Hostname: page-component-8448b6f56d-sxzjt Total loading time: 0 Render date: 2024-04-16T05:33:57.168Z Has data issue: false hasContentIssue false
  • English
  • Français

Tephritidae bacterial symbionts: potentials for pest management

Published online by Cambridge University Press:  21 June 2019

M.S. Noman ,
L. Liu ,
Z. Bai  and
Z. Li
M.S. Noman
Affiliation:
Department of Entomology, College of Plant Protection, China Agricultural University, Beijing 100193, P.R. China
L. Liu
Affiliation:
Department of Entomology, College of Plant Protection, China Agricultural University, Beijing 100193, P.R. China
Z. Bai
Affiliation:
Department of Entomology, College of Plant Protection, China Agricultural University, Beijing 100193, P.R. China
Z. Li*
Affiliation:
Department of Entomology, College of Plant Protection, China Agricultural University, Beijing 100193, P.R. China
*
*Author for correspondence Phone: 86-10-62733000 Fax: 86-10-62733404 E-mail: lizh@cau.edu.cn
Get access Rights & Permissions [Opens in a new window]

Abstract

Tephritidae is a large family that includes several fruit and vegetable pests. These organisms usually harbor a variegated bacterial community in their digestive systems. Symbiotic associations of bacteria and fruit flies have been well-studied in the genera Anastrepha, Bactrocera, Ceratitis, and Rhagoletis. Molecular and culture-based techniques indicate that many genera of the Enterobacteriaceae family, especially the genera of Klebsiella, Enterobacter, Pectobacterium, Citrobacter, Erwinia, and Providencia constitute the most prevalent populations in the gut of fruit flies. The function of symbiotic bacteria provides a promising strategy for the biological control of insect pests. Gut bacteria can be used for controlling fruit fly through many ways, including attracting as odors, enhancing the success of sterile insect technique, declining the pesticide resistance, mass rearing of parasitoids and so on. New technology and recent research improved our knowledge of the gut bacteria diversity and function, which increased their potential for pest management. In this review, we discussed the diversity of bacteria in the economically important fruit fly and the use of these bacteria for controlling fruit fly populations. All the information is important for strengthening the future research of new strategies developed for insect pest control by the understanding of symbiotic relationships and multitrophic interactions between host plant and insects.

Keywords

fruit flytephritidsbacterial symbiontspest management
Type
Review Article
Information
Bulletin of Entomological Research , Volume 110 , Issue 1 , February 2020 , pp. 1 - 14
Check for updates
Copyright
Copyright © Cambridge University Press 2019 

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.)

Footnotes

†

These authors contributed equally to this work.

References

Aharon, Y., Pasternak, Z., Yosef, M.B., Behar, A., Lauzon, C., Yuval, B. & Jurkevitcha, E. (2013) Phylogenetic, metabolic, and taxonomic diversities shape Mediterranean fruit fly microbiotas during ontogeny. Applied and Environmental Microbiology 79, 303–313.Google Scholar
Allen, T.C. & Riker, A.J. (1932) A rot of apple fruit caused by Phytomonas melophthora, n. sp., following invasion by the apple maggot. Phytopathology 22(6), 557–571.Google Scholar
Allen, T.C., Pinckard, J.A. & Riker, A.J. (1934) Frequent association of Phytomonas melophthora, with various stages in the life cycle of the apple maggot, Rhagoletis pomonella. Phytopathology 24(3), 228–238.Google Scholar
Amann, R.I., Ludwig, W. & Schleifer, K.H. (1995) Phylogenetic identification and in situ detection of individual microbial cells without cultivation. Microbiological Reviews 59, 143–169.Google Scholar
Andongma, A.A., Wan, L., Dong, Y.-C., Li, P., Desneux, N. et al. (2015) Pyrosequencing reveals a shift in symbiotic bacteria populations across life stages of Bactrocera dorsalis. Scientific Reports 5, 9470.Google Scholar
Augustinos, A.A., Drosopoulou, E., Gariou-Papalexiou, A., Asimakis, E.D., Cáceres, C., Tsiamis, G., Bourtzis, K., Mavragani-Tsipidou, P. & Zacharopoulou, A. (2015) Cytogenetic and symbiont analysis of five members of the B. dorsalis complex (Diptera, Tephritidae): no evidence of chromosomal or symbiont-based speciation events. Zookeys 540, 273–298.Google Scholar
Baerwald, R.J. & Boush, G.M. (1968) Demonstration of the bacterial symbiote Pseudomonas melophthora in the apple maggot, Rhagoletis pomonella, by fluorescent-antibody technique. Journal of Invertebrate Pathology 11(2), 251–259.Google Scholar
Baker, A.C., Stone, W.E., Plummer, C.C. & McPhail, M. (1944) A review of studies on the Mexican fruit fly and related Mexican species. Miscellaneous Publications, United States Department of Agriculture 531, 1–155.Google Scholar
Barclay, H.J. (1987) Models for pest control: complementary effects of periodic releases of sterile pests and parasitoids. Theoretical Population Biology 32, 76–89.Google Scholar
Baumann, P. (2005) Biology of bacteriocyte-associated endosymbionts of plant sap-sucking insects. Annual. Review of Microbiology 59, 155–189, 10.1146/annurev. micro.59.030804.121041.Google Scholar
Behar, A., Yuval, B. & Jurkevitch, E. (2005) Enterobacteria mediated nitrogen fixation in natural populations of the fruit fly, Ceratitis capitata. Molecular Ecology 14, 2637–2643.Google Scholar
Behar, A., Jurkevitch, E. & Yuval, B. (2008) Bringing back the fruit into fruit fly–bacteria interactions. Molecular Ecology 17, 1375–1386, 10.1111/j.1365-294X. 2008.03674.x.Google Scholar
Behar, A., Ben-Yosef, M., Lauzon, C.R., Yuval, B. & Jurkevich, E. (2009) Structure and function of the bacterial community associated with the Mediterranean fruit fly. pp. 251–271 in Bourtzis, K. & Miller, T.A. (Eds) Insect symbiosis. Boca Raton, FL, CRC Press.Google Scholar
Belcari, A. & Bobbio, E. (1999) The use of copper in the control of the olive fly, Bactrocera oleae. L'impiego del rame nel controllo della mosca delle olive, Bactrocera oleae. Informatore Fitopatologico 49(12), 52–55.Google Scholar
Belcari, A., Sacchetti, P., Marchi, G. & Surico, G. (2003) The olive fly and associated bacteria. Informatics Fitopatologia 53, 55–59.Google Scholar
Ben Ami, E., Yuval, B. & Jurkevitch, E. (2010) Manipulation of the microbiota of mass-reared Mediterranean fruit flies Ceratitis capitata (Diptera: Tephritidiae) improves sterile male sexual performance. Journal of International Society and Microbial Ecology 4, 28–37.Google Scholar
Ben-Yosef, M., Pasternak, Z., Jurkevitch, E. & Yuval, B. (2015) Symbiotic bacteria enable olive fly larvae to overcome host defences. Royal Society Open Science 2, 150170, 10.1098/ rsos. 150170.Google Scholar
Bergey, D.H., Holt, J.G. & Krieg, N.R. (2001) Bergey's Manual of Systematic Bacteriology. Baltimore, Williams and Wilkins.Google Scholar
Bian, G.W., Joshi, D., Dong, Y.M., Lu, P., Zhou, G.L., Pan, X.L., Xu, Y., Dimopoulos, G. & Xi, Z.Y. (2013) Wolbachia invades Anopheles stephensi populations and induces refractoriness to plasmodium infection. Science 340, 748–750.Google Scholar
Bloem, S., Bloem, K.A. & Knight, A.L. (1998) Oviposition by sterile codling moths, Cydia pomonella (Lepidoptera: Tortricidae) and control of wild populations with combined releases of sterile moths and egg parasitoids. Journal of the Entomological Society of British Columbia 95, 99–109.Google Scholar
Bourtzis, K., Nirgianaki, A., Onyango, P. & Savakis, C.A. (1994) Prokaryotic dnaA sequence in Drosophila melanogaster: Wolbachia infection and cytoplasmic incompatibility among laboratory strains. Insect Molecular Biology 3, 131–142.Google Scholar
Brauman, A., Dore, J., Eggleton, P., Bignell, D., Breznak, J.A. & Kane, M.D. (2001) Molecular phylogenetic profiling of prokaryotic communities in guts of termites with different feeding habits. FEMS Microbiology Ecology 35, 27–36.Google Scholar
Broderick, N.A., Raffa, K.F., Goodman, R.M. & Handelsman, J. (2004) Census of the bacterial community of the gypsy moth larval midgut by using culturing and culture-independent methods. Applied and Environmental Microbiology 70, 293–300.Google Scholar
Brune, A. (1998) Termite guts: the world's smallest bioreactors. Trends in Biotechnology 16, 16–21.Google Scholar
Capuzzo, C., Firrao, G., Mazzon, L., Squartini, A. & Girolami, V. (2005) ‘Candidatus Erwinia dacicola’, a coevolved symbiotic bacterium of the olive fly Bactrocera oleae (Gmelin). International Journal of Systematic Evolutionary Microbiology 55, 1641–1647.Google Scholar
Cayol, J.P., Causse, R., Louis, C. & Barthes, J. (1994) Medfly Ceratitis capitata Wiedemann (Diptera: Trypetidae) as a rot vector in laboratory conditions. Journal of Applied Entomology 117, 338–343.Google Scholar
Cheng, D., Guo, Z., Riegler, M., Xi, Z., Liang, G. & Xu, Y. (2017) Gut symbiont enhances insecticide resistance in a significant pest, the oriental fruit fly Bactrocera dorsalis (Hendel). Microbiome 5, 13, 10.1186/s40168-017-0236.Google Scholar
Chinnarajan, A.M., Jayaraj, S. & Narayanan, K. (1972) Destruction of endo symbionts with oxytetracycline and sulfanilamide in the gourd fruit fly Dacus-cucurbitae trypetidae diptera. Hindustan Antibiotics Bulletin 15(1–2), 16–22.Google Scholar
Cicero, L., Sivinski, J. & Aluja, M. (2012) Effect of host diet and adult parasitoid diet on egg load dynamics and egg size of braconid parasitoids attacking Anastrepha ludens. Physiological Entomology 37, 177–184.Google Scholar
Colman, D.R., Toolson, E.C. & Takacs, V.C.D. (2012) Do diet and taxonomy influence insect gut bacterial communities? Molecular Ecology 21, 5124–5137.Google Scholar
Cox, C.R. & Gilmore, M.S. (2007) Native microbial colonization of Drosophila melanogaster and its use as a model of Enterococcus faecalis pathogenesis. Infection and Immunity 75, 1565–1576.Google Scholar
Crotti, E., Rizzi, A., Chouaia, B., Ricci, I., Favia, G., Alma, A., Sacchi, L., Bourtzis, K., Mandrioli, M., Cherif, A., Bandi, C. & Daffonchio, D. (2010) Acetic acid bacteria, newly emerging symbionts of insects. Applied and Environmental Microbiology 76, 6963–6970.Google Scholar
Dale, C. & Moran, N.A. (2006) Molecular interactions between bacterial symbionts and their hosts. Cell 126, 453–465.Google Scholar
Damodaram, K.J.P., Ayyasamy, A. & Kempraj, V. (2016) Commensal Bacteria Aid Mate-selection in the Fruit Fly, Bactrocera dorsalis. Microbial Ecology 72, 725–729. DOI 10.1007/s00248-016-0819-4.Google Scholar
DeMilo, A.B., Lee, C.J., Moreno, D.S. & Martinez, A.J. (1996) Identification of volatiles derived from Citrobacter freundii fermentation of a trypticase soy broth. Journal of Agriculture and Food Chemistry 44, 607–612.Google Scholar
de Vries, E.J., Jacobs, G. & Breeuwer, J.A.J. (2001) Transmission of Gut Bacteria in the Western Flower Thrips, Frankliniella occidentalis. Journal of Invertebrate Pathology 77, 129–137, 10.1006/jipa.2001.5010.Google Scholar
Douglas, A.E. (1998) Nutritional interactions in insect–microbial symbioses: aphids and their symbiotic bacteria Buchnera. Annual Review of Entomology 43, 17–37, 10.1146/ annurev.ento.43.1.17.Google Scholar
Douglas, A.E., Minto, L.B. & Wilkinson, T.L. (2001) Quantifying nutrient production by the microbial symbionts in an aphid. Journal of Experimental Biology 204, 349–358.Google Scholar
Drew, R.A.I. (1987) Behavioral strategies of fruit flies of the genus Dacus (diptera: Tephritidae) significant in mating and host-plant relationships. Bulletin of Entomological Research 77, 73–81.Google Scholar
Drew, R.A.I. & Fay, H.A.C. (1988) Comparison of the roles of ammonia and bacteria in the attraction of Dacus tryoni (Froggatt) (Queensland fruit fly) to proteinaceous suspensions. Journal of Plant Protection in the Tropics 5(2), 127–130.Google Scholar
Drew, R.A.I & Lloyd, A.C. (1987) Relationship of fruit flies (Diptera: Tephritidae) and their Bacteria to host plants. Annals of the Entomological Society of America 80(5), 629–636. https://doi.org/10.1093/aesa/80.5.629Google Scholar
Drew, R.A.I. & Lloyd, A.C. (1991) Bacteria in the life cycle of tephritid fruit flies. pp. 441–465 in Barbosa, P., Krischik, V.A. & Jones, C.G. (Eds) Microbial Mediation of Plant–Herbivore Interactions New York, NY, Wiley and Sons.Google Scholar
Drew, R.A.I., Courtice, A.C. & Teakle, D.S. (1983) Bacteria as a natural source of food for adult fruit flies (Diptera: Tephritidae). Oecoiogia (Berlin) 60, 279–284.Google Scholar
Eben, A., Benrey, B., Sivinski, J. & Aluja, M. (2000) Host species and host plant effects on preference and performance of Diachasmimorpha longicaudata (Hymenoptera: Braconidae). Environmental Entomology 29, 87–94.Google Scholar
Egert, M., Stingl, U., Bruun, L.D., Pommerenke, B., Brune, A. & Friedrich, M.W. (2005) Structure and topology of microbial communities in the major gut compartments of Melolontha melolontha larvae (Coleoptera: Scarabaeidae). Applied and Environmental Microbiology 71, 4556–4566.Google Scholar
Epsky, N.D., Heath, R.H., Dueben, B.D., Lauzon, C.R., Proveaux, A.T. & Maccollom, G.B. (1998) Attraction of 3-methyl-l-butanol and ammonia identified from Enterobacter agglomerans to Anastrepha suspensa. Journal of Chemical Ecology 24(11), 1867–1880.Google Scholar
Eutick, M.L., O'Brien, R.W. & Slaytor, M. (1978) Bacteria from the gut of Australian termites. Applied and Environmental Microbiology 35(5), 823–828.Google Scholar
Fletcher, B.S. (1987) The biology of dacine fruit flies. Annual Review of Entomology 32, 115–144.Google Scholar
Fukatsu, T. & Hosokawa, T. (2002) Capsule transmitted gut symbiotic bacterium of the Japanese common plataspid stinkbug, Megacopta punctatissima. Applied and Environmental Microbiology 68(1), 389–396.Google Scholar
Fytizas, E. & Tzanakakis, M.E. (1966a) Some effects of streptomycin, when added to the adult food, on the adults of Dacus oleae (Diptera: Tephritidae) and their progeny. Annals of the Entomological Society of America 59(2), 269–273. https://doi.org/10.1093/aesa/59.2.269Google Scholar
Fytizas, E. & Tzanakakis, M.E. (1966b) Development of Dacus oleae Larvae in olives after addition of streptomycin to food of their parents. Annales Des Epiphyties 17(1), 53.Google Scholar
Gavriel, S., Gazit, Y., Jurkevitch, E. & Yuval, B. (2011) Bacterially enriched diet improves sexual performance of sterile male Mediterranean fruit flies. Journal of Applied Entomology 135, 564–573.Google Scholar
Girolami, V. (1973) Morphological histological findings on the bacterio symbiosis of Dacus oleae and other tephritids in field and artificial media rearing. Redia 54, 269–294.Google Scholar
Girolami, V. (1983) Fruit Fly Symbiosis and Adult Survival General Aspects. Cavalloro, r. (ed.). Fruit flies of economic importance; proceedings of the CEC/IOBC international symposium, Athens, Greece, Nov. 16–19, 1982. Xii+642p. A. A. A. Balkema: Rotterdam, Netherlands (dist. By mbs: salem, n.h., USA). Illus. 74–76.Google Scholar
Gow, P.L. (1954) Proteinaceous bait for the oriental fruit Fly. Journal of Economic Entomology 47(1), 153–160. https://doi.org/10.1093/jee/47.1.153Google Scholar
Greany, P.D. (1989) Host plant resistance to tephritids: an under-exploited control strategy. pp. 353–362 in Robinson, A.S. & Hooper, G. (Eds) Fruit Flies: Their Biology, Natural Enemies and Control. Amsterdam, The Netherlands, Elsevier.Google Scholar
Guo, Z.J., Lu, Y.Y., Yang, F., Zeng, L., Liang, G.W. & Xu, Y.J. (2017) Transmission modes of a pesticide-degrading symbiont of the oriental fruit fly Bactrocera dorsalis (Hendel). Applied Microbiology and Biotechnology 101, 8543–8556.Google Scholar
Gupta, M., Pant, N.C. & Lal, B.S. (1982a) Symbiotes of Dacus cucurbitae (Coquillette) 1. Location and nature of association. Indian Journal of Entomology 44(4), 325–330.Google Scholar
Gupta, M., Pant, N.C. & Lal, B.S. (1982b) Symbiotes of Dacus cucurbitae (Coquillette) 3. Transmission. Indian Journal of Entomology 44(4), 337–343.Google Scholar
Hadapad, A.B., Prabhakar, C.S., Chandekar, S.C., Tripathi, J. & Hire, R.S. (2016) Diversity of bacterial communities in the midgut of Bactrocera cucurbitae (Diptera: Tephritidae) populations and their potential use as attractants. Pest Management Science 72, 1222–1230, 10.1002/ps.4102.Google Scholar
Haniotakis, G.E. (2005) Olive pest control: present status and prospects. IOBC/WPRS Bulletin 28, 1–9.Google Scholar
Haynes, S., Darby, A.C., Daniell, T.J., Webster, G., van Veen, F.J.F., Godfray, H.C.J., Prosser, J.I. & Douglas, A.E. (2003) Diversity of bacteria associated with natural aphid populations. Applied and Environmental Microbiology 69, 7216–7223.Google Scholar
He, M., Jiang, J. & Cheng, D. (2017) The plant pathogen Gluconobacter cerinus strain CDF1 is beneficial to the fruit fly Bactrocera dorsalis. AMB Express 7, 207, 10.1186/s13568-017-0514-y.Google Scholar
Head, I.M., Saunders, J.R. & Piclup, R.W. (1998) Microbiological evolution, diversity and ecology: a decade of ribosomal RNA analysis of uncultivated microorganisms. Microbial Ecology 35, 1–21.Google Scholar
Hoffmeister, T.S. & Gienapp, P. (1999) Exploitation of the host's chemical communication in a parasitoid searching for concealed host larvae. Ethology 105, 223–232.Google Scholar
Howard, D.J., Bush, G.L. & Breznak, (1985) The evolutionary significance of bacteria associated with Ragoletis. Evaluation 39, 405–417.Google Scholar
Jamnongluk, W., Kittayapong, P., Baimai, V. & O'Neill, S.L. (2002) Wolbachia infections of tephritid fruit flies: molecular evidence for five distinct strains in a single host species. Current microbiology 45, 255–260, 10.1007/s00284-002-3746-1.Google Scholar
Jang, E.B. & Nishijima, K.A. (1990) Identification and attractancy of bacteria associated with Dacus dorsalis (Diptera: Tephritidae). Environmental Entomology 19(6), 1726–1731, 10.1093/ee/19.6.1726.Google Scholar
Janisiewicz, W.J., Conway, W.S., Brown, M.W., Sapers, G.M., Fratamico, P. & Buchanan, R.L. (1999) Fate of Escherichia coli O157:h7 on fresh cut apple tissue and its potential for transmission by fruit flies. Applied and Environmental Microbiology 65, 1–5.Google Scholar
Joachim-Bravo, I.S., Fernandes, O.A., Bortoli, S.R.A. & Zucoloto, F.S. (2001) Oviposition behavior of Ceratitis capitata Wiedemann (Diptera: Tephritidae): association between oviposition preference and larval performance in individual females. Neotropical Entomology 30, 559–564.Google Scholar
Kakani, E.G., Zygouridis, N.E., Tsoumani, K.T., Seraphides, N., Zalom, F.G. & Mathiopoulos, K.D. (2010) Spinosad resistance development in wild olive fruit fly Bactrocera oleae (Diptera: Tephritidae) populations in California. Pest Management Science 66, 447–453.Google Scholar
Khaeso, K., Andongma, A.A., Akami, M., Souliyanonh, B., Zhu, J., Krutmuang, P. & Niu, C.Y. (2018) Assessing the effects of gut bacteria manipulation on the development of the oriental fruit fly, Bactrocera dorsalis (Diptera; Tephritidae). Symbiosis 74, 97–105, 10.1007/s13199-017-0493-4.Google Scholar
Khan, M., Mahin, A.A., Pramanik, M.K. & Akter, H. (2014) Identification of gut bacterial community and their effect on the fecundity of pumpkin fly, Bactrocera tau (Walker). Journal of Entomology 11(2), 68–77, 10.3923/je.2014.68.77.Google Scholar
Kittayapong, P., Milne, J.R., Tigvattananont, S. & Baimai, V. (2000) Distribution of the reproduction-modifying bacteria, Wolbachia, in natural populations of tephritids fruit flies in Thailand. Science Asia 26, 93–103.Google Scholar
Kounatidis, I., Crotti, E., Sapountzis, P., Sacchi, L., Rizzi, A., Chouaia, B. et al. (2009) Acetobacter tropicalis is a major symbiont of the olive fruit fly (Bactrocera oleae). Applied and Environmental Microbiology 75, 3281–3288.Google Scholar
Kuzina, L.V., Peloquin, J.J., Vacek, D.C. & Miller, T.A. (2001) Isolation and identification of bacteria associated with adult laboratory Mexican fruit flies, Anastrepha ludens (Diptera: Tephritidae). Current Microbiology 42, 290–294.Google Scholar
Lauzon, C.R. (2003) Symbiotic relationships of tephritids. pp. 115–130 in Bourtzis, K. & Miller, T.A. (Eds) Insect Symbiosis. Boca Raton, FL, CRC Press.Google Scholar
Lauzon, C.R., Sjogren, R.E. & Prokopy, R.J. (2000) Enzymatic capabilities of bacteria associated with apple maggot flies, a postulated role in attraction. Journal of Chemical Ecology 26, 953–967.Google Scholar
Lee, C.J., Demilo, A.B., Moreno, D.S. & Martinez, A.J. (1995) Analyses of the volatile components of a bacterial fermentation that is attractive to the Mexican fruit fly, Anastrepha ludens. Journal of Agricultural and Food Chemistry 43, 1348–1351.Google Scholar
Lemos, L.D.N., Adaime, R., De Jesus-Barros, C.R. & De Deus, E.D.G. (2014) New hosts of Bactrocera carambolae (Diptera: tephritidae) in Brazil. Florida Entomologist 97(2), 841–843.Google Scholar
Leroy, P.D., Sabri, A., Heuskin, S., Thonart, P., Lognay, G. et al. (2011) Microorganisms from aphid honeydew attract and enhance the efficacy of natural enemies. Nature Communications 2, 348.Google Scholar
Li, Z.H., Jiang, F., Ma, X.L., Fang, Y., Sun, Z.Z., Qin, Y.J. & Wang, Q.L. (2013) Review on prevention and control techniques of Tephritidae invasion. Plant Quarantine 27, 1–10.Google Scholar
Liscia, A., Angioni, P., Sacchetti, P., Poddighe, S., Granchietti, A., Setzu, M.D. et al. (2013) Characterization of olfactory sensilla of the olive fly: behavioral and electrophysiological responses to volatile organic compounds from the host plant and bacterial filtrate. Journal of Insect Physiology 59, 705–716.Google Scholar
Liu, L.J., Martinez-Sañudo, I., Mazzon, L., Prabhakar, C.S., Girolami, V., Deng, Y.L., Dail, Y. & Li, Z.H. (2016) Bacterial communities associated with invasive populations of Bactrocera dorsalis (Diptera: Tephritidae) in China. Bulletin of Entomological Research 106, 718–728, 10.1017/S0007485316000390.Google Scholar
Liu, S.H., Chen, Y., Li, W., Tang, G.H., Yang, Y., Jiang, H.B., Dou, W. & Wang, J.J. (2018). Diversity of bacterial communities in the intestinal tracts of Two geographically distant populations of Bactrocera dorsalis (Diptera: Tephritidae). Journal of Economic Entomology 111(6), 2861–2868. doi: 10.1093/jee/toy231.Google Scholar
Lloyd, A.C., Drew, R.A.I., Teakle, D.S. & Hayward, A.C. (1986) Bacteria associated with some Dacus species (Diptera: Tephritidae) and their host fruits in Queensland. Australian Journal of Biological Sciences 39, 361–368.Google Scholar
Louradour, I., Monteiro, C.C., Inbar, E. et al. (2017) The midgut microbiota plays an essential role in sand fly vector competence for Leishmania major. Cellular Microbiology 19, e12755, doi: 10.1111/cmi.12755.Google Scholar
Luo, M., Zhang, H., Du, Y., Idrees, A., He, L., Chena, J. & Jia, Q. (2018) Molecular identification of cultivable bacteria in the gut of adult Bactrocera tau (Walker) and their trapping effect. Pest Management Science 74, 2842–2850.Google Scholar
MacCollom, G., Lauzon, C., Sjogren, R., Meyer, W. & Olday, F. (2009) Association and attraction of blueberry maggot fly (Diptera: Tephritidae) to Pantoea (enterobacter) agglomerans. Environmental Entomology 38, 116–120.Google Scholar
Malacrinò, A., Campolo, O., Medina, R.F. & Palmeri, V. (2018) Instar- and host-associated differentiation of bacterial communities in the Mediterranean fruit fly Ceratitis capitata. Plos One 13(3), e0194131.Google Scholar
Marchini, D., Rosetto, M., Dallai, R. & Marri, L. (2002) Bacteria associated with the oesophageal bulb of the medfly Ceratitis capitata (Diptera: Tephritidae). Current Microbiology 44, 120–124.Google Scholar
Martinez-Sañudo, I. (2009) Phylogenetic studies of tephritid flies (Diptera, Tephritidae) and their symbiotic bacteria. PhD Thesis, University of Padova, Padova, Italy.Google Scholar
Messina, F.J. & Jones, V.P. (1990) Relationship between fruit phenology and infestation by the apple maggot (Diptera: Tephritidae) in Utah. Annals of the Entomological Society of America 83, 742–752, doi: 10.1093/aesa/83.4.74.2.Google Scholar
Michael, B.Y., Jurkevitch, E. & Yuval, B. (2008) Effect of bacteria on nutritional status and reproductive success of the Mediterranean fruit fly Ceratitis capitata. Physiological Entomology 33(2), 145–154.Google Scholar
Miyata, R., Noda, N., Tamaki, H., Kinjyo, K., Aoyagi, H., Uchiyama, H. & Tanaka, H. (2007) Influence of feed components on symbiotic bacterial community structure in the gut of the wood-feeding higher termite Nasutitermes takasagoensis. Bioscience Biotechnology and Biochemistry 71, 1244–1251.Google Scholar
Moran, N.A., Degnan, P.H., Santos, S.R., Dunbar, H.E. & Ochman, H. (2005) The players in a mutualistic symbiosis: insects, bacteria, viruses, and virulence genes. Proceedings of the National Academy of Sciences, USA 102, 16919–16926.Google Scholar
Moran, N.A., McCutcheon, J.P. & Nakabachi, A. (2008) Genomics and evolution of heritable bacterial symbionts. Annual Review of Genetics 42, 165–190.Google Scholar
Morrow, J.L., Frommer, M., Royer, J.E., Shearman, D.C.A. & Riegler, M. (2015) Wolbachia pseudogenes and low prevalence infections in tropical but not temperate Australian tephritids fruit flies: manifestations of lateral gene transfer and endosymbiont spillover? BMC Evolutionary Biology 15, 202–218.Google Scholar
Naaz, N., Choudhary, J.S., Prabhakar, C.S., Moanaro, & Maurya, S. (2016) Identification and evaluation of cultivable gut bacteria associated with peach fruit fly, Bactrocera zonata (Diptera: Tephritidae). Phytoparasitica 44, 165–176. DOI 10.1007/s12600-016-0518-1.Google Scholar
Nakajima, H., Hongoh, Y., Usami, R., Kudo, T. & Ohkuma, M. (2005) Spatial distribution of bacterial phylotypes in the gut of the termite Reticulitermes speratus and the bacterial community colonizing the gut epithelium. FEMS Microbiology Ecology 54, 247–255.Google Scholar
Narit, T. & Anuchit, C. (2011) Attraction of Bactrocera cucurbitae and B. papayae (diptera: Tephritidae) to the odor of the bacterium Enterobacter cloacae. The Philippine Agricultural Scientist 94, 1–6.Google Scholar
Niyazi, N., Lauzon, C.R. & Shelly, T.E. (2004) Effect of probiotic adult diets on fitness components of Sterile male mediterranean fruit flies (Diptera: Tephritidae) under laboratory and field cage conditions. Journal Economic Entomology 97(5), 1570–1580.Google Scholar
Oliver, K.M., Russell, J.A., Moran, N.A. & Hunter, M.S. (2003) Facultative bacterial symbionts in aphids confer resistance to parasitic wasps. Proceedings of the National Academy of Sciences of the United States of America 100, 1803–1807.Google Scholar
Oliver, K.M., Moran, N.A. & Hunter, M.S. (2005) Variation in resistance to parasitism in aphids is due to symbionts not host genotype. Proceedings of the National Academy of Sciences of the United States of America 102(36), 12647–12648, doi: 10.1073/iti3605102.Google Scholar
Oliver, K.M., Smith, A.H. & Russell, J.A. (2014) Defensive symbiosis in the real world - advancing ecological studies of heritable, protective bacteria in aphids and beyond. Functional Ecology 28, 341–355.Google Scholar
Paredes, J.C., Herren, J.K., Schupfer, F. & Lemaitre, B. (2016) The role of lipid competition for endosymbiont-mediated protection against parasitoid wasps in Drosophila. American Society for Microbiology 7(4), e01006–e01016.Google Scholar
Pavlidi, N., Giotil, A., Wybouw, N., Dermauw, W., Ben-Yosef, M., Yuval, B., Jurkevich, E., Kampouraki, A., Leeuwen, T.V. & Vontas, J. (2017) Transcriptomic responses of the olive fruit fly Bactrocera oleae and its symbiont Candidatus Erwinia dacicola to olive feeding. Scientific Reports 7, 42633, doi: 10.1038/srep42633.Google Scholar
Perry, A.S., Yamamoto, I., Ishaaya., I. & Perry, R. (1998) Toxicology of insecticides. p. 11 in Insecticides in Agriculture and Environment. Berlin, Heidelberg, Springer.Google Scholar
Petri, L. (1909) Ricerche Sopra i Batteri Intestinali della Mosca Olearia. Roma, Memorie della Regia Stazione di Patologia Vegetale di Roma.Google Scholar
Petri, L. (1910) Untersuchung uber die darmbakterien der olivenfliege. Zentbl. Bakteriolog 26, 357–367.Google Scholar
Prabhakar, C.S., Sood, P., Kapoor, V., Kanwar, S.S., Mehta, P.K. & Sharma, P.N. (2009a) Molecular and biochemical characterization of three bacterial symbionts of fruit fly, Bactrocera tau (Tephritidae: Diptera). Journal of General and Applied Microbiology 55, 213–220.Google Scholar
Prabhakar, C.S., Sood, P., Mehta, P.K. & Choudhary, A. (2009b) Distribution and developmental biology of fruit flies infesting cucurbits in north-western Himalaya. Journal of Insect Science 22, 300–308.Google Scholar
Prabhakar, C.S., Sood, P., Kanwar, S.S., Sharma, P.N., Kumar, A. & Mehta, P.K. (2013) Isolation and characterization of gut bacteria of fruit fly, Bactrocera tau (Walker). Phytoparasitica 41, 193–201.Google Scholar
Prezotto, L.F., Perondini, A.L.P., Hernandez-Ortiz, , Marino, C.L. & Selivon, D. (2017) Wolbachia strains in cryptic species of the Anastrepha fraterculus complex (Diptera, Tephritidae) along the Neotropical Region. Syst Applied Microbiology 40, 59–67.Google Scholar
Qin, Y., Paini, D.R., Wang, C., Fang, Y. & Li, Z.H. (2015) Global establishment risk of economically important fruit fly species (Tephritidae). PLoS ONE 10(1), e0116424, doi: 10.1371/journal.pone.0116424.Google Scholar
Raghu, S., Clarke, A.R. & Bradley, J. (2002) Microbial mediation of fruit fly-host plant interactions: is the host plant the “Bcentre of activity”? Oikos 97, 319–328.Google Scholar
Rani, A., Sharm, A., Rajagopal, R., Adak, T. & Bhatnagar, R.K. (2009) Bacterial diversity analysis of larvae and adult midgut microflora using culture-dependent and culture-independent methods in lab-reared and field-collected Anopheles stephensi-an Asian malarial vector. BMC Microbiology 9, 96.Google Scholar
Ras, E., Leo, W., Beukeboom, , Caceres, C. & Bourtzis, K. (2017) Review of the role of gut microbiota in mass rearing of the olive fruit fly, Bactrocera oleae, and its parasitoids. Entomologia Experimentalis et Applicata 164(3), 237–256. DOI: 10.1111/eea.12609.Google Scholar
Rattanapun, W., Amornsak, W. & Clarke, A.R. (2009) Bactrocera dorsalis preference for and performance on two mango varieties at three stages of ripeness. Entomologia Exprementalis ET Appllicata 131, 243–253, doi: 10.1111/j.1570-7458.2009.00850.x.Google Scholar
Reddy, K., Sharma, K. & Singh, S. (2014) Attractancy potential of cultivable bacteria from the gut of peach fruit fly, Bactrocera zonata (Saunders). Phytoparasitica 42, 691–698. doi: 10.1007/s12600-014-0410-9.Google Scholar
Robacker, D.C. (2007) Chemical ecology of bacteria relationships with fruit flies, Integrated Protection of Olive Crops. IOBC/WPRS Bulletin 30, 9–22.Google Scholar
Robacker, D.C. & Flath, R.A. (1995) Attractants from staphylococcus Aureus cultures for Mexican fruit fly, Anastrepha ludens. Journal of Chemical Ecology 21, 1861, doi: 10.1007/BF02033682.Google Scholar
Robacker, D.C. & Lauzon, C.R. (2002) Purine metabolizing capability of Enterobacter agglomerans affects volatiles production and attractiveness to Mexican fruit fly. Journal of Chemical Ecology 28, 1549–1563.Google Scholar
Robacker, D.C., Martinez, A.J., Garcia, J.A. & Bartelt, R.J. (1998) Volatiles attractive to the Mexican fruit fly (Diptera: Tephritidae) from 11 bacteria taxa. Florida Entomologist 81, 497–509.Google Scholar
Robacker, D.C., Lauzon, C.R. & HE, X. (2004) Volatiles production and attractiveness to the Mexican fruit fly of Enterobacter Agglomerans isolated from apple maggot and Mexican fruit flies. Journal of Chemical Ecology 30(7), 1329–1347.Google Scholar
Robertson, B.K. & Alexander, M. (1994) Growth-linked and co-metabolic biodegradation: possible reason for occurrence or absence of accelerated pesticide biodegradation. Pesticide Science 41(4), 311–318.Google Scholar
Rossiter, M.C., Howard, D.J. & Bush, G.L. (1983) Fruit flies of economic importance; proceedings of the CEC/IOBCc/iobc international symposium, Athens, Greece, Nov. 16–19, 1982. Xii+642p. A. A. A. Balkema: Rotterdam, Netherlands (dist. By mbs: salem, n.h., USA). Illus. 77–84.Google Scholar
Sacchetti, P., Granchietti, A., Landini, S., Viti, L., Giovannetti, L. & Belcari, A. (2008) Relationships between the olive fly and bacteria. Journal Applied Entomology 132, 682–689.Google Scholar
Schmid, M., Sieber, R., Zimmermann, Y.S. & Vorburger, C. (2012) Development, specificity and sub lethal effects of symbiont conferred resistance to parasitoids in aphids. Functional Ecology 26, 207–215.Google Scholar
Schuler, H., Bertheau, C., Egan, S.P., Feder, J.L., Riegler, M., Schlick-Steiner, B.C., Steiner, F.M., Johannesen, J., Kern, P. & Tuba, K. (2013) Evidence for a recent horizontal transmission and spatial spread of Wolbachia from endemic Rhagoletis cerasi (Diptera: Tephritidae) to invasive Rhagoletis cingulata in Europe. Molecular Ecology 22, 4101–4111.Google Scholar
Sela, S., Nestel, D., Pinto, R., Lavy, E.N. & Joseph, M.B. (2005) Mediterranean fruit fly as a Potential Vector of Bacterial Pathogens. Applied and Environmental Microbiology 71(7), 4052–4056, doi: 10.1128/AEM.71.7.4052–4056.2005.Google Scholar
Shi, Z., Wang, L. & Zhang, H. (2012) Low diversity bacterial community and the trapping activity of metabolites from cultivable bacteria species in the female reproductive system of the oriental fruit fly, Bactrocera dorsalis Hendel (Diptera: Tephritidae). International Journal of Molecular Sciences 13, 6266–6278.Google Scholar
Sonia Rodríguez-Cruz, M., Jones, J.E. & Bending, G.D. (2006) Field-scale study of the variability in pesticide biodegradation with soil depth and its relationship with soil characteristics. Soil Biology and Biochemistry 38(9), 2910–2918.Google Scholar
Sood, P. & Nath, A. (2002) Bacteria associated with Bactrocera sp. (Diptera: Tephritidae) – isolation and identification. Pest Management and Economic Zoology 10, 1–9.Google Scholar
Sood, P. & Nath, A. (2005) Colonization of marker strains of bacteria in fruit fly, Bactrocera tau. The Indian Journal of Agricultural Research 39, 103–109.Google Scholar
Sood, P. & Prabhakar, C.S. (2009) Molecular diversity and antibiotic sensitivity of gut bacterial symbionts of fruit fly, Bactrocera tau Walker. Journal of Biological Control 23(3), 213–220.Google Scholar
Sood, P., Prabhakar, C.S. & Mehta, P.K. (2010) Eco-friendly management of fruit flies through their gut bacteria. Journal of Insect Science 23, 275–283.Google Scholar
Stammer, H.J. (1929) Die bakteriensymbiose der trypetiden (Diptera). Zeitschrift für Morphologie und Ökologie der Tiere 15(3), 481–523.Google Scholar
Stouthamer, R., Breeuwer, J.A.J. & Hurst, G.D.D. (1999) Wolbachia pipientis: microbial manipulator of arthropod reproduction. Annual Review of Microbiology 53, 71–102.Google Scholar
Sun, X., Cui, L.W. & Li, Z.H. (2007) Diversity and Phylogeny of Wolbachia infecting Bactrocera dorsalis (Diptera: Tephritidae) populations from China. Environmental Entomology 36, 1283–1289.Google Scholar
Thaochan, N., Drew, R.A.I., Hughes, J.M., Vijaysegaran, S. & Chinajariyawong, A. (2010) Alimentary tract bacteria isolated and identified with API- 20E and molecular cloning techniques from Australian tropical fruit flies, Bactrocera cacuminata and B. tryoni. Journal of Insect Science 10, 131.Google Scholar
Thaochan, N., Drew, R.A.I., Chinajariyawong, A., Sunpapao, A. & Pornsuriya, C. (2015) Gut bacterial community structure of two Australian tropical fruit fly species (Diptera: Tephritidae). Songklanakarin Journal of Science and Technology 37(6), 617–624.Google Scholar
Thibout, E., Guillot, J.F. & Auger, J. (1993) Microorganisms are involved in the production of volatile kairomones affecting the host seeking behaviour of Diadromus pulchellus, a parasitoid of Acrolepiopsis assectella. Physiological Entomology 18, 176–182.Google Scholar
Toth, E., Kovacs, G., Schumann, P., Kovacs, A.L. & Steiner, U. (2001) Shineria larvae gen. nov. Isolated from the 1st and 2nd larval stages of Wohlfahrtia magnifica (Diptera: Sarcophagidae). International Journal of Systematic Evolution and Microbiology 51, 401–407.Google Scholar
Tsiropoulos, G.J. (1976) Bacteria associated with the Walnut Husk Fly, Rhagoletis completa. Environmental Entomology 5(1), 83–86, doi: 10.1093/ee/5.1.83.Google Scholar
Van Houdt, J.K.J., Breman, F.C., Virgilio, M. & Meyer, M.D. (2010) Recovering full DNA barcodes from natural history collections of Tephritids fruit flies (Tephritidae, Diptera) using mini barcodes. Molecular Ecology Resources 10, 459–465.Google Scholar
Ventura, C., Briones-Roblero, C.I., Briones-Roblero, E., Rivera-Orduña, F.N. & Zúñiga, G. (2018) Comparative analysis of the gut bacterial community of four Anastrepha fruit flies (Diptera: Tephritidae) based on pyrosequencing. Current Microbiology 75(8), 966–976. DOI.org/10.1007/s00284-018-1473-5.Google Scholar
Vorburger, C., Gehrer, L. & Rodriguez, P. (2010) A strain of the bacterial symbiont Regiella insecticola protects aphids against parasitoids. Biology Letters 6, 109–111.Google Scholar
Waleron, M., Waleron, K., Podhajska, A.J. & Lojkowska, E. (2002) Genotyping of bacteria belonging to the former Erwinia genus by PCR–RFLP analysis of a recA gene fragment. Microbiology (Reading, England) 148, 583–595.Google Scholar
Wang, H., Jin, L., Peng, T., Zhang, H., Chen, Q. & Hua, Y. (2013) Identification of cultivable bacteria in the intestinal tract of Bactrocera dorsalis from three different populations and determination of their attractive potential. Pest Management Science 70, 80–87.Google Scholar
Wang, H., Jin, L. & Zhang, H. (2011) Comparison of the diversity of the bacterial communities in the intestinal tract of adult Bactrocera dorsalis from three different populations. Journal of Applied Microbiology 110, 1390–1401.Google Scholar
Wang, A., Yao, Z., Zheng, W. & Zhang, H. (2014) Bacterial communities in the gut and reproductive organs of Bactrocera minax (Diptera: Tephritidae) based on 454 pyrosequencing. PLoS ONE 9(9), e106988. DOI: 10.1371/journal.pone.0106988.Google Scholar
Wernegreen, J.J. (2002) Genome evolution in bacterial endosymbionts of insects. Nature Reviews Genetics 3(11), 850–861, doi: 10.1038/nrg931.Google Scholar
Xie, J.C., Winter, L., Winter, C. & Mateos, M. (2015) Rapid spread of the defensive endosymbiont Spiroplasma in Drosophila hydei under high parasitoid wasp pressure. FEMS Microbiology Ecology 91, 1–11.Google Scholar
Yamvris, C., Panagopoulos, C.G. & Psallidas, P.G. (1970) Preliminary study of the internal bacterial Flora of the olive fruit Fly Dacus Oleae. Annales de l'Institut Phytopathologique Benaki 9(3), 201–206.Google Scholar
Yong, H.S., Song, S.L., Chua, K.O. & Lim, P.E. (2017a) Microbiota associated with Bactrocera carambolae and B. dorsalis (insecta: Tephritidae) revealed by next-generation sequencing of 16S rRNA gene. Meta Gene 11, 189–196.Google Scholar
Yong, H.S., Song, S.L., Chua, K.O. & Lim, P.E. (2017b) High diversity of bacterial communities in developmental stages of Bactrocera carambolae (Insecta: Tephritidae) revealed by illumina MiSeq sequencing of 16S rRNA gene. Current Microbiology 74(9), 1076–1082. 10.1007/s00284-017-1287-x.Google Scholar
Yuval, B., Ben-Ami, E., Behar, A., Ben-Yosef, M. & Jurkevitch, E. (2013) The Mediterranean fruit fly and its bacteria potential for improving sterile insect technique operations. Journal of Applied Entomology 137, 39–42, 10.1111/j.1439-0418.2010.01555.x.Google Scholar
Zhao, X., Zhang, X., Chen, Z., Wang, Z., Lu, Y. & Cheng, D. (2018) The divergence in bacterial components associated with Bactrocera dorsalis across developmental stages. Frontiers in Microbiology 9, 114, 10.3389/fmicb.2018.00114.Google Scholar
Zinder, D.E., & Dworkin, M. (2000) Morphological and physiological diversity. pp. 185-220 in Dworkin, M. et al. (Eds) The Prokaryotes. New York, Springer Verla.Google Scholar