Biology, taxonomy, and IPM strategies of Bactrocera tau Walker and ...

Environmental Science and Pollution Research https://doi.org/10.1007/s11356-018-2306-6

REVIEW ARTICLE

Biology, taxonomy, and IPM strategies of Bactrocera tau Walker and complex species (Diptera; Tephritidae) in Asia: a comprehensive review Waqar Jaleel 1

&

Lihua Lu 2 & Yurong He 1

Received: 2 January 2018 / Accepted: 11 May 2018 # Springer-Verlag GmbH Germany, part of Springer Nature 2018

Abstract Bactrocera flies are the serious pests of fruit, vegetables, and nuts over the world. Bactrocera tau Walker is an economically important pest of agricultural crops. In Asia, approximately 30–40% losses of agricultural products are caused by B. tau infestation every year. In Asia, the B. tau contains a complex of sibling species that called the tau complex. However, the basic studies of B. tau and complex species are very important for integrated management. A comprehensive review of the B. tau and complex species has not been provided elsewhere. So, considering the importance of B. tau and complex species, this study provides the published information on ecology, nomenclature, identification tools, geographical distribution, potential invasion, and IPM tactics of B. tau and complex species, which would be more informative for publication facilitating related to integrated pest management (IPM) strategies of B. tau and complex species. In IPM of B. tau and complex species, the phytochemical and biological controls have not been applied successfully in Asia; there is an urgent need to study and applications of these two mentioned control techniques against the B. tau and complex species in Asia. Keywords Bactrocera tau and complex species . Biology . Pumpkin fruit fly . Nomenclature . IPM . Asia . Taxonomy

Introduction In the world, the agricultural sector is an economically most important source of earning for 789 million people among other sectors (FAO 2015). Development and progress of agricultural sectors are most important tasks for scientists because these sectors are providing foods and employment to people of developing countries worldwide. But insect pests are one of the big hurdles in the development and progress of the agricultural sector that are continuously damaging to food and their commodities

Responsible editor: Philippe Garrigues * Yurong He [email protected] 1

College of Agriculture, South China Agriculture University, Wushan Road, Tianhe District, 510642 Guangzhou, China

2

Plant Protection Research Institute, Guangdong Academy of Agricultural Sciences, Jinying No. 7, Tianhe District, Guangzhou 510640, China

(Meade and Thome 2017). However, the preservation and protection of food crops from insect pest especially Bactrocera flies (Diptera: Tephritidae) are most important in agricultural sectors (Ekesi et al. 2016; Paul et al. 2009). Globally, Bactrocera species are significant pests of agricultural crops in Asia since the beginning of the last century (Allwood and Drew 1996; Armstrong and Jang 1997; Clarke et al. 2005; Jaleel et al. 2017a). Among Bactrocera flies, the pumpkin fruit fly or B. tau and complex species are economically most important pests of vegetables, fruits, and nuts (Fletcher 1987; Jaleel et al. 2017a; Li et al. 2017; Shi et al. 2017; Singh et al. 2010). The B. tau and complex species feed on varieties of agricultural crops (Allwood et al. 1999; Chinajariyawong et al. 2003; Shi et al. 2017; Singh et al. 2010; Wu et al. 2011; Yan et al. 2015). Approximately 41–89% infestation of bitter gourd in Indonesia (Gupta and Verma 1978; Hasyim et al. 2016; Ravindranath and Pillai 1986), 5.6% infestations of ripen Luffa acutangula in Thailand (Ramadan and Messing 2003), and 10–15% of vegetable crop losses have been caused by B. tau and complex species (Yan et al. 2015). The B. tau has caused 21–34 and 21–32% yield losses of Siraitia grosvenorii and Cucurbita moschata respectively in Taiwan

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(Liu et al. 2005). In Himachal Pradesh, India, the 80% losses of vegetable crops have been reported by B. tau and complex species (Prabhakar et al. 2009; Sood et al. 2010). Application of integrated pest management (IPM) for the control of B. tau and complex is very important in farms and orchards. In IPM programs, it is very important to understand the basic and applied information of insect pest (Jaleel et al. 2013, 2017a, b; Shakeel et al. 2017; Yang et al. 1994). However, information regarding taxonomy, biology, and integrated management of different Bactrocera flies have been reported in Asia and Africa (Dhillon et al. 2005; Ekesi et al. 2016; Sood et al. 2010) except B. tau and its complex species. A new scientific and up-to-date information is needed to improve the management strategies for B. tau and complex species. In this view, this study provides the detailed and updated information on geographical distribution, host records, biology, nomenclature, identification tools, symbiotic relationship, and different management techniques of B. tau and complex species, which explore the IPM of B. tau and complex species.

Nomenclature and identification of B. tau and complex species Nomenclature The B. tau Walker was described by Walker in (1849), Fujian, China. In 1912 and 1913, this species has been reported with name, i.e., Zeugodacus tau in Yunnan, Guangdong and Sichuan provinces of China (Freidberg 1999; Wang 1996; Yang et al. 1994). This species has also been included in the subgenus Zeugodacus and so in most of the literature; its name was quoted as Bactrocera (Zeugodacus) tau (Hardy 1973; Yang et al. 1994). Taxonomic revisions were studied by Drew et al. (1998) (Drew and Hancock 1994; Drew et al. 1998; Drew and Hooper 1983; Drew 1989). The B. tau and complex species in Southeast Asia were called the tau complex. Due to the reason, its taxon contains the complex species (Drew and Romig 1997). The scientific names of the pumpkin fruit fly have been published with more than one name as Dacus hageni de Meijere or D. nubilus and D. tau. According to White and Hancock in 1997, these are different species. In Southern India, Bactrocera zahadi has been reported synonym of this species and most of the literature it called as pumpkin fruit fly (Khalid 1999; White and Hancock 1997). Now, the scientific name of pumpkin fruit fly is written as Bactrocera tau.

Conventional and molecular identification of B. tau Taxonomical studies of B. tau and complex species are very important in IPM because a proper identification provides a strong framework for future evolutionary and environmental studies (Chakravarthy 2015; Clarke et al. 2005).

Conventional techniques Taxonomy of B. tau has been studied based on the alpha taxonomy. The B. tau has a distinct cephalopharyngeal skeleton and easily identified at third instar larval stage (Singh et al. 2010). The identification of B. tau has been done by wing vein analysis within complex species’ as-designed forms BA^ and BC^ that is a good strategy in control program (Kitthawee and Rungsri 2011). In Thailand, the seven members of B. tau and complex species were compared based on the ovipositor morphology by using the scanning electron microscopy. The seven members of B. tau complex (A to I) have been further classified into two groups based on the shape of the aculeus apex. The first group was trilobed aculeus apices (C and I) and remaining groups (A, D, E, F, and G) were pointed apices (Sumrandee et al. 2011). The external morphology, antennae types, and antennal sensilla in both male and female adults of B. tau, B. dorsalis, B. cucurbitae, B. minax, B. diaphora, and B. scutellata (Hendel) have been compared with the help of scanning electron microscopy. Six distinct morphological types of sensilla were observed in above species, i.e., microtrichial sensilla, sensilla chaetica, sensilla trichoid, sensilla basiconica, short type of sensilla basiconica, and sensilla coeloconica (Hu et al. 2010; Zhang et al. 2012). In Himachal Pradesh, India, the identification of B. tau was done by wings morphology that is an easy and accurate method for fruit flies identification (Prabhakar et al. 2012).

Molecular identification Study of the systematic relationships between and within species by using new molecular techniques is better and convenient as compared to traditional methods (Hillis et al. 1992; Tan et al. 2016). The identification of B. tau has been studied by modern approaches like morphometrics (Rohlf and Marcus 1993). Identification of B. tau with COI gene amplification is a better way for a description of genetic pattern or sequence. The sequences of the mitochondrial cytochrome oxidase I gene of B. tau complex have been compared with Bactrocera dorsalis, Bactrocera pyrifoliae, Ceratitis capitata, Anopheles gambiae, and Locusta migratoria. So, this sequence of divergence was concluded up to 29% (Jamnongluk et al. 2003). The identification of B. tau and complex species has been identified based on the analysis of mitotic karyotypes of wild specimens in Thailand. The seven distinct chromosome forms were made and named A to G. These forms were categorized based on the quantity and dissemination of heterochromatin in sex chromosomes and autosomes. Further, karyotype was updated as H, and I (V.B. unpublished) for pumpkin fruit fly (Baimai et al. 2000; Jamnongluk et al. 2003; Saelee and Baimai 2006; Thanaphum and Thaenkham 2003; Tigvattananont 1986). The quick and better way of identifications of Bactrocera flies is RFLP markers of mitochondrial DNA that have been

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used for six species of fruit flies in South China. The banding patterns of (B.) dorsalis, B. (B.) rubiginus, B. (Zeugodacus) cucurbitae, B. (Z.) tau, B. (Z.) scutellata, and B. (B.) hyaline were different from each other (Wu et al. 2004). The Bthsc1 markers are the best tool to resolve cryptic taxon of B. tau. The taxon of B. tau was classified based on the host–plant preferences, cytological differences, and external morphologies into A, B, C, D, E, F, G, and I (Saelee and Baimai 2006). Crude boiling of DNA is the best method to study the phylogenetic relationship of fruit flies (Zhang et al. 2010). Invasion pathways and colonization history of B. tau and complex species have been studied by allelic-based markers (Lombaert et al. 2010). Random amplified polymorphic DNA–polymerase chain reaction (RAPD–PCR) is a useful way to identify the sensilla of the segment in Bactrocera flies. Kitthawee and Dujardin (2010) were collected the B. tau from different plant hosts in Thailand and then divided into 11 samples according to respected host and geographic position. Two clusters were identified by geometric morphometrics and designated as A and C, respectively. The B. tau contains the distinct antenna sensillae among other species of fruit flies (Hu et al. 2010; Zhang and Zhang 2007). The identification of B. tau usually is done by DNA heat shock protein. About 50% positive results can be avail by this method. So, B. carambolae, B. papayae, B. tau, B. latifrons, B. cucurbitae B. umbrosa, and B. caudata have been identified through polymerase chain reaction–restriction fragment length polymorphism (PCR– RFLP) of cytochrome oxidase I (COI) gene using primers COIR, COIF, UEA7, and UEA10 and restriction enzymes (MseI, RsaI, and Alu1). The binding profiles of B. tau have been analyzed in the electrophoresis gel. PCR–RFLP analyzed and identified five Bactrocera species positively, but B. papayae and B. carambolae were not easily identified from one another, which even used immature life stages or adult body parts (Chua et al. 2010). Six genetic groups of the B. tau have been identified in Asian countries, and homogeneous genetic patterns have shown weak relationships in southern China, while Western China, Thailand, and Laos have shown strong genetic relationships. The B. tau and B. dorsalis have been identified by esterases bands detection. The six esterase bands (Est-1, Est-2, Est-3, Est-4, Est-5, and Est-6) have been recorded and shown a different pattern in both species and concluded that expression of isoenzymes is directly proportional to the age of fruit flies (Rashid et al. 2012). The mtDNA is considered a best marker for tracking the origin and evolutionary history of organisms (Rollins et al. 2011). The immature and mature stages of B. zonata, B. tau, and B. dorsalis have been identified by using COX-I gene. The species-specific markers of B. zonata and B. tau were designed as 500 and 220 bp, respectively. The Bactrocera spp. are monophyletic that can be confirmed by using

maximum parsimony (MP) and Bayesian phylogenetic approach (BP) (Asokan et al. 2011). Phylogenetic studies of fruit flies are most important to find out their taxon. Mitochondrial DNA (mtDNA) and nuclear markers, replication of DNA, and recombinant DNA are the most popular ways for identification and description of the cryptic taxon (Wan et al. 2012). The variation in population genetic structure of B. tau and complex species was studied by mitochondrial cytochrome oxidase I (mtCOI) gene sequences. In conclusion, the B. tau complex was originated since 0.4 million years ago (Prabhakar et al. 2013). The 28S rDNA is considered better and accurate tools for identification of immature stages of fruit flies. However, the 28S rDNA has been used to identify eggs, larvae, pupae, and adults of Bactrocera spp. The B. tau was supported by 100% bootstrap that is why this species was considered phylogenetically different from B. dorsalis, B. zonata, and B. correcta (Asokan et al. 2013). The complete mitochondrial genome (mitogenome) sequence had shown 15,687 bp in length, with composition of non-coding control region and 37 genes of bilaterian animals (13 protein-coding genes, 22tRNA genes, and 2rRNA genes) in oriental region; the mitogenome of B. tau gave the idea of development of new DNA markers for the identification of fruit flies (Tan et al. 2016). The highly polymorphic and co-dominant markers, microsatellites, also known as simple sequence repeats (SSRs), are commonly used for eukaryotic genomes. Yan et al. (2015) have been studied 22 microsatellite markers loci through enriched genomic library protocol and introduced in classification and population genetic analysis of B. tau. According to the BHardy–Weinberg equilibrium,^ the polymorphic information values of B. tau were from 0.124 to 0.818.

Geographical distribution, host plant spectrum, and potential invasion Geographical distribution and host plants of B. tau are available on CAB International CABI 2009 (http://www.cabi.org/ isc/datasheet/8741). But, this study provides the update information of hosts and geographical distribution of B. tau and complex (Fig. 1) and hosts (Table 1).

Geographical distribution In 1849, the B. tau has been reported for the first time in Fujian, China. In 1912 and 1913, these species have been reported in Yunnan, Guangdong, and Sichuan provinces of China, respectively (Freidberg 1999; Wang 1996; Yang et al. 1994). Bactrocera tau and complex species have been reported in South Asia to Southeast Asia during 2000 to 2014 (Akhtaruzzaman et al. 1999; Amice and Sales 1997; Hossain et al. 2011; Hu et al. 2010; Sh et al. 2014; Thanaphum and Thaenkham 2003; White and Elson-Harris 1992) and also in Solomon Islands (Fig. 1). The low to midhill areas were

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Fig. 1 Geographical distribution of the pumpkin fruit fly, Bactrocera tau, in the world

considered the favorable regions for the activity of pumpkin fruit fly, while no record has been found in high hills (> 3200 mamsl).

Host plant spectrum and potential invasion The B. tau and complex species have been reported to infest 91 species of host plants of 16 families including Anacardiaceae, Cucurbitaceae, Elaeocarpaceae, Moraceae, Myrtaceae, Oxalidaceae, Rutaceae, Sapotaceae, and Solanaceae. The B. tau and complex species usually not only are considered as vegetable pests and named pumpkin fruit flies but also have been recorded on fruit and other wild plants (Table 1). The wild host plants perhaps could be the reservoir for hosts of B. tau and complex species (Baimai et al. 2000; Jamnongluk et al. 2003; Kitthawee and Dujardin 2010; Sumrandee et al. 2011). According to the survey reports, the 110 samples of B. tau and complex species have been trapped from Cucurbitaceae crops

with cue-lure traps at different locations in Malaysia (Tan and Nishida 2000), Thailand (Ramadan and Messing 2003; Sumrandee et al. 2011), Taiwan (Liu et al. 2005), and Bangladesh (Leblanc et al. 2014). Recently, this species has been reported as a serious pest of a tomato plant in India (Boopathi et al. 2017) (Table 1). Bactrocera tau and complex species were reported major invasive pests of agricultural crops (Bai et al. 2012). In China, six genetic groups of B. tau and complex species have been described with the weak pattern in Southern, Central China, and Northern Vietnam, while continuous in southern China (Sh et al. 2014). Understanding the re-establishment pathway of invasive species helps to find out the location and genetic makeup, and growth routes (Wan et al. 2012). Invasion incidence of B. tau and complex species has been reported in Australia (Hossain et al. 2011; Ohno et al. 2008). However, the evolutionary history of B. tau and complex species is still undecided because of the scarcity of historical records.

Environ Sci Pollut Res Table 1

Host plant spectrum for the pumpkin fruit fly, Bactrocera tau Walker

Scientific names

Common names

References

Carica papaya L. Cucurbitaceae

Papaya

Borah and Dutta (1996)

Benincasa hispida (Thunb.) Bryonia laciniosa L.

Winter melon/wax gourd Ayurvedic herb

Allwood and Drew (1996); Huque (2006) Kapoor (1993); White and Elson-Harris (1992)

Coccinia grandis L.

Voigt scarlet gourd

Baimai et al. (2000); Kitthawee and Dujardin (2010)

Cucumis sativus L. Cucurbita maxima Duchesne

Cucumber Giant pumpkin

Allwood et al. (1999); Huque (2006); Thakur and Gupta (2012) Huque (2006); Singh et al. (2010)

C. pepo L. C. moschata Duchesne ex Poir.

Zucchini Pumpkin

Prabhakar et al. (2009); Shen et al. (2014) Guoping et al. (2015); Jamnongluk et al. (2003); Sumrandee et al. (2011)

Vegetables Caricaceae

Diplocyclos palmatus (L.)

Striped cucumber/Jeffrey

Koizumi and Yamamoto (1972)

Lagenaria siceraria Ser

Bottle gourd

Koizumi and Yamamoto (1972); Prabhakar et al. (2009); White and Elson-Harris (1992)

Luffa acutangula (L.) Roxb. L. aegyptiaca Mill. L. cylindrica Mill.

Angled luffa Loofah Towel gourd

Drew and Romig (2013); Koizumi and Yamamoto (1972) Allwood et al. (1999); Borah and Dutta (1996) Allwood et al. (1999); Khan et al. (2014); Lin et al. (2006)

Momordica charantia L. Solanaceae Capsicum annuum L. C. frutescens L. Lycopersicon esculentum L.

Bitter gourd

Prabhakar et al. (2009); Shen et al. (2014)

Bell pepper Chili pepper Tomato

Borah and Dutta (1996) Borah and Dutta (1996); Wang (1996) Boopathi et al. (2017); Koizumi and Yamamoto (1972)

Mango

Koizumi and Yamamoto (1972); Wee and Shelly (2013)

Cucumis melo L.

Muskmelon

M. cochinchinensis (Lour.) Spreng. M. cochinensis Kankrol

Gac fruit Vietnamese = gac

Allwood et al. (1999); Drew and Romig (2013); Koizumi and Yamamoto (1972) Sumrandee et al. (2011) Jamnongluk et al. (2003); Kitthawee and Rungsri (2011).

Fruits Anacardiaceae Mangifera indica L. Cucurbitaceae

Siraitia grosvenorii (Swingle) Trichosanthes dioica Roxb. T. cucumerina anguina T. tricuspidata L. T. laceribracteata Hayata T. ovigera T. pilosa (Ser.) Maxim, Franch. & Sav. T. palmat Moraceae Artocarpus heterophyllus Lam Ficus racemosa Myrtaceae Psidium guajava L. Syzygium samarangense (Blume) Merr. & L.M. Perry Oxalidaceae Averrhoa carambola L. Passifloraceae Passiflora edulis Sims.

Parval or pointed gourd Tropical or subtropical vine (snake gourd) Tropical and subtropical vines.

Liu et al. (2005) Huque (2006) Baimai et al. (2000); Huque (2006)

Japanese snake gourd

Allwood et al. (1999); Sumrandee et al. (2011) Allwood et al. (1999); Baimai et al. (2000) Allwood et al. (1999); Christenson and Foote (1960)

Red ball snake gourd

Kapoor (1993)

Jack fruit Cluster tree

White and Elson-Harris (1992) Borah and Dutta (1996)

Guava Wax apple

Allwood et al. (1999); Wee and Shelly (2013) Christenson and Foote (1960); Kapoor (1993)

Star fruit

Koizumi and Yamamoto (1972); Wee and Shelly (2013)

Passion fruit

Hasyim et al. (2016); Octriana (2013)

Environ Sci Pollut Res Table 1 (continued) Scientific names

Common names

References

Rutaceae Citrus reticulata Blanco.

Mandarin Tangerine

Wu et al. (2011); Zhang et al. (2012)

C. maxima Merr.

Pomelo

Drew and Romig (2013)

C. sinensis L. Manilkara zapota L.

Orange Sapodilla

Zhang et al. (2012) Borah and Dutta (1996); Drew and Romig (2013)

Dimocarpus longan Lour Vitaceae

Longan

Borah and Dutta (1996)

Vitis vinifera Beans

Grapes

Margosian et al. (2007)

Common bean

Borah and Dutta (1996)

Sapindaceae

Fabaceae Phaseolus vulgaris L. Other wild plants Achariaceae Hydnocarpus anthelminticus Pierre ex Gagnep Arecaceae

Jamnongluk et al. (2003); Sumrandee et al. (2011)

Borassus flabellifer L. Celastraceae

Toddy palm

Borah and Dutta (1996)

Siphonodon celastrineus Griff.

Hyunja

Thanaphum and Thaenkham (2003)

Loganiaceae Strychnos thorelii Pierre ex Dop

Biology and demography Usually, there are great variations in survival, population dynamics, the immature and mature development time of B. tau and complex species on different hosts, temperature (Ganie et al. 2013), and humidity (Li et al. 2009). However, the comparative biological studies of B. tau and B. dorsalis have been done on Momordica charantia L. and concluded that B. tau gained higher oviposition rate than B. dorsalis (Yang et al. 1994). The life cycle of B. tau was recorded 120–140 days on C. maxima. Mating and the pre-oviposition period were remains for 408.03 ± 235.93 min and 11.7 ± 4.49 days, respectively. However, male and female adult longevity were 130.33 ± 14.18 and 104.66 ± 31.21 days, respectively (Singh et al. 2010). Another study had shown the life cycle of B. tau that remained at 145–160 days on cucurbitaceous crops (Ganie et al. 2013; Singh et al. 2010). In the field, the population of B. tau usually remains highest from July to November (Liu et al. 2005). Female adults of B. tau and complex species live loger than male adults (Fig. 2). Humidity is one of the most important factors determining the growth and population rate of Bactrocera flies. The effects of soil relative water content (SRWC) and air relative humidity (RH) were tested on pupal development, survival of B. tau. So, the pupal emergence of B. tau was failed at high humidity (80–90%) (Li et al. 2009, 2013).

Baimai et al. (2000); Sumrandee et al. (2011)

The food mass one of the most important factors to determine the biological and life table parameters of Bactrocera flies. The suitable hosts of B. tau and complex species are Cucumis sativus, Luffa cylindrica, C. mixta, M. charantia, and C. unshiu (Zhou et al. 2005). For example, the B. tau was reared on different hosts (C. sativus, L. cylindrica, M. charantia, P. guajava, and C. reticulate) under high-density population (Wu et al. 2011). Another study has been reported that around 23.68, 19.94, and 21.18% of individuals of B. tau aggregate on cucumber, pumpkin, and towel gourd for egg laying, respectively. The kankrol (M. cochinensis) is the best host plant for B. tau among six vegetables (sweet gourd, kankrol, cucumber, potol, bottle gourd, and snake gourd) (Huque 2006). In a comparative study, it has been reported that B. tau and B. cucurbitae preferred the sponge gourd and cucurbitaceae crops (Mahfuza et al. 2011). The comparison of interspecific and intraspecific competitions was studied between B. tau and B. cucurbitae at a different temperature; a conventional ecological model was developed for these two species. But the pupal duration was not affected by intraspecific and interspecific competitions. However, the significant difference has been observed in development time of fruit flies at the following temperatures 18, 21, 24, 27, and 30 °C (Shen et al. 2014). Jaleel et al. (2017a) have studied the two-sex life tables of four Bactrocera flies such as B. correcta, B. dorsalis, B, cucurbitae, and B. tau on a semi-artificial diet,

Environ Sci Pollut Res Fig. 2 Life cycle of pumpkin fruit fly

which found the highest variation among four Bactrocera flies. However, there is an important and urgent work need for entomologist to study the age-stage, two-sex life table traits of B. tau on cucurbitaceae hosts; it is important for IPM program.

Symbiotic relationship Symbiotic interactions between insect pest and microorganism especially bacteria are interesting for scientist and provide cues of ecological revolutions. Symbionts provide may provide a suitable environment for producing enzymes in the host that are helpful to digest the food. Insect ecology in relation to insect symbiosis can provide novel boulevards for the insect pest control especially dipteran pests including fruit flies through targeted operation of the insect symbionts associations (Berasategui et al. 2016). However, bacterial symbionts might be ingested by the fruit flies through food. Most of the bacteria are used to degradation of proteins and toxic substances. For example, three bacteria were tested against the B. tau; as the first one, its symbiont named as Pseudomonas putida, the second fruit fly’s pathogen as Bacillus subtilis, and the third was non-associated strain Escherichia coli. All these bacteria have abilities to established colonies in B. tau (Sood et al. 2010). In Thailand, the Wolbachia strains from B. tau were detected by PCR analysis t (Sintupachee et al. 2006). The most prominent gut bacteria, i.e., Klebsiella oxytoca,

Pantoea spp., and Staphylococcus spp., had been identified by 16S rDNA (rrs gene) in B. tau (Prabhakar et al. 2009; Prabhakar et al. 2013). In the symbiont-like bacteria, eight of midgut bacteria were identified by genus Proteus, Klebsiella, Streptobacillus, Alcaligenes, Haemophilus, Erwinia, Chromobacterium, and Flavobacterium form B. tau. Proteus rettgeri and Klebsiella oxytoca were tested against B. tau and found no significant impact on fecundity (Khan et al. 2014). The Wolbachia affects the reproductive system and speciation of insect pests. Wolbachia has been reported in the management of fruit flies as it infects the B. tau that reported in Thailand but still needs further work to understand the mechanism of interaction (Kittayapong et al. 2000). Sood and Nath (2005) have tested the P. putida against the B. tau. The P. putida contains the ability to develop its colonies in B. tau and concluded that if virulent gene would be incorporated, then it might be useful in the suppression of B. tau and fruit flies in a wide area management.

Integrated management In this review article, the importance of different IPM techniques was highlighted against the B. tau. Sustainable agriculture had been obtained by applying the integrated pest management (IPM) in farms and orchards. Educated growers always were found to be willing to adopt these IPM technologies (Ekesi et al. 2016).

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Phytosanitary treatment Bactrocera flies are serious quarantine pests worldwide. Actually, larvae of fruit fly feed inside the fruit; so, quarantine measurements are most important to check and treat those fruits infested by the fruit flies attacks. About US$35 million have been used to eradicate occurrences of Ceratitis capitata (Wiedemann) in Florida since 1997–1998 (Hallman and Loaharanu 2002). The B. tau and complex species are serious threats of invasion as invasion pests through transportation to Japan, the USA, Indonesia, and Pakistan (Hasyim et al. 2016; Ohno et al. 2008). Post-harvest treatments are the best option across quarantine to treat infestation cause by Bactrocera flies (Hallman 2011). Irradiation, cold storage, heat water treatments (HWT), dips in systemic insecticides, and fumigation with methyl bromide are the most used quarantine treatments (Hossain et al. 2011). Irradiation and hot water treatments are the most important phytosanitary treatments.

Irradiation Irradiation is quarantine treatment that is increasing in use against infestation of Bactrocera flies, especially B. tau, because, in the USA, the B. tau has been reported in cucurbitaceae crops. Irradiation is a better treatment to apply on fresh commodities, ability to treat in final packaging in pallet loads, and lack of residues as compared to other phytosanitary treatments (Hallman 2011). Usually, irradiation techniques were done to the prevention of Bactrocera adults’ emergence, not larval mortality inside the fruit, because irradiations should be applied within the suitable range to the fruit treatments. However, control actions have been taken in France airport in 1993 for the tropical fruits that were shipped from Asia and European countries (Bayart et al. 1997). In Asia and Australia, most of the host commodities shipped or export and import from infested areas to an uninfested area. Irradiation applications have been found most useful that reduced the risk of shipping viable flies. The quarantine problem of Bactrocera species has reduced by adopting phytosanitary irradiation treatments in many countries (Hallman 2011; Hallman et al. 2010). Actually, during export and import, infested plant materials are the main cause of pest and disease problem to the non-infested area. The B. tau has been reported in mangoes and assortment of other vegetables that had been imported from India (Hossain et al. 2006, 2011). The USDA/APHIS have designed the generic dose of irradiations for reduction of insects’ attack, e.g., 150 Gy for Bactrocera species, 250 Gy for other insect pests, and 300 Gy for mites (Corcoran and Waddell 2003; Follett and Armstrong 2004). A Bgeneric^ quarantine treatment is described as one that provided quarantine security for a broad group of pests. The approved doses were 210 Gy for B. cucurbitae, 225 Gy for C. capitata, and 250 Gy for B. dorsalis (Follett and Armstrong 2004). The

International Plant Protection Convention (IPPC) have approved the irradiation dose of 150 Gy for Bactrocera species and prevented the normal adult emergence 99.9968% when applied at third instars (Hallman 2012; Hallman et al. 2013). Different fruit attacked by seven Bactrocera species were treated with generic dose 150 Gy of irradiation designed by IPPC (Zhao et al. 2017). The irradiation 60 Gy has been found most effective against Bactrocera flies. Results have shown that deformation was increased with the increase of irradiation dose (Zahan et al. 2016). Adult emergence of B. tau was reduced when the irradiation treatments were applied with doses 85 and 72 Gy at the efficacy of 99.9972 and 99.9938%, respectively (Guoping et al. 2015). Cai et al. (2018) reported that when pupae of B. tau were treated with the irradiation dose > 150 Gy, then fecundity was significantly reduced. However, irradiation treatments with high doses have potential negative effects on quality of fruits and vegetables (Zhao et al. 2016; TorresRivera and Hallman 2007). Zhao et al. (2016) have designed the irradiation dose e.g. 116 Gy to treat the Bactrocera species. The 70 Gy has been recommended for the irradiation treatment of attacked mango fruit by the larvae of Bactrocera fly (Odai et al. 2014; Guoping et al. 2015). The emergence and survival rate, as well as competitiveness of male adults of B. tau, were significantly affected by irradiation at dose 100 Gy (Du et al. 2016). The X-ray irradiations have been tested against the B. dorsalis and concluded decreased mating ability and fecundity of B. dorsalis (Chang et al. 2015). However, every fruit has their own vulnerability against the irradiation doses (Zhao et al. 2017); more work is needed to design the specific or low doses of irradiation for fruits and vegetable crops.

Cold treatment Cold treatment is the most useful phytosanitary treatment against the larval infestation of Bactrocera flies. In this treatment, cold temperature and its duration depend on the fruit and insects developmental stages (Follett and Snook 2013). The lowest temperature for a longer period is better than increasing temperature for short period that causes malformation of fruits (Asahira et al. 1982). However, the cold treatment, e.g., 1.7 °C for 18 days, has been reported for oranges against B. zonata that was found effective, while against C. capitata and Anastrepha ludens requires 22 days (Hallman et al. 2013; Ndlela 2017). These techniques still were not used against B. tau. So, there is urgent need to set cold temperature for cucurbitae crops against B. tau infestation.

Hot water treatment The hot water treatment (HWT) is defined as Ba treatment of seeds/fruits for the eradication of insect parts or parasites

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(fungus) involving immersion in water at a temperature above the thermal death point of the parasite but below that of the plant parts^ (Hanif et al. 2007). The use of hot water techniques still has not been reported against B. tau in fruits and vegetables, but these techniques have been shown best result against B. dorsalis control. The water temperatures and time vary within the species, i.e., cultivars and between species of fruit and vegetables (Kumah et al. 2011). In Pakistan, Iran, and China, the HWT has been used in mango cultivars against diseases and B. zonata during import and export (Faheem et al. 2012; Jabbar et al. 2011). The hot water treatment is an important part in quarantine issues especially in mango against B. dorsalis and C. capitata (Hernández et al. 2012). So, in the future, the treatment against B. tau in fruit and vegetable would be the designed HWT. There is urgent need to give the education, training, and awareness to the farmers about phytosanitary treatments before exportation and importation of agricultural products.

Soil relative water content technique Water management in the orchard is important cultural techniques to manage the Bactrocera flies at pupal stage. One study was reported in a laboratory condition that is soil relative water content (SRWC) technique was tested against the B. tau. The pupal emergence of B. tau failed in the case of high humidity (80–90%) (Li et al. 2013). In the future, this technique can be used at the farm level. In Indonesia, the different fruit flies have been controlled by sanitation, as they were removed rotten passion fruits from the orchards. About 20% of the yield losses were decreased in the sanitation plot as compared to without sanitation (Hasyim et al. 2007; Hasyim et al. 2016). It is an important way against the attack of Bactrocera spp. in the orchard. Uses of different types of bags on the fruit for 2–3 days intervals are helpful to prevent 40 to 58% losses (Fang and Chang 1984). The bagging of fruits should be done after 3 days anthesis and hanged in the orchard for 5 days for effective control in fruit orchards (Akhtaruzzaman et al. 1999).

Trapping techniques Traps are important tools in the management of fruit flies. The pinnacle is Australian protein bait prepared in Queensland and Thailand. It has been used in the trap to capture the male adults of B. tau and the B. cucurbitae (Chinajariyawong et al. 2003). In Indonesia, the male adults of B. tau have been trapped in a mineral water bottle. The bottle has been baited with 3 ml cue lure on the cotton wick, 1 cm in diameter, and had been replaced every two weeks interval that has been found successful control (Hasyim et al. 2007). Yellow color traps with attractant are most effective for trapping the Bactrocera species (Wee et al. 2018). Ravikumar (2006) have reported that in guava and mango

orchard, the yellow and transparent traps captured significantly higher number of B. correcta than other color (red, green, orange, black, blue, and white) traps. Bactrocera species respond to colors that are similar to host such as orange, yellow, and green. Attraction to yellow and orange color might also be a factor in the attractiveness of fruit flies to these colors (Ravikumar and Viraktamath 2007; Vargas et al. 2009). Further studies are needed to understand the mechanism of attraction of Bactrocera species to different colors. Organic-based attractants are also the best tools for trapping the fruit flies. In Momordica charantia orchard, coconut toddy, coconut solution (two-part coconut toddy/one-part liquid molasses), and coconut toddy-sugar solutions have been used as organic-based attractants used against Bactrocera spp. to find out the behavior among food sources that have been designed in a plastic bottle trap (Barba et al. 2014). The five colors green, yellow, dark yellow, orange, and transparent have been used in egging devices. The green color has been found more attractive to both species of fruit flies (Mahfuza et al. 2011). The 22 Bactrocera spp. have been captured by the mixture of methyl eugenol and torula yeast in guava orchard, and B. tau was one of them (Danjuma et al. 2014). The green color has been found best for trapping B. tau. In the future, different colors might be selected. The color choice varied with the physiological age of B. tau (Guoping et al. 2015). The traps names, i.e., cook and Cunningham (C&C) trap, LT Lynfield trap, CE Capilure trap, CH ChamP trap, ST Steiner trap, ME Methyl eugenol trap, ET Easy trap, SE Sensus trap, JT Jackson trap, TP Tephri trap, and YP Yellow panel trap have been used with each pheromone against the adults of Bactrocera spp. The Jackson traps have been used to capture the fruit flies. The color trapping techniques have been used against B. tau in the laboratory. Chromatic cues considered the important source for trapping Bactrocera flies. The adult of B. tau has been attracted by the wavelengths in the range of 515 to 604 nm (Li et al. 2017). The cue lure has been used in the abovementioned traps to attract the B. tau (Chinajariyawong et al. 2003). Elsholtzia pubescens (Bith) have camphor that has been used in passion fruit as cuelure for the B. tau (Hasyim et al. 2007, 2016). In Fuzhou, China, the B. tau, B. dorsali, B. cucurbitae, and B. scutellata have been sterilized by the application of chemicals like methyl eugenol, cue lure, and trimedlure (Lin et al. 2006). They are environmentally safe and are speciesspecific methods; so, they have been used against different fruit flies species (Teal et al. 2007).

Mixing chemical pesticides with baits The mixture of 0.05% fenthion and 0.1% carbaryl had been used continuously for 3 days after fertilization in the farm that have found useful, in the management of Bactrocera spp. The mixture of molasses and fenvalerate in the form bait spray has been found

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an effective control against B. tau (Saikia and Dutta 1997). The boric acid–borax (toxicant) and protein hydrolysate (attractant) have been used against the B. tau, and 40–98% mortality has been found after 24 h of exposure (Sunandita and Gupta 2001). The B. tau and B. cucurbitae have been controlled by the application of pinnacle (Australian protein bait) with trichlorfon in Thailand (Chinajariyawong et al. 2003). In mango orchard, before ripening fruits, the B. tau has been controlled by application of endrin, sialodrin, diptrex, diazinon, and dimecron. The mixture of carbaryl and malathion has shown the best results (Panhwar 2005). A mixture of molasses, malathion (Limithion 50 EC), and water has been found an effective control against the different fruit flies (Akhtaruzzaman et al. 1999; Ali 2000).

Male annihilation techniques The male annihilation technique (MAT) is the most important control method against the adult’s stage of insect pests, is considered to deplete the males available for mating in a population, and thus breaks the reproductive cycle (Dominiak and Nicol 2012). The methyl eugenol with the ratio 68.5–72.0% and cue-lure with 8.0–8.5% used in Ishigaki Island (300 km away from Taiwan, China) has been found best against the B. dorsalis and B. tau (Ohno et al. 2008). Fruit fly species were collected through methyl eugenol-baited and cue-baited traps in whole Asia (Chen and Ye 2009). The male annihilation techniques (MAT) have been successfully applied in worldwide against Bactrocera species. The maximum and minimum population of fruit flies in a specific region might be detected by pheromone traps (Alyokhin et al. 2001). The Bulbophyllum vinaceum contain phenylpropanoids or lure that was found best pheromone for B. tau (Tan et al. 2006). The pheromone traps help in an indication of species and population size, but these are designed to trap male fruit flies. The B. tau has been trapped by methyl eugenol in Bangladesh (Toledo et al. 2004). The different ways have been chosen as airdrops and manual ground applications, bait stations like, fiberboard, coconut blocks, cotton wicks, and molded paper pulp impregnated with male lures mixed with a toxicant (naled, malathion, or fipronil) (Vargas et al. 2015).

Phytochemical attractant Host plant volatiles or phytochemicals are most useful attractants for insect pests. The volatiles from the different fruits have been detected by gas chromatography–mass spectrometry (GC/MS). Coupled gas chromatography–electroantennogram detection (GC-EAD) has been used to detect the elicited response by insect pests towards the plant’s volatiles. Food baits like fermenting sugars, hydrolyzed protein, and yeasts are

effective to attract the tephritid fruit flies but have some limitations that they also attract the non-target organisms. Host plant volatiles from the leaves, flowers, and fruits are most effective as compared to food baits because it only attracts the target species (Jang 2002). Few studies have been recorded on the Cucurbitaceae volatiles against the B. tau and complex. The fragrance of Bulbophyllum patens that is a strong attractant named zingerone [4-(4-hydroxy-3-methoxyphenyl)-2butanone] has been used to attract the fruit flies. Zingerone has resemblance with methyl eugenol and raspberry ketone (RK). In Malaysia, it has been used to attract the B. tau and other Bactrocera flies via traps. The RK was found most attractive for B. tau (Tan and Nishida 2000). But the for the B. dorsalis, females have been shown strong response as compared to male adults to the nine volatiles (ethanol, ethyl acetate, ethyl hexanoate, hexyl acetate, linalyl acetate, ethyl nonanate, nonyl acetate, ethyl cinnamate, and (E)-β-farnesene) of Terminalia catappa (Siderhurst and Jang 2006). The B. cucurbitae have shown strong response towards the nine-component lure from the cucumber, but the octen-3-ol and (Z)-6-nonenal was the most attractive to the B. cucurbitae (Siderhurst and Jang 2010). Dacus ciliatus is an important pest of Cucurbitaceae like B. tau. Benzyl acetate, hexanyl acetate, (Z)-3-hexenyl acetate, octanyl acetate, (Z)-3-octenyl acetate, (E)-3-decenyl acetate, (Z)-3-decenyl acetate, and (E)-β-farnesene were identified from melon by GC/ MS using GC/MS libraries, retention indices (RI), and authentic standards. All compounds were strongly attracted the D. ciliates (Alagarmalai et al. 2009). However, still, successful reports on phytochemicals have not been reported against the B. tau and complex species in farmer field.

Biological control Parasitoids The Diachasmimorpha albobalteata C., Fopius arisanus S., F. deeralensis F., F. persulcatus S., F. skinneri F., F. vandenboschi F., Opius bellus G., P. fletcheri S., Utetes bianchii F., and three undescribed parasitoids have been reported against B. tau in cucurbitaceous crop (Chinajariyawong et al. 2000; Purcell 1998). The Psyttalia fletcheri in Thailand has been reported against the B. tau in L. acutangula (Ramadan and Messing 2003). In passion fruits orchard, the biocontrol agents against the larvae of B. tau, four species of parasitoid have been reported, i.e., Opius oophilus, O. longicaudatus, O. vandenboschi, and Tetrastichus giffardianus in Asia. On the fallen fruits, their parasitism had been found up to 31.20% (Octriana 2013).

Fungi The use of fungi against Bactrocera spp. is also the best option to control fruit flies; so, the Beauveria and Metarhizium have

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been reported best control against the B. tau (Wang and Ma 2009). The Metarhizium anisopliae and Verticillium lecani have been found entomopathogenic against B. tau (Sun et al. 2014). There is still need for more work on pathogenic fungi against B. tau and complex species.

Use of ants The predator ants are very important biological control agents but still not used against Bactrocera fruit flies. In Sri Lanka, the weaver ants extract mixed with biopesticides and insecticides have been used against the Bactrocera spp. (Peng and Christian 2006). The damage of Bactrocera spp. had been compared in mango orchard as 1% damage has been found with abundant Oecophylla spp., while 24% has been recorded without weaver ants (Van Mele et al. 2007). The weaver ant genus Oecophylla has been found best predators in fruits and vegetable pests (Van Mele 2008). The weaver ant extract is an important deterrent cue against tephritid fruit flies (Adandonon et al. 2009). There is one important aspect of the application of ant as predator: ants are general predators, so there is a need to find out the interaction with other beneficial insects in ecosystems; however, there are good tools in the management of B. tau at pupae stage, so it is most important to know these ants’ roles against Bactrocera fruit flies.

Sterile insect technique The sterile insect technique (SIT) or sterile insect release method (SIRM) is a method of biological insect control and described as BThe inundative release of sterile insects of same species in the wide area to reduce the population^ (Dowell et al. 2000). The application of SITs is environmentally safe and insect-specific and has no negative effects on the non-target insect pests (Pereira et al. 2013). The application of SITs against the B. tau and complex species has not been done under area-wide integrated pest management (AW-IPM) elsewhere, due to less information of regarding SITs or optimal irradiation doses. The sterilization in male adult can be done by insect irradiation by considering the amount of irradiation dose that should not affect the quality of fruits and vegetables (Cai et al. 2018; Follett and Armstrong 2004). The SITs against B. tau and complex species can be applied by using induced large number of sterile males at farm and orchard, considering the competitive mating potential to wild males of that flies, to mate with female flies. Studies of cytogenetic are very important to understand behavior and stability of genetic sexing strains (GSSs) of Bactrocera flies. The GSS development of C. capitata by using the cytogenetics tools for the application of SITs is an interesting topic for scientists (Zacharopoulou et al. 2017). Another technique for developing sterility in Bactrocera flies is the use of beneficial bacteria. However, the useful bacteria (Klebsiella pneumoniae, Citrobacter freundii, and Enterobacter spp.) incorporated with

larval diet have been tested against the medfly; laboratory-based result had shown that high community of these bacteria induced the male adults sterility (Hamden et al. 2013). Application of SITs against the B. dorsalis has been successfully reported in Naoway, Guimaras, Island (Manoto et al. 1996). The successful application of SITs has been reported against the Bactrocera flies by the 6-year FAO/IAEA Coordinated Research Project (CRP) with 31 research institutes from seventeen different countries. They treated the pupae of Bactrocera flies and shipped at farm orchard (FAO 2003; Pereira et al. 2013). The B. cucurbitae was eradicated by the application of SITs in Japan (Koyama et al. 2003). However, there is an urgent need of SITs against B. tau and complex species under AW-IPM programs.

Botanical repellency The botanical extract disturbed the biology of B. tau as ethanol extracts of seed kernel of Melia azedarach L., leaves of Lantana camara L., bulbs of Allium sativum L., and corms of Curcuma longa L. and Azadirachta indica with different formulation effects on pre-oviposition, oviposition period, and hatching ability of eggs. The fecundity of B. tau has been found lower in all treatments, and the result has found that the effects increased with the increase of concentration. The A. sativum, A. indica, and M. azedarach extracts have been found best against B. tau as reduced egg hatching percentages are 27.9, 44.7, and 51.9%, respectively (Thakur and Gupta 2012). The M. azedarach L. seed kernel extract (DSKE) in aqueous or bait forms had been shown as the best effects against B. tau, as they decrease the oviposition rate and gonad development under laboratory conditions. At 2%, aqueous DSKE gave 79.1% oviposition deterrent after 24 h (Sharma et al. 2012). These laboratory studies have shown that DSKE was the most effective biopesticide against the B. tau but still needs further work to confirm at farm and field.

Area-wide integrated pest management Area-wide integrated pest management (AW-IPM) programs base on the social enterprises that are always ready to adopt advanced technologies; they have a tendency to be difficult to implement, especially in terms of management. The cue-lure traps, sterile chemical, and ionizing radiation are the best tools for area-wide management of B. tau (Horn and Wimmer 2003). The area-wide management program by traps and different types of pheromone and food bait for B. tau have been reported in Malaysia (Tan and Nishida 2000), Thailand (Chinajariyawong et al. 2003; Sumrandee et al. 2011), and Bangladesh (Leblanc et al. 2014). The study of genetic makeup and colonization pattern of insect pests is a useful way to find out their invasion pathway that is helpful for area-wide control strategies (Wan et al. 2012). For the establishment of pest-free area, global positioning system (GPS) and

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geographic information systems (GIS), public security for trap installment, and regular survey are helpful trapping tools for Bactrocera species (Hendrichs et al. 2005).

Conclusion This study concluded that B. tau and complex species have created major losses to Cucurbitaceae plants among other agricultural crops. Various studies have been reported on the fitness parameters of B. tau and complex species on artificial and natural diets. But age-stage, two-sex life table study of this complex species is lacking. The B. tau and complex species usually considered vegetable pests due to less concentration of scientist, but this study gives the detailed host spectrum that it also feeds on fruit and wild crops and during off season of vegetables. These species might be surviving on fruits and wild plants/trees. The B. tau and complex species have variables taxonomic confusion. The identification of B. tau has been acquired priorities among taxonomist. This study provides the detailed information on the conventional and molecular techniques for identification of B. tau complex, which would be more helpful in behavioral study of these pests. The most recent techniques like mitochondrial cytochrome oxidase I (mtCOI), 28S rDNA, and expression of isoenzymes are most useful for the identification of B. tau and complex species taxon. Symbiotic relation is very interesting in B. tau. The P. putida (a symbiont) has been used in a laboratory to suppress the population of B. tau. The Wolbachia strains have been detected from the B. tau, but this strain is still not to be used against the B. tau. However, this strain was reported as a virulent strain against other Dipteran pests. Pathogenic symbionts might be used against the B. tau complex for AW-IPM programs. The B. tau and complex species are the most serious quarantine pests and kept strong ability of invasion. This study concluded that the genetic makeup, geographical location, and growth routes of B. tau and complex species are useful to make a better plan for management especially in quarantine program. However, irradiation techniques have been used for treatment of mango attacked by B. tau. We concluded that irradiation, cold temperature, and hot water treatments (HWT) are most suitable techniques quarantine treatment against the infestation of B. tau and complex species in vegetables and fruits. The soil relative water content (SRWC) techniques were found most effective and cheapest technique against the B. tau at laboratory treatment but still not to be used at farms and orchard. This study concluded that water drainage management in farms and orchard would be more effective control against the B. tau by considering the importance of water requirements of fruits and vegetable crops. This study reports the successful use of phytochemicals that strongly affects the host finding and oviposition behavior of Bactrocera flies. This study provides cues for future work

as to identify the phytochemicals that will be more useful attractants for the Bactrocera flies as compared to food-type attractants, such as fermenting sugars, hydrolyzed protein, and yeast, because these are general attractants. But no phytochemical studies were done for the B. tau. The chromatic cue is considered the most effective trapping technique against the Bactrocera flies. Recently, it has been used against the B. tau. Few studies have been done on the parasitoid potential of parasitoid of B. tau. However, Psyttalia and Wolbachia have found most effective against B. tau, but due to less concern of scientist, the proper biological control techniques have not focused against this species. The extract of weaver ant (Oecophylla spp.) has been found effective against the Bactrocera jarvisi. But no previous studies have been done on the weaver ant against B. tau. So, there are urgent needs to the applications of abovementioned control techniques against the B. tau and complex species. Funding information This research was supported by the National Science and Technology Pillar Program of China (2015BAD08B02).

Compliance with ethical standards Conflict of interest The authors declare that they have no conflict of interest.

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