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Effects of reproductive interference on the competitive displacement between two invasive whiteflies

Published online by Cambridge University Press:  13 February 2014

Di-Bing Sun ,
Jie Li ,
Yin-Quan Liu ,
David W. Crowder  and
Shu-Sheng Liu
Di-Bing Sun
Affiliation:
Ministry of Agriculture Key Laboratory of Agricultural Entomology, Institute of Insect Sciences, Zhejiang University, Hangzhou 310058, China
Jie Li
Affiliation:
Ministry of Agriculture Key Laboratory of Agricultural Entomology, Institute of Insect Sciences, Zhejiang University, Hangzhou 310058, China
Yin-Quan Liu
Affiliation:
Ministry of Agriculture Key Laboratory of Agricultural Entomology, Institute of Insect Sciences, Zhejiang University, Hangzhou 310058, China
David W. Crowder
Affiliation:
Department of Entomology, Washington State University, 166 FSHN Building, PO Box 646382, Pullman, WA 99164, USA
Shu-Sheng Liu*
Affiliation:
Ministry of Agriculture Key Laboratory of Agricultural Entomology, Institute of Insect Sciences, Zhejiang University, Hangzhou 310058, China
*
*Author for correspondence Phone: +86 571 88982505 Fax: +86 571 88982355 E-mail: [email protected]
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Abstract

Reproductive interference is one of the major factors mediating species exclusion among insects. The cryptic species Middle East-Asia Minor 1 (MEAM1) and Mediterranean (MED) of the whitefly Bemisia tabaci complex have invaded many parts of the world and often exhibit niche overlap and reproductive interference. However, contrasting patterns of competitive displacement between the two invaders have been observed between regions such as those in USA and China. Understanding the roles of reproductive interference in competitive interactions between populations of the two species in different regions will help unravel other factors related to their invasion. We integrated laboratory population experiments, behavioural observations and simulation modelling to investigate the role of reproductive interference on species exclusion between MEAM1 and MED in China. In mixed cohorts of the two species MEAM1 always excluded MED in a few generations when the initial proportion of MEAM1 was ⩾0.25. Even when the initial proportion of MEAM1 was only 0.10, however, MEAM1 still had a higher probability of excluding MED than that for MED to exclude MEAM1. Importantly, we show that as MEAM1 increased in relative abundance, MED populations became increasingly male-biased. Detailed behavioural observations confirmed that MEAM1 showed a stronger reproductive interference than MED, leading to reduced frequency of copulation and female progeny production in MED. Using simulation modelling, we linked our behavioural observations with exclusion experiments to show that interspecific asymmetric reproductive interference predicts the rate of species exclusion of MED by MEAM1. These findings not only reveal the importance of reproductive interference in the competitive interactions between the two invasive whiteflies as well as the detailed behavioural mechanisms, but also provide a valuable framework against which the effects of other factors mediating species exclusion can be explored.

Keywords

invasion ecologyinvasive speciescompetitive displacementmating behaviourcommunity ecology
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 104 , Issue 3 , June 2014 , pp. 334 - 346
Copyright
Copyright © Cambridge University Press 2014 

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References

Boykin, L.M., Armstrong, K.F., Kubatko, L. & De Barro, P.J. (2012) Species delimitation and global biosecurity. Evolutionary Bioinformatics 8, 1–37.CrossRefGoogle ScholarPubMed
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
Chu, D., Hu, X.S., Gao, C.S., Zhao, H.Y., Nichols, R.L. & Li, X.C. (2012) 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
Crowder, D.W., Horowitz, A.R., De Barro, P.J., Liu, S.S., Showalter, A.M., Kontsedalov, S., Khasdan, V., Shargal, A., Liu, J. & Carrière, Y. (2010 a) 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. (2010 b) Plasticity in mating behaviour drives asymmetric reproductive interference in whiteflies. Animal Behaviour 79, 579–587.CrossRefGoogle 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.CrossRefGoogle 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.CrossRefGoogle ScholarPubMed
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., 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
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.CrossRefGoogle Scholar
Hochkirch, A., Gröning, J. & Bücker, A. (2007) Sympatry with the devil: reproductive interference could hamper species coexistence. Journal of Animal Ecology 76, 633–642.CrossRefGoogle ScholarPubMed
Hsieh, C.H., Chiang, Y.H. & Ko, C.C. (2011) Population genetic structure of the newly invasive Q biotype of Bemisia tabaci in Taiwan. Eetomologia Experimentalis et Applicata 138, 263–271.CrossRefGoogle Scholar
Hu, J., De Barro, P.J., Zhao, H., Wang, J., Nardi, F. & Liu, S.S. (2011 a) An extensive field survey combined with a phylogenetic analysis reveals rapid and widespread invasion of two alien whiteflies in China. PLoS ONE 6, e16061.CrossRefGoogle ScholarPubMed
Hu, X.S., Dennehy, T.J., Ni, X.Z., Zhao, H.Y., Nichols, R.L. & Li, X.C. (2011 b) 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.CrossRefGoogle Scholar
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
Kuno, E. (1992) Competitive exclusion through reproductive interference. Researches on Population Ecology 34, 275–284.CrossRefGoogle 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.CrossRefGoogle 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
Luan, J.B. & Liu, S.S. (2012) Differences in mating behaviour lead to asymmetric mating interactions and consequential changes in sex ratio between an invasive and an indigenous whitefly. Integrative Zoology 7, 1–15.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
Luan, J.B., De Barro, P.J., Ruan, Y.M. & Liu, S.S. (2013) Distinct mating strategies underlying asymmetric mating interactions between whiteflies. Entomologia Experimentalis et Applicata 146, 186–194.CrossRefGoogle 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.CrossRefGoogle Scholar
Microsoft (2002) Microsoft Excel 2002, Seattle, WA, USA, Microsoft.Google Scholar
Muniz, M., Nombela, G. & Barrios, L. (2002) Within-plant distribution and infestation pattern of the B- and Q-biotypes of the whitefly, Bemisia tabaci, on tomato and pepper. Entomologia Experimentalis et Applicata 104, 369–373.CrossRefGoogle Scholar
Naranjo, S.E. & Ellsworth, P.C. (2009) Fifty years of the integrated control concept: moving the model and implementation forward in Arizona. Pest Management Science 65, 1267–1286.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Park, J.G., Jahan, S.M.H., Song, W.G., Lee, H.J., Lee, Y.S., Choi, H.S., Lee, K.S., Kim, C.S., Lee, S.C. & Lee, K.Y. (2012) Identification of biotypes and secondary endosymbionts of Bemisia tabaci in Korea and relationships with the occurrence of TYLCV disease. Journal of Asia-Pacific Entomology 15, 186–191.CrossRefGoogle 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.CrossRefGoogle 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
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
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.CrossRefGoogle Scholar
Reitz, S.R. & Trumble, J.T. (2002) Species exclusion among insects and arachnids. Annual Review of Entomology 47, 435–65.CrossRefGoogle Scholar
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
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.CrossRefGoogle 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.Google Scholar
Statsoft, Inc. (2003) STATISTICSA (data analysis software system), version 6.1, 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: genetic and behavioural evidence. Bulletin of Entomological Research 101, 211–220.CrossRefGoogle Scholar
Sun, D.B., Liu, Y.Q., Qin, L., Xu, J., Li, F.F. & Liu, S.S. (2013) Competitive displacement between two invasive whiteflies: insecticide application and host plant effects. Bulletin of Entomological Research 103, 344–353.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
Wang, P., Crowder, D.W. & Liu, S.S. (2012) Roles of mating behavioural interactions and life history traits in the competition between alien and indigenous whiteflies. Bulletin of Entomological Research 102, 395–405.CrossRefGoogle ScholarPubMed
Wang, X.W., Luan, J.B., Li, J.M., Su, Y.L., Xia, J. & Liu, S.S. (2011) Transcriptome analysis and comparison reveal divergence between two invasive whitefly cryptic species. BMC Genomics 12, 458.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
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