Main Article Content

Authors

Whiteflies are economically important plant pests that cause damage to crops worldwide. This study aimed to update the status of whiteflies in Jordan by combining the classical morphological identification and the DNA markers using the mitochondrial cytochrome oxidase I (mtCOI) gene. Over the course of three consecutive years, 111 whiteflies were collected from different geographical regions and different plant hosts in Jordan. The results showed that, in addition to Bemisia tabaci, another nine different whitefly species were identified, including two species that were recorded for the first time in Jordan: Africaleurodes coffeacola, and Tetraleurodes neemani. A special focus has been given to economically important plant pests like the B. tabaci species complex. Three different diagnostic techniques were used to identify B. tabaci putative species based on mtCOI gene. All the collected samples of B. tabaci species complex were identified as Middle East–Asia Minor 1 (MEAM1) putative species.

Ghabeish, I., Sweiss, M. ., & Anfoka, G. (2021). Updated status of whiteflies (Hemiptera: Aleyrodidae) in Jordan with emphasis on the Bemisia tabaci species complex. Revista Colombiana De Entomología, 47(1), 1–9. https://doi.org/10.25100/socolen.v47i1.8944

ALLAWI, T. R. 1994. Whitefly species in Jordan. Arab Journal Plant Protection 12 (1): 30-32.

BARINAGA, M. 1993. Is devastating whitefly invader really a new species? Science 259 (5091): 30-31. https://doi.org/10.1126/science.8418492

BING, X. L.; RUAN, Y. M.; RAO, Q.; WANG, X. W.; LIU, S. S.2012. Diversity of secondary endosymbionts among different putative species of the whitefly Bemisia tabaci. Insect Science 20(2): 194-206. https://doi.org/10.1111/j.1744-7917.2012.01522.x

BOYKIN, L. M. 2014. Bemisia tabaci nomenclature: lessons learned. Pest Management Science 70 (10): 1454-1459. https://doi.org/10.1002/ps.3709

BOYKIN, L. M.; SHATTERS JR, R. G.; ROSELL, R. C.; McKENZIE, C. L.; BAGNALL, R. A.; DE BARRO, P.; FROHLICH, D. R. 2007. Global relationships of Bemisia tabaci (Hemiptera: Aleyrodidae) revealed using Bayesian analysis of mitochondrial COI DNA sequences. Molecular Phylogenetic and Evolution 44(3): 1306-1319. https://doi.org/10.1016/j.ympev.2007.04.020

BOYKIN, L. M.; ARMSTRONG, K. F.; KUBATKO, L.; DE BARRO, P. 2012. Species delimitation and global biosecurity. Evolutionary Bioinformatics 8: 1-37. https://doi.org/10.4137/EBO.S8532

BROADBENT, A. B.; FOOTTIT, R. G.; MURPHY, G. D. 1989. Sweet potato whitefly Bemisia tabaci (Gennadius) (Homoptera: Aleyrodidae), a potential insect pest in Canada. Canadian Entomology 121 (11): 1027-1028. https://doi.org/10.4039/ Ent1211027-11

BROWN, J. K. 2007. The Bemisia tabaci complex: genetic and phenotypic variation and relevance to TYLCV-vector interactions. pp. 25-56. In: Czosnek, H. (Ed.). Tomato yellow leaf curl virus disease. Springer. Jerusalem, Israel. 447 p. https://doi.org/10.1007/978-1-4020-4769-5_3

BROWN, J. K.; FROHLICH, D. R.; ROSELL, R. C. 1995a. The sweet potato or silverleaf whiteflies: biotypes of Bemisia tabacior a species complex? Annual Review of Entomology 40 (1): 511-534. https://doi.org/10.1146/annurev.en.40.010195.002455

BROWN, J. K.; COATS, S. A.; BEDFORD, I. D.; MARKHAM, P. G.; BIRD, J.; FROHLICH, D. R. 1995b. Characterization and distribution of esterase electromorphs in the whitefly, Bemisia tabaci (Genn.) (Homoptera: Aleyrodidae). Biochemical Genetics 33: 205-214. https://doi.org/10.1007/BF02401851

BYRNE, D. N.; BELLOWS JR, T. S. 1991. Whitefly biology. Annual Review Entomology 36 (1): 431 457. https://doi.org/10.1146/ annurev.en.36.010191.002243

CENIS, J. L.; PEREZ, P.; FERERES, A. 1993. Identification of aphid (Homoptera: Aphididae) species and clones by random amplified polymorphic DNA. Annals of the Entomological Society of America 86 (5): 545-550. https://doi.org/10.1093/aesa/86.5.545

CERVERA, M. T.; CABEZAS, J. A.; SIMON, B.; MARTINEZ-ZAPATER, J. M.; BEITIA, F.; CENIS, J. L. 2000. Genetic relationships among biotypes of Bemisia tabaci (Hemiptera: Aleyrodidae)

based on AFLP analysis. Bulletin of Entomological Research 90(5): 391-396. https://doi.org/10.1017/S0007485300000523

CHEEK, S.; MACDONALD, O. 1994. Statutory controls to prevent the establishment of Bemisia tabaci in the United Kingdom. Pest Science 42 (2): 135-142.

COSTA, H. S.; BROWN, J. K. 1991. Variation in biological characteristics and esterase patterns among populations of Bemisiatabaci, and the association of one population with silverleaf

symptom induction. Entomologia Experimentalis et Applicata 61 (3): 211-219. https://doi.org/10.1111/j.1570-7458.1991.tb01553.x

DE BARRO, P. J.; DRIVER, F.; TRUEMAN, J. W. H.; CURRAN, J. 2000. Phylogenetic relationships of world populations of Bemisia tabaci (Gennadius) using ribosomal ITS1. Molecular

Phylogenetic and Evolution 16 (1): 29-36. https://doi.org/10.1006/mpev.1999.0768

DE BARRO, P. J.; LIU, S. S.; BOYKIN, L. M.; DINSDALE, A. B. 2011. Bemisia tabaci: a statement of species status. Annual Review of Entomology 56: 1-19. https://doi.org/10.1146/annurevento-112408-085504

DINSDALE, A.; COOK, L.; RIGINOS, C.; BUCKLEY, Y. M.; DE BARRO, P. 2010. Refined global analysis of Bemisia tabaci (Gennadius) (Hemiptera: Sternorrhyncha: Aleyrodidae) mitochondrial CO1 to identify species level genetic boundaries.

Annals of the Entomological Society of America 103 (2): 196- 208. https://doi.org/10.1603/AN09061

EUROPEAN AND MEDITERRANEAN PLANT PROTECTION ORGANIZATION. 2004. Bemisia tabaci. Bulletin OEPP/EPPO Bulletin 34: 281-288. https://doi.org/10.1111/j.1365-2338.2004.00729.x

FROHLICH, D. R.; TORRES-JEREZ, I.; BEDFORD, I. D.; MARKHAM, P. G.; BROWN, J. K. 1999. A phylogeographical analysis of the Bemisia tabaci species complex based on mitochondrial

DNA markers. Molecular Ecology 8 (10): 1683-1691.

https://doi.org/10.1046/j.1365-294x.1999.00754.x GAMARRA, H. A.; FUENTES, S.; MORALES, F. J.; GLOVER, R.; MALUMPHY, C.; BARKER, I. 2010. Bemisia afersensu lato, avector of Sweet potato chlorotic stunt virus. Plant Diseases 94 (5): 510-514. https://doi.org/10.1094/PDIS-94-5-0510

GHAHARI, H.; ABD-RABOU, S.; ZAHRADNIK, J.; OSTOVAN, H. 2009. Annotated catalogue of whiteflies (Hemiptera: Sternorrhyncha: Aleyrodidae) from Arasbaran, Northwestern Iran. Journal of Entomology and Nematology 1 (1): 007-018. https://doi.org/10.5897/JEN.9000004

GHANIM, M.; KONTSEDALOV, S. 2007. Gene expression in pyriproxyfen- resistant Bemisia tabaci Q biotype. Pest Management Science: formerly Pesticide Science. 63 (8): 776-783. https://doi.org/10.1002/ps.1410

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. https://doi.org/10.1007/BF02979772

HOROWITZ, A. R.; KONTSEDALOV, S.; KHASDAN, V.; ISHAAYA, I. 2005. Biotypes B and Q of Bemisia tabaci and their relevanceto neonicotinoid and pyriproxyfen resistance. Archives of Insect Biochemistry and Physiology 58 (4): 216-225. https://doi.org/10.1002/arch.20044

IDRISS, M.; ABDALLAH, N.; AREF, N.; HARIDY, G.; MADKOUR, M. 1997. Biotypes of the castor bean whitefly Trialeurodes ricini (Misra) (Hom., Aleyrodidae) in Egypt: biochemical

characterization and efficiency of geminivirus transmission. Journal of Applied Entomology 121 (1-5): 501-509. https://doi. org/10.1111/j.1439-0418.1997.tb01440.x

JONES, D. R. 2003. Plant viruses transmitted by whiteflies. European Journal of Plant Pathology 109 (3): 195-219. https://doi.org/10.1023/A:1022846630513

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 (6): 605-613. https://doi.org/10.1079/BER2005390

KIRK, A. A.; LACEY, L. A.; BROWN, J. K.; CIOMPERLIK, M. A.; GOOLSBY, J. A.; VACEK, D. C.; WENDEL, L. E.; NAPOMPETH, B. 2000. Variation in the Bemisia tabaci species complex (Hemiptera: Aleyrodidae) and its natural enemies leading to successful biological control of Bemisia biotype B in the USA. Bulletin of Entomological Research 90 (4): 317-327. https://doi.

org/10.1017/S0007485300000444

KO, C.; CHANG, S.; HU, C. 2005. Survey of whiteflies and their transmission of plant viruses in Taiwan. Taipei: ASPAC Food and Fertilizer Technology Centre. https://www.fftc.org.tw/htmlarea_file/library/20110712181840/eb571.pdf

KUMAR, S.; STECHER, G.; LI, M.; KNYAZ, C.; TAMURA, K. 2018. MEGA X: Molecular Evolutionary Genetics Analysis across Computing Platforms. Molecular Biology and Evolution 35 (6): 1547-1549. https://doi.org/10.1093/molbev/msy096

LIU, S.; COLYIN, 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 (2): 176- 186. https://doi.org/10.1016/S2095-3119(12)60002-1

LIU, G.; MA, H.; XIE, H.; XUAN, N.; GUO, X.; FAN, Z.; RAJASHEKAR, B.; ARNAUD, P.; OFFMANN, B.; PICIMBON, J-F. 2016. Biotype characterization, developmental profiling, insecticide response and binding property of Bemisia tabaci chemosensory proteins: role of CSP in insect defense. PLoS ONE 11 (5): e0154706. https://doi.org/10.1371/journal.pone.0154706

LUO, C.; YAO, Y.; WANG, R.; YAN, F.; HU, D.; ZHANG, Z. 2002. The use of mitochondrial cytochrome oxidase I (mt CO I) gene sequences for the identification of biotypes of Bemisia tabaci (Gennadius) in China. Acta Entomologica Sinica 45 (6): 757- 763. https://europepmc.org/article/cba/381891

MARTIN, J. H. 2004. Whiteflies of Belize (Hemiptera: Aleyrodidae). Part 1-introduction and account of the subfamily Aleurodicinae Quaintance & Baker. Zootaxa 681 (1): 1-119. https://doi.org/10.11646/zootaxa.681.1.1

MARTIN, J. H.; MOUND, L. A. 2007. An annotated check list of the world’s whiteflies (Insecta: Hemiptera: Aleyrodidae). Zootaxa 1492 (1): 1-84. https://doi.org/10.11646/zootaxa.1492.1.1

MLYNAREK, J. J., LABBÉ, R. M. 2018. Trialeurodes abutiloneus (Haldeman) (Hemiptera: Aleyrodidae), a species long present but never officially recorded in Canada. The Canadian Entomologist 150 (4): 532-538. https://doi.org/10.4039/tce.2018.26

MORGULIS, A.; COULOURIS, G.; RAYTSELIS, Y.; MADDEN, T. L.; AGARWALA, R.; SCHAFFER, A. A. 2008. Database indexing for production MegaBLAST searches. Bioinformatics 24 (16): 1757-1764. https://doi.org/10.1093/bioinformatics/btn554

NAUEN, R.; DENHOLM, I. 2005. Resistance of insect pests to neonicotinoid insecticides: current status and future prospects. Archive of Insect Biochemistry and Physiology 58 (4): 200-215.

https://doi.org/10.1002/arch.20043

NAUEN, R.; STUMPF, N.; ELBERT, A. 2002. Toxicological and mechanistic studies on neonicotinoid cross resistance in Q-type Bemisia tabaci (Hemiptera: Aleyrodidae). Pest Management Science 58 (9): 868-875. https://doi.org/10.1002/ps.557

NAVAS-CASTILLO, J.; FIALLO-OLIVE, E.; SANCHEZ-CAMPOS, S. 2011. Emerging virus diseases transmitted by whiteflies. Annual Review of Phytopathology 49: 219-248. https://doi.

org/10.1146/annurev-phyto-072910-095235

OLIVEIRA, M. R. V.; HENNEBERRY, T. J.; ANDERSON, P. 2001. History, current status, and collaborative research projects for Bemisia tabaci. Crop Protection 20 (9): 709-723. https://doi.

org/10.1016/S0261-2194(01)00108-9

OYELADE, O. J.; AYANSOLA, A. A. 2015. Diversity and distribution of whiteflies in south-western Nigeria. African Crop Science Journal 23 (2): 135-149. https://www.ajol.info/index.php/acsj/

article/view/117735

POLSTON, J. E.; DE BARRO, P.; BOYKIN, L. M. 2014. Transmission specificities of plant viruses with the newly identified species of the Bemisia tabaci species complex. Pest Management Science 70 (10): 1547-1552. https://doi.org/10.1002/ps.3738

PRABHAKER, N.; COUDRIET, D. L.; TOSCANO, N. C. 1988. Effect of synergists on organophosphate and permethrin resistance in sweet potato whitefly (Homoptera: Aleyrodidae). Journal of Economic Entomology 81 (1): 34-39. https://doi.org/10.1093/jee/81.1.34

ROSELL, R. C.; BEDFORD, I. D.; FROHLICH, D. R.; GILL, R. J.; BROWN, J. K.; MARKHAM, P. G. 1997. Analysis of morphological variation in distinct populations of Bemisia tabaci

(Homoptera: Aleyrodidae). Annals of Entomological Society of America 90 (5): 575-589. https://doi.org/10.1093/aesa/90.5.575

SHARAF, N.; ALLAWI, T. F. 1980. Studies on whiteflies on tomato in Jordan Valley I. Host range of the tobacco whitefly Bemisia tabaci Genn. (Homoptera: Aleyrodidae). Dirasat 7 (1): 53-63.

SHARAF, N.; HASAN, H. 2003. The identification of two biotypes of Bemisia tabaci in Jordan. Dirasat 30 (1): 101-108. https://www.cabdirect.org/cabdirect/abstract/20033042084

SHI, X.; TANG, X.; ZHANG, X.; ZHANG, D.; LI, F.; YAN, F.; ZHANG, Y.; ZHOU, X.; LIU, Y. 2018. Transmission efficiency, preference and behavior of Bemisia tabaci MEAM1 and MED under the influence of Tomato chlorosis virus. Frontiers in Plant Science 8: 1-9. https://doi.org/10.3389/fpls.2017.02271

SHUKLA, A. K.; UPADHYAY, S. K.; MISHRA, M.; SAURABH, S.; SINGH, R.; SINGH, H.; THAKUR, N.; RAI, P.; PANDEY, P.; HANS, A. L.; SRIVASTAVA, S. 2016. Expression of an insecticidal fern protein in cotton protects against whitefly. Nature Biotechnology 34 (10): 1046-1051. https://doi.org/10.1038/nbt.3665

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 (2): 211-220. https://doi.org/10.1017/S0007485310000416

TAMURA, K.; NEI, M. 1993. Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Molecular Biology and Evolution

(3): 512-526. https://doi.org/10.1093/oxfordjournals.molbev.a040023

TAY, W. T.; EVANS, G. A.; BOYKIN, L. M.; DE BARRO, P. J. 2012. Will the real Bemisia tabaci please stand up? PLoS One 7 (11): e50550. https://doi.org/10.1371/journal.pone.0050550

TSAGKARAKOU, A.; TSIGENOPOULOS, C. S.; GORMAN, K.; LAGNEL, J.; BEDFORD, I. D. 2007. Biotype status and genetic polymorphism of the whitefly Bemisia tabaci (Hemiptera: Aleyrodidae) in Greece: mitochondrial DNA and microsatellites. Bulletin of Entomological Research 97 (1): 29-40. https://doi.org/10.1017/S000748530700466X

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

(1): 1-12. https://doi.org/10.1186/1471-2164-12-458 WANG, H-L.; YANG, J.; BOYKIN, L. M.; ZHAO, Q-Y.; LI, Q.; WANG, X-W.; LIU, S-S. 2013. The characteristics and expression profiles of the mitochondrial genome for the Mediterranean species of the Bemisia tabaci complex. BMC Genomics. 14 (1):1-15. https://doi.org/10.1186/1471-2164-14-401

WANG, J.; DU, Y.; XU, Z. 2016. Six newly recorded species of whitefly (Hemiptera: Aleyrodidae) from China. Zoological Systematics 41 (4): 427-438. https://doi.org/10.11865/zs.201647

WATANABE, L. F. M.; BELLO, V. H.; DE MARCHI, B. R.; SILVA, F. B.; FUSCO, L. M.; SARTORI, M. M. P.; PAVAN, M. A.; KRAUSE-SAKATE, R. 2019. Performance and competitive displacement of Bemisia tabaci MEAM1 and MED cryptic species on different host plants. Crop Protection 124: 104860. https://doi.org/10.1016/j.cropro.2019.104860

WU, X.; LI, Z.; HU, D.; SHEN, Z. 2003. Identification of Chinese populations of Bemisia tabaci (Gennadius) by analyzing ribosomal ITS1 sequence. Progress in Natural Science 13 (4): 276-281. https://doi.org/10.1080/10020070312331343530

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 (3): 359-366. https:// doi.org/10.1017/S0007485310000015

YANG, N.; XIE, W.; YANG, X.; WANG, S.; WU, Q.; LI, R.; PAN, H.; LIU, B.; SHI, X.; FANG, Y.; XU, B.; ZHOU, X.; ZHANG, Y. 2013. Transcriptomic and proteomic responses of sweet potato whitefly, Bemisia tabaci, to thiamethoxam. PLoS One 8 (5): e61820. https://doi.org/10.1371/journal.pone.0061820

YANG, J.; XIE, W.; LIU, B.; WANG, S.; WU, Q.; HE, Y.; ZHANG, Y; JIAO, X. 2020. Phenolics, rather than glucosinolates, mediate host choice of Bemisia tabaci MEAM1 and MED on five cabbage

genotypes. Journal of Applied Entomology 144 (4): 287-296. https://doi.org/10.1111/jen.12737

ZHANG, Z.; SCHWARTZ, S.; WAGNER, L.; MILLER, W. 2000. A greedy algorithm for aligning DNA sequences. Journal of Computational Biology 7 (1-2): 203-214. https://doi.org/10.1089/10665270050081478

ZHANG, L. P.; ZHANG, Y. J.; ZHANG, W. J.; WU, Q. J.; XU, B. Y.; CHU, D. 2005. Analysis of genetic diversity among different geographical populations and determination of biotypes of Bemisia tabaci in China. Journal of Applied Entomology 129 (3): 121-128. https://doi.org/10.1111/j.1439-0418.2005.00950.x

Received 2020-02-21
Accepted 2020-10-09
Published 2021-05-21