Translator Disclaimer
11 April 2019 Wolbachia Infection of Neoceratitis asiatica (Diptera: Tephritidae)
Author Affiliations +

Neoceratitis asiatica (Becker) (Diptera: Tephritidae), known as wolfberry fruit fly, is a harmful pest of Lycium barbarum (Solanaceae). Neoceratitis asiatica female adults insert the ovipositor into the peel of L. barbarum and lay eggs, causing reductions in yield and economic loss. The symbiotic bacteria Wolbachia spp. have attracted considerable attention and interest by entomologists in recent years. Wolbachia infect many genera of tephritid fruit flies, such as Anastrepha, Bactrocera, Rhagoletis, Dacus, Ceratitis, and Carypomya. Wolbachia can induce complete cytoplasmic incompatibility in novel hosts, leading to complete suppression of laboratory populations by single releases of infected males, which potentially makes it a useful method for pest management. In this study, the infection of Wolbachia in N. asiatica from the Ningxia region in China was detected based on the Wolbachia surface protein gene sequence. The neighbor-joining tree showed Wolbachia in wolfberry fruit fly was wRi strain. This research lays the foundation for further study about Wolbachia in Chinese wolfberry fruit fly, and also provides a basis for the prevention and control of other economically important fruit flies using Wolbachia.

Neoceratitis asiatica (Becker) (Diptera: Tephritidae), known as wolfberry fruit fly, became the most harmful pest to Lycium barbarum (Solanaceae) during the 1950s through the 1970s in the Ningxia region of China (Wu et al. 1963), and yield loss was more than 20%, sometimes as high as 55%. From the 1990s to the beginning of the 21st century, it was a consistently damaging pest (Ren & Hu 2004; Ren 2010). Lycium barbarum, which is called Chinese wolfberry in English, is a source of Chinese herbal medicines. Its dried ripe fruit has beneficial effects on the liver, kidneys, and eyes (Zhao et al. 2009; Xu et al. 2014). Berries, leaves, and roots of L. barbarum contain polysaccharides, amino acids, vitamins, and trace elements that are of high medicinal and nutritional value (Xu et al. 2014). Lycium barbarum is an important economic crop in the northwest region of China, especially in Ningxia, Xinjiang, and Gansu. Inner Mongolia, Qinghai, Hebei, Xizang, Shaanxi, Shanxi, Liaoning, Jiangsu, Zhejiang, and Guangdong Provinces also have this species (Wu & Gao 1964; Hu et al. 2009; Xue & Lin 2009; Xu et al. 2014).

The infestation rate of wolfberry trees has attained 70% in severely affected areas (Zheng 2015). Neoceratitis asiatica female adults insert the ovipositor into the peel of L. barbarum and lay eggs. Initially, the exterior surface of damaged L. barbarum shows no difference from healthy fruit, but in the late stage, white curved stripes appear on the peel. Beneath the peel of infested fruit, the flesh is consumed by N. asiatica and the fruit is full of frass. Under these circumstances, the fruit cannot be used as a commodity or medicine, and thus has no economic value (Wu et al. 1963; Guo et al. 2017; Li et al. 2017).

Neoceratitis asiatica occurs during May to Sep, producing 3 generations per yr. It has 3 fairly unique characteristics. First, N. asiatica is monophagous, feeding only on L. barbarum. Second, the adult female generally lays only 1 egg per fruit. If 2 or 3 eggs are laid in a fruit, only 1 larva survives. Third, adults have no phototaxis, and cannot be baited with sweet or sour wine (Wu & Meng 1963). These traits make it difficult to capture and culture N. asiatica. Investigations into N. asiatica began in the 1960s, and in the nearly half century following, research principally focused on the identification, pattern of occurrence, and control of the pest. Methods combining morphological characteristics and DNA barcoding have been used for its identification (Guo et al. 2017). The mitochondrial genome of this fruit fly also has been studied to determine its phylogenetic status (Su et al. 2017).

The symbiotic bacteria Wolbachia spp. (Anaplasmataceae) have attracted a great deal of attention by entomologists in recent years. Wolbachia were first detected in Culex pipiens (L.) (Diptera: Culicidae) (Hertig 1936). They are thought to have potentially important roles in genetic control of pests because of their effects on the reproduction of their hosts. Wolbachia can induce cytoplasmic incompatibility, parthenogenesis, and feminization of their host (Werren 1997). Cytoplasmic incompatibility provides a reproductive advantage to infected females over uninfected females, resulting in the invasion of Wolbachia into a population (Pan et al. 2018). Wolbachia can interfere with pathogen infection and inhibit some human pathogens, such as dengue and Zika viruses, malaria parasites, and filarial worms (Kambris et al. 2009; Moreira et al. 2009; Bian et al. 2010, 2013; Dutra et al. 2016). Wolbachia also infect many genera of tephritid fruit flies, including Anastrepha, Bactrocera, Rhagoletis, Dacus, Ceratitis, and Carypomya (Jamnongluk et al. 2002; Riegler & Stauffer 2002; Arthofer et al. 2009; Coscrato et al. 2009; Schuler et al. 2011, 2013; Augustinos et al. 2013, 2015; Coats et al. 2013; Karimi & Darsouei 2014; Morrow et al. 2015). Zabalou et al. (2004) transinfected cytoplasmic incompatibility-Wolbachia from Rhagoletis cerasi (L.) to Ceratitis capitata (Wiedemann) (both Diptera: Tephritidae), and Wolbachia induced complete cytoplasmic incompatibility in the novel host, leading to complete suppression of laboratory populations by single releases of infected males. Several studies also reported occurrence of Wolbachia in Chinese populations of Bactrocera dorsalis (Hendel) (Diptera: Tephritidae). However, there were no infections of B. dorsalis by Wolbachia in Yunnan, Fujian, and Wuhan populations (Augustinos et al. 2015). Similar to this result, Liu et al. (2016) also found the absence of Wolbachia in 16 collection sites in Thailand, China (Yunnan, Guizhou, Guangxi, Guangdong, Hainan, Fujian, Zhejiang, Shanghai Provinces), and the lab population. In contrast, Wolbachia had been positively detected in the Fujian, Guangdong, Hainan, Yunnan, and Guangxi Provinces, but the infection rates were very low (0.7–3%) (Sun et al. 2007). That may be the reason why the cytoplasmic incompatibility-Wolbachia based method has not been used in B. dorsalis successfully. However, if we can find Wolbachia strains that can cause cytoplasmic incompatibility in other fruit flies, such as Wolbachia in N. asiatica, we can try to transinfect this specific strain to B. dorsalis to reduce its population. In brief, Wolbachia-induced cytoplasmic incompatibility may be used as an environmentally friendly tool for the biological control of fruit flies. However, lack of a suitable strain prevented the application of Wolbachia in fruit fly management. We believe that assessment of Wolbachia in different species of fruit flies can provide more candidate strains for pest management.

In this study, Wolbachia infection in different developmental stages of N. asiatica from Ningxia Province in China was detected based on wsp gene sequence, and then the phylogenetic relationship of the Wolbachia strain in this fruit fly w as analyzed via neighbor-joining tree building. This research will help us in screening more putative strains with good potential for future applications in pest management, and thus provide a basis for the prevention and control of other economically important fruit flies.

Materials and Methods


Larvae, pupae, and adults were collected in wolfberry trees from Zhongning County, Ningxia (1.090166°E, 37.190000°E) on 30 Sep 2017 (Table 1). All samples were preserved in 100% ethanol and stored at −4 °C before DNA extraction.


Total genomic DNA was isolated from whole individuals of N. asiatica using the commercial TIANamp Genomic DNA Kit (TIANGEN Biotech Co. Ltd., Beijing, China) following the manufacturer's protocol. Polymerase chain reaction (PCR) was completed in a final volume of 25 μL containing 12.5 μL 2 × Taq PCR MasterMix, 9.5 μL sterilized distilled water, 1 μL DNA as a template, 1 μL forward and 1 μL reverse primer, respectively. Amplifications were performed with general primers (Table 2) for wsp gene (Braig et al. 1998) used the following thermal cycling profile: 95 °C for 3 min; followed by 35 cycles of 94 °C for 1 min, 55 °C for 1 min, and 72 °C for 1 min; then 72 °C for 10 min. The reaction was performed on Veriti TM 96-well Thermal Cycler (Applied Biosystems Inc., Waltham, Massachusetts, USA). After amplification, 5 μL of PCR products were separated in 1.5% (w/v) agarose gels (1 × Tris Acetate-EDTA buffer) and stained with GeneGreen Nucleic Acid Dye (TIANGEN Biotech Co. Ltd., Beijing, China) and visualized under UV light. The PCR products were purified and bi-directional sequenced using the same amplification primers used commercially by the Sangon Biotech Co. Ltd., Shanghai, China.


The sequences obtained from N. asiatica were Basic Local Alignment Search Tool (BLAST) in National Center for Biotechnology Information, Bethesda, Maryland, USA. The wsp gene sequences from this study were aligned using MEGA 7.0 (Temple University, Philadelphia, Pennsylvania, USA) (Kumar et al. 2016), and 3 representative sequences were selected. The 3 sequences then were compared with 24 reference wsp sequences from GenBank representing different Wolbachia strains infecting various hosts (Table 3). We used Gblocks Server ( to eliminate poorly aligned positions and divergent regions so that it became more suitable for phylogenetic analysis. The neighbor-joining tree was conducted in MEGA version 7.0, distances were calculated using the Kimura 2-parameter (K2P) model (Kimura 1980) in the bootstrap test (1,000 replications) (Felsenstein 1985). All 3 sequences were submitted to GenBank; the accession numbers MG950140, MG940141, MG950142 were wsp genes in larvae, pupae, and adults of N. asiatica, respectively (Table 1).

Table 1.

Sample information of collection site and accession number.


Table 2.

General primers used to amplify wsp gene.




The BLAST result from National Center for Biotechnology Information showed that all the sequences from the total DNA of Neoceratitis asiatica were the wsp gene of Wolbachia. The sequences of the wsp gene of Wolbachia in different stages of N. asiatica showed that they were identical, and were similar to the wRi strain.


Using the universal primers (81F, 691R) for Wolbachia, we screened 50 larvae, 50 pupae, and 32 adults. Thirteen larvae, 26 pupae, and 32 adults were positively detected in agarose gels.


Phylogenetic analysis of partial sequences of the wsp gene identified in N. asiatica, other fruit flies, and several other arthropod species are shown in Figure 1. In this neighbor-joining tree, 3 wsp gene sequences of Wolbachia in this study were in A Group, and together with the wRi strain in Drosophila simulans. However, the infection of Wolbachia in females and males has not been compared, and should to be the focus of future research.

Table 3.

Wolbachia strains used to construct the phylogenetic tree.



Wolbachia are one of the most abundant symbiotic microbes in arthropods (Werren 1997). In 1 species, when a male is infected by 1 or more kinds of Wolbachia, mating with an uninfected female or carrying a different strain, cytoplasmic incompatibility results in embryonic mortality (Bourtzis et al. 2003). The cytoplasmic incompatibility caused by Wolbachia can be used as an environmentally benign tool for the biological control of fruit flies. Most Wolbachia in fruit flies belonged to group A. Sun et al. (2007) found that B. dorsalis in Yunnan and Hainan provinces carried strain Cuc and Mel of Wolbachia, respectively. Rhagoletis cerasi (L.), Anastrepha spp., and C. capitata (all Diptera: Tephritidae) also had the strain Mel; Dacus destillatoria (Bezzi) contained the strain Des (Coscrato et al. 2009). Ceratitis vesuviana Costa showed infection with Wolbachia between Mors and Riv in the phylogenetic tree (Karimi & Darsouei 2014).

This research confirmed that different development stages of wolfberry fruit fly can be infected with the wRi strain of Wolbachia. wRi have a significant influence on cytoplasmic incompatibility in their natural host D. simulans (Hoffmann et al. 1986; Weeks et al. 2007), which may contribute to the pest management of economically important fruit flies by Wolbachia transmission. Bian et al. (2010) used Wolbachia strain wAlbB to control the mosquito Aedes aegypti (L.) (Diptera: Culicidae), the vector of dengue and Zika viruses. They found this strain could inhibit viral replication and dissemination in Ae. aegypti; thus, the spread of dengue and Zika viruses can be blocked through the control of the insect. They also used Wolbachia strain wAlbB to increase resistance in the mosquito Anopheles stephensi Liston (Diptera: Culicidae) to the human malaria parasite Plasmodium falciparum (Bian et al. 2013). Wolbachia can change the symbiotic relationship and can boost the immune system response to enhance the host's resistance to pathogens (Pan et al. 2018). However, there is still an absence of population control of B. dorsalis using Wolbachia. The low infection rate of Wolbachia in B. dorsalis is the biggest obstacle. Transinfecting Wolbachia strains from other fruit flies maybe a good solution to this problem. This research provided a candidate strain, isolated from wolfberry fruit fly, with the potential for controlling B. dorsalis. In further research, we will focus on the suitability of Wolbachia for population control in B. dorsalis. The potential exists to control not only B. dorsalis, but also other economically important fruit flies.

Phylogenetic tree of Wolbachia strains based on the wsp gene. Neighbor-joining based on wsp gene sequences showing the relationships among arthropod hosts and Wolbachia strains. Distances were calculated using the K2P model with a bootstrap test (1,000 replications). The number at each branch point is the percentage supported by the bootstrap. Only numbers greater than 50 are shown.


Our study was the first to document the existence of Wolbachia in Chinese wolfberry fruit fly. We suggest that the wRi strain of Neoceratitis asiatica has the potential to assist in the prevention and control of other economically important fruit flies.


Financial support was provided by the National Key Research and Development Project of China (No. 2016YFC1200605), and the Science and Technology Innovation Pilot Fund Project of the Ningxia Academy of Agriculture and Forestry Sciences (NKYZ-16–0502). We are grateful to Jing Wei of China Agricultural University for help with collecting larvae from wolfberry fruit.

References Cited


Arthofer W, Riegler M, Schneider D, Krammer M, Miller WJ, Stauffer C. 2009. Hidden Wolbachia diversity in field populations of the European cherry fruit fly, Rhagoletis cerasi (Diptera, Tephritidae). Molecular Ecology 18: 3816–3830. Google Scholar


Augustinos AA, Asimakopoulou AK, Moraiti CA, Mavragani-Tsipidou P, Papadopoulos NT, Bourtzis K. 2013. Microsatellite and Wolbachia analysis in Rhagoletis cerasi natural populations: population structuring and multiple infections. Ecology and Evolution 4: 1943–1962. Google Scholar


Augustinos AA, Drosopoulou E, Gariou-Papalexiou A, Asimakis ED, 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


Bian G, Joshi D, Dong YM, Lu P, Zhou GL, Pan XL, Xu Y, Dimopoulos G, Xi ZY. 2013. Wolbachia invades Anopheles stephensi populations and induces refractoriness to Plasmodium infection. Science 340: 748–751. Google Scholar


Bian G, Xu Y, Lu P, Xie Y, Xi ZY. 2010. The endosymbiotic bacterium Wolbachia induces resistance to dengue virus in Aedes aegypti. PLoS Pathogens 6: e1000833.[10.1371/journal.ppat.1000833] Google Scholar


Bourtzis K, Braig HR, Karr TL. 2003. Cytoplasmic incompatibility, pp. 217–246 In Bourtzis K, Miller TA [eds.], Insect Symbiosis, 1st edition. CRC Press, Boca Raton, Florida, USA. Google Scholar


Braig HR, Zhou W, Dobson S, O'Neill SL. 1998. Cloning and characterization of a gene encoding the major surface protein of the bacterial endosymbiont Wolbachia. Journal of Bacteriology 180: 2373–2378. Google Scholar


Coats VC, Stack PA, Rumpho ME. 2013. Japanese barberry seed predation by Rhagoletis meigenii fruit flies harboring Wolbachia endosymbionts. Symbiosis 59: 145–156. Google Scholar


Coscrato VE, Braz ASK, Perondini ALP, Selivon D, Marino CL. 2009. Wolbachia in Anastrepha fruit flies (Diptera: Tephritidae). Current Microbiology 59: 295–301. Google Scholar


Dutra HL, Rocha MN, Dias FB, Mansur SB, Caragata EP, Moreira LA. 2016. Wolbachia blocks currently circulating Zika virus isolates in Brazilian Aedes aegypti mosquitoes. Cell Host & Microbe 19: 771–774. Google Scholar


Felsenstein J. 1985. Confidence intervals on phylogenies: an approach using the bootstrap. Evolution 39: 783–791. Google Scholar


Guo SK, He J, Zhao ZH, Liu LJ, Gao LY, Wei SH, Guo XY, Zhang R, Li ZH. 2017. Identification of Neoceratitis asiatica (Becker) (Diptera: Tephritidae) based on morphological characteristics and DNA barcode. Zootaxa 4363: 553–560. Google Scholar


Hertig M. 1936. The rickettsia, Wolbachia pipientis and associated inclusions of the mosquito Culex pipiens. Parasitology 28: 453–486. Google Scholar


Hoffmann AA, Turelli M, Simmons GM. 1986. Unidirectional incompatibility between populations of Drosophila simulans. Evolution 40: 692–701. Google Scholar


Hu JF, Miu K, Dong ZH. 2009. Study on the occurrence and prevention of the disease and insect pests of Chinese wolfberry. Modern Agricultural Science and Technology 4: 101–102. (in Chinese with English summary) Google Scholar


Jamnongluk W, Kittayapong P, Baimai V, O'Neill SL. 2002. Wolbachia infections of tephritid fruit flies: molecular evidence for five distinct strains in a single host species. Current Microbiology 45: 255–260. Google Scholar


Kambris Z, Cook PE, Phuc HK, Sinkins SP. 2009. Immune activation by life-shortening Wolbachia and reduced filarial competence in mosquitoes. Science 326: 134–136. Google Scholar


Karimi J, Darsouei R. 2014. Presence of the endosymbiont Wolbachia among some fruit flies (Diptera: Tephritidae) from Iran: a multilocus sequence typing approach. Journal of Asia-Pacific Entomology 17: 105–112. Google Scholar


Kimura M. 1980. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide-sequences. Journal of Molecular Evolution 16: 111–120. Google Scholar


Kumar S, Stecher G, Tamura K. 2016. MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Molecular Biology and Evolution 33: 1870–1874. Google Scholar


Li F, Liu XL, Ma JG. 2017. Study on the occurrence and prevention of wolfberry trypetid in Ningxia. Ningxia Journal of Agriculture and Forestry Science and Technology 58: 35–36. (in Chinese with English summary) Google Scholar


Liu LJ, Martinez-Sañudo I, Mazzon L, Prabhakar CS, Girolami V, Deng YL, Dai Y, Li ZH. 2016. Bacterial communities associated with invasive populations of Bactrocera dorsalis (Diptera: Tephritidae) in China. Bulletin of Entomological Research 106: 1–11. Google Scholar


Moreira LA, Iturbe-Ormaetxe I, Jeffery JA, Lu GJ, Pyke AT, Hedges LM, Rocha BC, Hall-Mendelin S, Day A, Riegler M, Hugo LE, Johnson KN, Kay BH, McGraw EA, van den Hurk AF, Ryan PA, O'Neill SL. 2009. A Wolbachia symbiont in Aedes aegypti limits infection with dengue, chikungunya, and plasmodium. Cell 139: 1268–1278. Google Scholar


Morrow JL, Frommer M, Royer JE, Shearman DCA, Riegler M. 2015. Wolbachia pseudogenes and low prevalence infections in tropical but not temperate Australian tephritid fruit flies: manifestations of lateral gene transfer and endosymbiont spillover? BMC Evolutionary Biology 15: 202.[10.1186/s12862-015-0474-2] Google Scholar


Pan XL, Pike A, Joshi D, Bian GW, McFadden MJ, Lu P, Liang X, Zhang FR, Raikhel AS, Xi ZY. 2018. The bacterium Wolbachia exploits host innate immunity to establish a symbiotic relationship with the dengue vector mosquito Aedes aegypti. The ISME Journal 12: 277–288. Google Scholar


Ren YP. 2010. Evolution of disease and insect pest population of cultivated medlar in different periods and their chemical control method. Journal of Anhui Agriculture Science 38: 2443–2445. (in Chinese with English summary) Google Scholar


Ren YP, Hu ZQ. 2004. The progress of research on chemical control for main diseases and insect pests of Chinese wolfberry in Ningxia. Journal of Ningxia Agricultural College 25: 88–91. (in Chinese with English summary) Google Scholar


Riegler M, Stauffer C. 2002. Wolbachia infections and superinfections in cytoplasmically incompatible populations of the European cherry fruit fly Rhagoletis cerasi (Diptera, Tephritidae). Molecular Ecology 11: 2425–2434. Google Scholar


Schuler H, Arthofer W, Riegler M, Bertheau C, Krumböck S, Köppler K, Vogt H, Teixeira LAF, Stauffer C. 2011. Multiple Wolbachia infections in Rhagoletis pomonella. Entomologia Experimentalis et Applicata 139: 138–144. Google Scholar


Schuler H, Bertheau C, Egan SP, Feder JL, Riegler M, Schlick-Steiner BC, Steiner FM, Johannesen J, Kern P, Tuba K, Lakatos F, Köppler K, Arthofer W, Stauffer C. 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


Su Y, Zhang Y, Feng SQ, He J, Zhao ZH, Bai ZZ, Liu LJ, Zhang R, Li ZH. 2017. The mitochondrial genome of the wolfberry fruit fly, Neoceratitis asiatica (Becker) (Diptera: Tephritidae) and the phylogeny of Neoceratitis Hendel genus. Scientific Reports 7: 16612. Google Scholar


Sun X, Cui LW, Li ZH. 2007. Diversity and phylogeny of Wolbachia infecting Bactrocera dorsalis (Diptera: Tephritidae). Molecular Ecology and Evolution 36: 1283–1289. Google Scholar


Weeks AR, Turelli M, Harcombe WR, Reynolds KT, Hoffmann AA. 2007. From parasite to mutualist: rapid evolution of Wolbachia in natural populations of Drosophila. PLoS Biology 5: e114.[10.1371/journal.pbio.0050114] Google Scholar


Werren JH. 1997. Biology of Wolbachia. Annual Review of Entomology 42: 587–609. Google Scholar


Wu FZ, Gao ZN. 1964. A preliminary report on the fauna of agricultural insects of Ningxia autonomous region, China. Acta Entomologica Sinica 13: 572–580. Google Scholar


Wu FZ, Huang RX, Meng QX, Liang ZQ. 1963. Studies on the life history and the control of Lycium fruit fly Neoceratitis asiatica (Becker) (Diptera: Tephritidae). Journal of Plant Protection 2: 387–398. (in Chinese with English summary) Google Scholar


Wu FZ, Meng QX. 1963. Distribution, damage, life habit and prevention and control method of Neoceratitis asiatica (Becker). Ningxia Agricultural Science Communication 6: 35–37. (in Chinese with English summary) Google Scholar


Xu CQ, Liu S, Xu R, Chen J, Qiao HL, Jin HY, Lin C, Guo K, Cheng HZ. 2014. Investigation of production status in major wolfberry producing areas of China and some suggestions. China Journal of Chinese Materia Medica 39: 1979–1984. (in Chinese with English summary) Google Scholar


Xue FX, Lin HM. 2009. The prevention and control strategy of Lycium barbarum. Scientific and Technical Information of Gansu 38: 57–58. (in Chinese with English summary) Google Scholar


Zabalou S, Riegler M, Theodorakopoulou M, Stauffer C, Savakis C, Bourtzis K. 2004. Wolbachia-induced cytoplasmic incompatibility as a means for insect pest population control. Proceedings of National Academy of Sciences of the USA 101: 15042–15045. Google Scholar


Zhao ZH, Zhang R, He DH, Wang F, Zhang TT, Zhang ZS. 2009. Risk assessment and control strategies of pest in Lycium barbarum fields under different managements. Chinese Journal of Applied Ecology 20: 843–850. (in Chinese with English summary) Google Scholar


Zheng QW. 2015. Preliminary progress has been made in the development of the control technology of Chinese wolfberry in Ningxia. Pesticide Market News 26: 66. (in chinese with english summary) Google Scholar
Xiaoxue Wang, Zhihong Li, Rong Zhang, Jia He, Zihua Zhao, Shuhua Wei, and Lijun Liu "Wolbachia Infection of Neoceratitis asiatica (Diptera: Tephritidae)," Florida Entomologist 102(1), 125-129, (11 April 2019).
Published: 11 April 2019

Back to Top