisia tabaci in Japan by mitochondrial cytochrome oxidase 1 sequence analysis. Phytoparasitica 34, 405–411.CrossRefGoogle Scholar
Wan, F.H., Zhang, G.F., Liu, S.S., Chen, L., Chu, D., Zhang, Y.J., Zang, L.S., Jiu, M., Lu, Z.C., Cui, X.H., Zhang, L.P., Zhang, F., Zhang, Q.W., Liu, W.X., Liang, P., Lei, Z.R. & Zhang, Y.J. (2009) Invasive mechanism and management strategy of Bemisia tabaci (Gennadius) biotype B: Progress report of 973 Program on invasive alien species in China. Science in China Series C: Life Sciences 52, 88–95.Google ScholarPubMed
Wang, P., Ruan, Y.M. & Liu, S.S. (2010) Crossing experiments and behavioural observations reveal reproductive incompatibility among three putative species of the whitefly Bemisia tabaci. Insect Science 17, 508–516.CrossRefGoogle Scholar
Wang, P., Sun, D.B., Qiu, B.L. & Liu, SS. (2011) The presence of six cryptic species of the whitefly Bemisia tabaci complex in China as revealed by crossing experiments. Insect Science 18, 67–77.CrossRefGoogle 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 ScholarPubMed
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.CrossRefGoogle Scholar
Xue, M., Wang, C.X., Bi, M.J., Li, Q.L. & Liu, T.X. (2010) Induced defense by Bemisia tabaci biotype B (Hemiptera: Aleyrodidae) in tobacco against Myzus persicae (Hemiptera: Aphididae). Environmental Entomology 39, 883–891.CrossRefGoogle ScholarPubMed
Zang, L.S. & Liu, S.S. (2007) A comparative study on mating behaviour between the B biotype and a non-B populations of the whitefly, Bemisia tabaci (Hemiptera: Aleyrodidae) from Zhejiang, China. Journal of Insect Behaviour 20, 157–171.CrossRefGoogle 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 (Homoptera, Aleyrodidae) in Zhejiang, China. Biodiversity Science 13, 181–187 (in Chinese with an English summary).CrossRefGoogle Scholar