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Review of Zeugodacus tau (Walker) (Diptera: Tephritidae): biological characteristics and control strategy

Abstract

Zeugodacus tau is an important worldwide quarantine pest. The female adults insert their oviposition tube into the fruit epidermis to lay eggs, and the larvae feed inside the fruit. Therefore, the hazard of Z. tau primarily rely on adult egg laying and larval feeding. Zeugodacus tau is widely distributed in China and has caused serious economic losses to the industry of fruit and vegetable. Due to the need for a systematic compilation of basic biological knowledge and the increasing economic importance of fruits and vegetables, this paper systematically summarized the distribution and damage, morphological characteristics, biological characteristics and control strategies of Z. tau. Basic biological knowledge, such as geographical distribution, host species, the characteristics of its damage, spread, and transmission, characteristics of each insect stage, occurrence generations, growth and development, population dynamics, and living habits, will deepen our understanding of Z. tau. Preventive measures, such as risk analysis, prediction of suitable areas and quarantine monitoring, can guide pest prevention for crop production in safe areas. Management measures, such as agricultural control represented by fruit bagging and clean fields, physical and chemical attractants designed and developed by the characteristics of colour, phototaxis and chemotaxis, chemical control based on new green pesticides, biological control supported by predatory and parasitic natural enemies, can fully guide the integrated prevention and control of Z. tau. Depending on the size of the planting management area, both broad-area joint prevention and control as well as localized comprehensive management can be flexibly selected. While ensuring economic benefits, it also takes into account the cost input, and is committed to achieving an economically efficient and long-term green control of Z. tau.

Background

Zeugodacus tau (Walker 1849) (Diptera: Tephritidae) is a serious fruit-boring insect pest (Jaleel et al. 2018; Noman et al. 2021), and the potential economic loss to the Chinese pumpkin industry is as high as ¥23,157,830,800 (Fang et al. 2015). Walker (1849), first reported Z. tau in Fujian, China at which time it was classified as belonging to the genus Dacus. The genus was, however, later revised to Bactrocera and Zeugodacus (Walker 1849; Singh et al. 2010; Liu et al. 2023). Zeugodacus tau is a phytophagous insect, and its larva is latent feeding insect, which can damage various parts of the host (Guo et al. 2023). Zeugodacus tau has a wide range of hosts and strong fecundity and adaptability, and many countries and regions have listed Z. tau as a key quarantine species (Zhou et al. 1993; Hasyim et al. 2016).

As the most basic and important characteristic component of pests, biological characteristics are important reference for establishing integrated pest management (IPM) systems (Liang et al. 2020; Yao et al. 2021a; Duan et al. 2022). Therefore, it is necessary to fully understand the basic biological characteristics of Z. tau. However, early studies on the biological characteristics of Z. tau were relatively broad and did not detail the characteristics of each stage (Batra 1968; Gupta and Verma 1993). The increasingly serious damage caused by Z. tau urges us to further study the biological characteristics and control strategies of Z. tau (Boopathi et al. 2017; Sharma and Tiwari 2020). Therefore, this paper reviews the research progress on the distribution, damage, morphological characteristics, biological characteristics and control strategies of Z. tau, aiming to provide basic guidelines for IPM of Z. tau.

Geographical distribution

Zeugodacus tau has a wide distribution, primarily including China, India, Korea, Japan, Vietnam, Myanmar, Thailand, Laos, Bhutan, Brunei, the Philippines, Cambodia, Nepal, Singapore, Bangladesh, Malaysia, Sri Lanka and Indonesia (Allwood and Drew 1997; Akhtaruzzaman et al. 1999; Ohno et al. 2008; Kitthawee and Rungsri 2011; Prabhakar 2011; Jaleel et al. 2018). In China, Z. tau is primarily distributed in Fujian, Jiangxi, Guangdong, Taiwan, Hainan, Zhejiang, Anhui, Hunan, Hubei, Yunnan, Guizhou, Sichuan, Chongqing, Guangxi, Henan, Shanxi, Shaanxi and Gansu (Fig. 1), and especially in South China, where Z. tau occurs in large numbers, has many host species and causes serious damage (Wang et al. 2007; Sh et al. 2014; Li et al. 2020). In India, Z. tau is primarily distributed in Delhi, Sikkim, Jammu, Punjab, Uttar Pradesh, Kashmir, Uttar Pradesh, Bihar, Kerala, Uttarakhand, Mizoram, Tripura, Himachal Pradesh, West Bengal, Haryana, Karnataka, Meghalaya, Chhattisgarh, Tamil Nadu and Maharashtra (Agarwal and Sueyoshi 2005; Prabhakar 2011; Nair et al. 2017).

Fig. 1
figure 1

Distribution map of Zeugodacus tau (blue-colored areas) in China

Host species

Zeugodacus tau has a wide host range (25 family, 62 species), and it is commonly found in species of the cucurbit family, such as pumpkin and luffa. Other species, such as, guava, jackfruit, passion fruit, heart fruit, mulberry, apple, eggplant, tomato, star fruit, capsicum, string bean, mango and peach, also serve as hosts (Table 1) (Khan et al. 2011; Li et al. 2014; Karnjanaungkool and Julsirikul 2021). For host selection, adult fruit flies primarily use vision and olfaction to search for and identify host plants. Therefore, exploring the selection of host plants by phytophagous insects and the relationships between them will elucidate the damage mechanism of fly pests, and provide scientific evidence for formulating control strategies (Niu et al. 2023).

Table 1 A comprehensive list of plant host species for Zeugodacus tau

Damage symptoms

The oviposition tube of adult female Z. tau pierces into the pericarp and penetrates deep into the flesh to lay egg. This process creates egg piles in a similar manner as other fly pests. Hatched larvae feed on the flesh during development. The skin of the fruit rots and turns brown and black. Severely damaged fruits are often entirely consumed and most rot and fall. Less damage to fruit causes poor growth, which results in deformity thus affecting fruit quality and economic value. Zeugodacus tau is quite active and causes severe damage during its larval stage. Larvae move soon after hatching and continually eat the insides of fruits. Third-instar larvae eat the most and cause the most serious damage (Zhang et al. 1991; Deng 1992).

Dispersal and spread

Zeugodacus tau has strong flight and dispersal capabilities. The adult's flight (feeding, mating, and migration) and the spread aided by air currents are the main pathways for the natural dispersal of Z. tau. Unintentional human factors also play a crucial role. Trade transportation, especially fruit export from endemic areas, provides a way for the long-distance spread of fruit fly eggs and larvae hidden within the fruit. The pests are difficult to be found and have strong concealment (Huang et al. 2005; Gong et al. 2016; Ma et al. 2020).

Morphological characteristics

Eggs

The morphology of Z. tau egg have been described by several authors (Singh et al. 2010; Sharma and Tiwari 2020). According to these researchers, the eggs of Z. tau have similar size of approximately 1.30 ± 0.07 mm × 0.24 ± 0.04 mm and 1.31 ± 0.01 mm × 0.24 ± 0.00 mm (Singh et al. 2010; Sharma and Tiwari 2020). Zeugodacus tau eggs are white, glossy and prismatic in shape. The front end of the egg is pointed, the tail is slightly rounded, and the egg becomes darker as it nears hatching. The eggshells have polygonal dots. Fertilized eggs with thicker shells are translucent and sink in water, and unfertilized eggs with damaged shells are transparent and float (Fig. 2A) (Zhang et al. 1991; Singh et al. 2010; Sharma and Tiwari 2020).

Fig. 2
figure 2

Morphological characteristics of the eggs (A), larvae (B), pupae (C) and adults (D) of Zeugodacus tau

Larvae

Zeugodacus tau larvae are divided into three instars (Zhang and Chen 2018). The body lengths of the first, second and third instars are 3.80 ± 0.07 mm × 0.55 ± 0.10 mm, 4.15 ± 0.73 mm × 1.25 ± 0.19 mm and 8.02 ± 1.02 mm × 1.52 ± 0.17 mm, respectively. First-instar larvae with fewer markings are mostly translucent and less hardened. Second-instar larvae are milky white and slightly sclerotic. Third-instar larvae are yellowish white, with a thin head and a thick tail (Singh et al. 2010). The head is conical, and the mouth hook is black (Zhang et al. 1991). There are two spiracles: the anterior spiracle is annular with 14–18 digitations, and the posterior spiracle is crescentic with yellow holes. There are 3 pairs of long oval valve cracks, each of which is large and radially arranged, and the edges are obviously hardened (Zhang and Chen 2018). In the anal region, the lobes are large and protruded, surrounded by 2–6 discontinuous rows of small spikes. The spike closest to the anal lobe is thick, long and curved. After approximately two weeks, the larvae stop feeding and pupate in sand or soil (Fig. 2B) (White and Elson-Harris 1992; Singh et al. 2010).

Pupae

Zeugodacus tau pupae are oval in shape and approximately 4.90 ± 0.35 mm × 1.95 ± 0.29 mm in size (Singh et al. 2010). Pupae are light yellow at first then gradually darkens to reddish-brown (Deng 1992). The front and rear are round, the sides are slightly curved outwards, and traces of the front and rear spiracles are seen at both ends of the body (Fig. 2C) (Zhang et al. 1991; Singh et al. 2010).

Adults

Adults bodies are yellowish-brown to reddish-brown in colour, with an average length of 6–9 cm. The body length of female adults is generally greater than male adults. There is a red spot on the top of the head, and the head is yellow with 2 medium-sized black oval facial spots. The midsternal midplane is yellowish-brown with 3 yellow bands on the posterior side, and the scutellum is yellow with bristles (An et al. 2011). The wings are approximately 6–8 cm long, with a leading edge width of R2+3 veins that spread to a large brown spot (Singh et al. 2010). The brown transverse band and spotted short band are located at the leading edge of the second and third backplanes and the lateral edge of the fourth and fifth backplanes, respectively. The black longitudinal strip, which is sometimes cut off by the internode, is located in the middle of the backplane of the third to fifth backplanes and forming a “T” shape with the baseband on the basal segment. The feet are yellow, and the middle and hind tibia are reddish-brown or brown (Huang 2017). The end of ventral ovipositor of female adult is pointed, and the third backplane of male adult has a pectinate seta (Zhang and Chen 2018). The posterior lobe of the lateral caudal leaf is long, and the stereoscopic stripes are wide and dark. The time for adult flies to reach sexual maturity varies slightly due to factors such as food, weather and season. In most cases, it takes approximately two weeks to reach sexual maturity. For example, the duration of immature stage decreased with increasing temperature when muskmelon was breeding host. The time to sexual maturity of long-term domesticated strains in the laboratory is significantly shorter than wild strains (Fig. 2D) (Cayol 1999; Liu and Lin 2000; Agarwal and Sueyoshi 2005; Singh et al. 2010; An et al. 2011).

Biological characteristics

Generation

The number of generations of Z. tau varies by regions, ranging from one to several generations per year, with a severe overlap of insect generations. Overlapping may occur within eight generations in Xiamen, five generations in Huangyan, three to five generations in Guangxi, three to four generations in Hangzhou, and one generation in Longdong. Zeugodacus tau overwinter as adults or pupae, and adults overwinter in late November. Reproduction ceases at this time, but there is no diapause phenomenon, and normal adult activity may be observed when temperature conditions become suitable. Pupae that overwintered in soil begin to emerge in late May of the subsequent year (Zhang et al. 1991; Zhou et al. 1993; Zhang and Chen 2018).

Growth and development

Similar to other insects, the development rate of Z. tau is significantly affected by temperature, which is an important factor influencing its growth, development, and reproduction. The starting temperature for development of Z. tau is 13.83 °C, and the effective accumulated temperature is 407.22 °C (Lin and Zhang 1989). The starting development temperatures of Z. tau eggs, larvae, pupae, males and females are 9.34 °C, 15.68 °C, 9.09 °C, 18.27 °C and 23.20 °C, respectively. The accumulated development temperatures of Z. tau eggs, larvae, pupae, males and females are 15.84 °C, 79.79 °C, 161.30 °C, 217.61 °C and 222.07 °C, respectively (Zhang et al. 1991). Different temperatures significantly affect the survival rate, development duration, development rate, fecundity and lifespan of Z. tau (Yuan et al. 2015a). There is an S-shaped curve between growth rate and temperature, and the optimum development temperature is 25–26 °C (Zhou et al. 1994; Zhou 2005). The eggs of Z. tau exhibit weak high-temperature tolerance but strong low-temperature tolerance, and they can tolerate low-temperature stress (Liu et al. 2022).

The growth and development of Z. tau are not only affected by temperature but also influenced by humidity, light, host and space height. With food spoilage or inadequacy, the mortality rates of first- and second-instar larvae increase, but third instar larvae pupate prematurely, resulting in a smaller body size. Mature larvae generally exit the infested fruit, bounce to the ground, and burrow into soil, sand, rocks, and crevices to pupate. Most larvae pupate in soil with a relative water content of 20%-60%. Pupal development duration was shortest in soil with 40% and 60% relative water content, and the emergence rate was highest. When the relative water content of the soil reached 100%, all of the pupae died (Li et al. 2009). The depth of pupation is related to the degree of soil porosity. The general depth of entered soil is 2–3 cm, but the depth of pupation may reach 10 cm when the soil is loose. When a suitable pupation environment cannot be found, pupation may be directly exposed. If Z. tau does not escape from the victim fruit, it may pupate directly in the injured fruit. A medium-long photoperiod is conducive to the growth and development of Z. tau. Southwood classified Z. tau as an ecological responder of the “r” type (r-strategists characteristics: high reproductive rate, low investment, rapid growth, high mortality) (Zhou et al. 1995).

Population dynamics

Due to differences in location and climatic conditions, the population dynamics of Z. tau adults differ between regions. In China, the peak period of adult Z. tau occurrence is throughout the year. The peak period varies from 1–2 (see the numbers in Table 2) and lasts 1–6 months (Table 2).

Table 2 The peak occurrence of Zeugodacus tau adults in several regions of China

Biological habits

Adult Z. tau emergence occurs throughout the day, but especially from 9:00 to 10:00. Adults become sexually mature 8–14 days after emergence, and then the males and females begin to mate. Mating generally occurs at dusk approximately one hour or more after sunset and lasts 408.03 ± 235.93 min or all night (Kabir et al. 1997). On the third day after mating, females begin to lay fertile eggs, which are mostly laid between 16:00 and 17:00. Females Z. tau lay eggs in newly formed wounds and cracks on fruits. When laying eggs on intact fruits, female Z. tau arches its body so that the retractable oviposition tube penetrates the fruit to lay eggs at a depth of approximately 5 mm below the epidermis. An average of 16.01 ± 12.01 eggs per day are deposited. A female Z. tau can lay multiple eggs in the same or multiple oviposition holes. Each hole contains several to dozens of eggs, and a total of 464.6 ± 67.97 eggs may be laid. The oviposition interval varies from 1 to 5 days, and the oviposition period is approximately 50 days (Zhang et al. 1991; Zhou et al. 1993).

The egg stage of Z. tau is 1.30 ± 0.41 days, the first, second and third instar larval stages are 1.20 ± 0.42 days, 1.70 ± 0.48 days and 4.00 ± 0.94 days, respectively, and the pre-pupal and pupal stages are 1.20 ± 0.42 days and 7.00 ± 0.47 days, respectively. The cycle from egg to adult is 14.20 ± 1.69 days. The lifespans of male and female adults are 111.90 ± 26.35 days and 92.56 ± 33.05 days, respectively (Singh et al. 2010). A biological study of Z. tau from India showed that females laid 4–10 eggs alone or in clusters, with the eggs buried vertically or slightly diagonally within the fruit. The pre-oviposition, oviposition, post-oviposition and hatching periods are 10–16 days, 11–28 days, 1–4 days and 1–3 days, respectively. The mean larval stages of the first, second and third instars are 1.4 days, 1.8 days and 2.8 days, respectively, and the total larval stage is 6.0 days. The prepupal stage lasts for 0.9 days and the pupal stage lasted for 8.2 days. The average lifespans of males and females are 28.4 days and 31.6 days, respectively (Ashraf et al. 2022). The time difference of more than a decade in collecting the Z. tau, the different methods used, the differences in food sources, and the differences in experimental methods led to significant differences in the lifespan results of the two studies. Another study on the biology of Z. tau from Nepal showed that the egg-to-pupa stage of Z. tau was 26–30 days (Sharma and Tiwari 2020). The main differences between studies are the time and place of the investigation and the hosts.

Management strategy

With the continuous development of modern agriculture and the deepening of economic and trade globalization, the difficulty and cost of controlling Z. tau have gradually increased. Natural conditions, such as temperature, light and humidity, and ambient conditions, such as the abundance of host species in most areas of China, have created the growth, development and colonization hazards of Z. tau. Therefore, the distribution of Z. tau is becoming quite widespread in China. Because of the current situation and economic importance of Z. tau, comprehensive, specific and targeted control strategies are necessary.

Risk analysis

Conducting a risk analysis of Z. tau and assessing the concentration points of potential risks (Papadopoulos et al. 2024). Implementing scientifically risk management measures based on the level of risk can help to plan and formulate pest control strategies in advance, thereby achieving the best epidemic prevention and control effectiveness (Zhou 2012; Qin et al. 2015; Lv et al. 2016). The risk assessment of Z. tau requires a comprehensive consideration of bioclimatological conditions and geographical environments, and the full utilization of software, such as CLIMEX, GARP, GIS, MAXENT, MED-FOES, IT2FLS and VARMAX for scientific prediction and analysis of the specific suitable living areas and grades of Z. tau in China. This provide basic guidelines for formulating specific quarantine management measures (Wang et al. 2018; Wang 2019).

A computer model of the viability of fruit flies (CMVFF) was used to predict the viability of Z. tau in China. The results showed that the safety, slight danger, danger and high danger zones accounted for 66.72%, 23.88%, 2.24% and 7.16%, respectively (Huang 2010). The Maxent niche model and ArcGIS were used to predict the suitable areas of Z. tau in China according to four types of suitable area indicators. The results showed that the potential distribution areas of Z. tau were primarily central, southern and southwestern China (Wu 2014).

Quarantine and monitoring

Zeugodacus tau has been listed as a key quarantine pest in many countries. In May 2007, Z. tau was included on the List of Imported Plant Quarantine Pests of the People’s Republic of China, issued by the Ministry of Agriculture and Rural Affairs of the People’s Republic of China. Based on current geographical distribution and risk analysis of Z. tau, it is necessary to strengthen the entry quarantine of related trade transport goods and closely investigate the pest situation in suitable domestic areas to guard against pest outbreaks (Reddy et al. 2010; Hasyim et al. 2016). Common quarantine techniques include irradiation, fumigation, soaking, refrigeration and heat treatment (Hossain et al. 2011; Faheem et al. 2012; Follett and Snook 2013). The irradiation dose approved by the International Plant Protection Convention (IPPC) is 150 Gy (Hallman 2012). According to the principle of minimum dose, study demonstrated that 72 Gy and 85 Gy were the lowest radiation doses for Z. tau quarantine, and the inhibition rate of adult emergence was near 100% (Zhan et al. 2015). However, Hossain et al. suggested that radiation doses of 300–350 Gy should be used to ensure adequate killing of the eggs and larvae of Z. tau (Hossain et al. 2006). The use of methyl bromide is common in pest fumigation (Bell 2000). For temperature treatment of Z. tau, Liu et al. showed that the greatest tolerance to heat and cold treatment at the third-instar larvae. The upper limits of chill injury zone of 1-day-old pupae and 3-day-old adults were 2.50 °C and 2.51 °C, respectively, and the lower limit of thermal injury zone were 38.29 °C and 39.39 °C, respectively. This series of temperature parameters related to the cold and heat tolerance of Z. tau provide basis for quarantine treatment (Liu et al. 2022).

The detection and identification of fruit flies is key for control and management of fly pests, and it is an important guarantee for maintenance of non-infected and low-occurrence areas of fruit flies (Zhu et al. 2022). The technical core of fly monitoring includes establishing monitoring locations (considering many factors, such as surrounding host, hanging height, daily maintenance and collection of monitoring data, and setting density according to monitoring purpose), selecting of lures (e.g., sex lures, food lures and synthetic baits) and matching traps (e.g., dry, wet and mixed dry and wet types) (Kong et al. 2021). Since 2000, the Guangxi Entry-Exit Inspection and Quarantine Bureau, which relies on the work of quarantine fly monitoring performed by the General Administration of Quality Supervision, Inspection and Quarantine of the People's Republic of China (AQSIQ), has used chemical information, remote sensing and biotechnology for monitoring and investigation, and it has established a three-dimensional monitoring system for fruit and vegetable fly pests. Nearly 3000 fly monitoring points have been established at ports under Guangxi’s jurisdiction (Lu et al. 2014). The technology for automatic monitoring of fruit fly pests based on electronic sensors is increasingly popular. Compared to traditional methods, automatic methods are time- and labour-saving, efficient and accurate and provide more options for the monitoring of fruit flies (Lello et al. 2023).

Agricultural practices

Fruit bagging

Bagging can protect fruit from pests, birds, sun exposure, pathogens, physiological diseases, pesticide residues and abrasions and further change the microenvironment of fruit development to provide multiple beneficial effects on external and internal quality (Buthelezi et al. 2021). Different types of protective bags are selected according to the economic value of growing fruits and vegetables, and the packaging materials such as paper, plastic and composite (Sharma et al. 2014). In general, the input cost of protective bags is proportional to economic value of growing fruits and vegetables (Sarker et al. 2009; Ali et al. 2021). For fruits with high economic value, paper bags may be used to protect the fruits at young stage and guard against damage of Z. tau (Mao et al. 2020).

Clean farmland

Green and yellow fruit with obvious egg laying traces and larval infestations should be removed quickly, as well as fallen insect-infected fruit. The damaged fruits are burned, buried deep or soaked in medicinal liquid to prevent the spread of Z. tau (Zhang and Chen 2018; Ma et al. 2020). For high-quality organic agriculture plantations, weed removal is also an important part of cleaning fields. It can not only reduce the impact of weeds on crop yield but also significantly clear excessive hosts of pests, which plays a crucial role in the development of clean organic agriculture (Abouziena and Haggag 2016).

Deep ploughing

Digging deep into orchard soil can destroy the overwintering sites of insect pupae and expose more pupae to the surface. The pupae either die because they cannot adapt to the low temperatures, or they are eaten by birds and other animals, thereby reducing the base number of overwintering population (Kumar et al. 2020). Before the emergence of residual overwintering Z. tau pupae, ground spraying of chemical agents to kill pests (vegetables using ground cover film) may compensate for the defects of deep ploughing (Verghese et al. 2004; Wang and Zhang 2009).

Scientific management

Management measures, such as free-range poultry, timely pruning, rational distribution, selection of early (late) ripening and insect-resistant varieties, crop rotation, optimal density planting, improvement of cultivation can reduce the incidence of farm pests (Liang 2013). Raising chickens, ducks and geese in a free-range manner not only helps to clear the fields of pests and weeds, but also the manure produced by poultry can increase soil fertility. However, when using organic fertilizer, attention should be paid to its full fermentation and maturation treatment to fully increase fertility and maximize fertilizer efficiency (Clark and Gage 1996; Zhou 2022). A scientific and reasonable planting plan should be formulated based on the specific situations for fruits and vegetables, and the optimal planting density should be selected to ensure sufficient growth space. Reasonable crop rotation improves the soil environment and its physical and chemical properties, and promotes crop growth. These measures fully utilize limited land resources and improve utilization efficiency (Bullock 1992; Wang et al. 2021b). Planting early (late) ripe varieties of vegetables and using mulch film for cultivation can stagger the fruit set period of vegetables with the egg-laying period of fruit flies, while effectively suppressing the emergence of adult flies. Regular pruning of fruit trees to remove bad leaves and branches enhances tree strength and its ability to resist pests and diseases. Scientific and effective management adds new vigour and vitality to agricultural control measures.

Physicochemical induction

Sticky traps

Sticky traps are effective pest control tools based on the differences in colour preferences of insects. The yellow board, as a representative classic sticky trap, attracts a variety of pests using the pest’s taxis to yellow. The bait-killing agent yellow board and sex pheromone yellow board effectively and stably control fly pests (Wu et al. 2007; Yao et al. 2021b; Yan et al. 2023). The yellow board may be reasonably improved by changing its shape and adding windproof devices, such as fixed holes and metal strips, which improve the efficiency of attracting insects and reducing the trap rate of natural enemies (Huang 2021, 2022; Tu et al. 2022). However, newly emerged adult Z. tau prefer green and avoid red (Zhou et al. 2009). Yellow and yellowish-green are suitable for attracting Z. tau at ages of 5–7 days and 30–32 days, respectively (Li et al. 2017a, b).

Phototaxis

Based on the phototaxis of Z. tau, frequency trembler grid lamps may be used at night to trap adults and other phototactic pests. Frequency trembler grid lamp trapping is low cost and produces marked effects. The switching of frequency trembler grid lamp with light control is automatic, time-saving, labour-saving, convenient and fast, and it is an important pollution-free pest control method (Wang and Zhang 2009).

Chemotaxis

The active substances in male and bisexual lures play important roles in the field of fly pest control. Male lures have strong species-specific properties, and bisexual lures attract a wider range of pests (Cai et al. 2018b). Cue lure (CL), raspberry ketone (RK) and zingerone (ZG) attract male Z. tau adults. CL is a standardized lure for the monitoring and trapping of Z. tau (Tan and Nishida 2000, 2005; Ohno et al. 2008). As early as 1984, an outdoor CL activity test of home make was performed in nursery of the Fujian Institute of Subtropical Botany on the outskirts of Xiamen. The results showed that CL attracted the largest number of Z. tau (Zhang and Lin 1987). A study in Indonesia showed that camphor, which is the main component of the extract of Elsholtzia pubescens, had a similar attractant effect as CL, and it has been used in passion fruit orchards to trap Z. tau (Hasyim et al. 2007, 2016). From 2008 to 2015, Li et al. used McPhail traps in an 8-year investigation of the population dynamics of Z. tau in northern Jiangxi Province. The results showed that Z. tau accounted for 68.12% of the total population trapped by the lure, and Z. tau introduced from Fujian to Jiangxi Province was the dominant population in invasion region (Li et al. 2020). Boopathi et al. investigated the species of fruit fly in Indian Himalayas using three types of fly traps equipped with CL and reported the relative abundance and seasonal population dynamics of Z. tau-infested tomatoes in this region for the first time (Boopathi et al. 2017).

The bisexual lure was developed based on the fact that fruit flies need to eat a certain amount of sugar and protein during the growth and development process to achieve synchronous control of male and female adults (Wang et al. 2021a). As an economical and safe lure for fly pests, protein baits have been studied for a hundred years. Fu demonstrated that protein baits effectively controlled Z. tau by hanging pot trapping and spot spraying (Fu 2011). Protein baits mixed with borax and trichlorfon and syrups mixed with arsenic and fenvalerate exhibited great control effects on Z. tau (Saikia and Dutta 1997; Chinajariyawong et al. 2003; Sunandita and Gupta 2001; Zhang 2014). With further research, solid lures with longer durations and different colours and shapes have been continuously produced and applied. A wax-based bait station with a mixture of sugar and toxic substances had excellent control effects on fly pests. However, more research is needed to develop new lures for Z. tau (Heath et al. 2009; Lin et al. 2022; Gan et al. 2023).

Host plant attractants

The use of plant resistance, plant extracts, plant secondary chemicals and their active components plays an important role in the control of fly pests. Li et al. confirmed that cucumbers, pumpkins and loofahs were the preferred oviposited fruits of Z. tau compared to citrus, winter and bitter melon (Li et al. 2007). Wang et al. studied the use of six kinds of fruits to induce female Z. tau adults to lay eggs and showed that ginger melon produced the most eggs from Z. tau (Wang et al. 2009). Yuan used a Y-type olfactometer to determine the effect of crude extracts from eight host plants on attracting Z. tau adults. The results showed that the crude extracts of eight host plants had obvious attraction effects (with relative attraction rates greater than 30.00%) on female Z. tau adults in their peak egg laying period. The hexane (40.83%) and ethanol (38.33%) extracts of papaya from Caricaceae, the ethyl acetate (32.50%) extract of pepino melon from Solanaceae and the ethyl acetate (31.12%) extract of pumpkin from Cucurbitaceae were obtained (Yuan 2022). Melia azedarach seeds, Lantana camara leaves, Allium sativum garlic heads, Curcuma longa bulbs and Azadirachta indica bulbs were fed different concentrations of ethanol extracts. With increasing feeding concentration, the phenomenon of delayed oviposition of Z. tau adults became more obvious (Thakur and Gupta 2012). Yuan et al. used the Y-type olfactometer and demonstrated that (E)-3-nonene-1-ol, n-hexadecane, octadecene and cili-3-hexene-1-ol had good attractant effects on Z. tau adults, and may be further developed as components of plant-derived lures for Z. tau adults (Yuan et al. 2023). Using Y-type olfactometry, Jia et al. used gas chromatography-mass spectrometry (GC‒MS) to identify and analyse the volatile compounds of Solanum muricatum and demonstrated that nine compounds induced behavioural responses in adult female Z. tau (Jia et al. 2023).

Symbiotic bacteria

Symbiotic microorganisms in insects account for 1–10% of insect biomass, and symbiotic microorganisms play important roles in insect biological traits, diversity, ecological adaptability and stress resistance (Wang et al. 2021c). During long-term evolution, a unique reciprocal relationship formed between various microorganisms colonizing the gut of insects and their hosts, which provide unique survival advantages for the hosts (Feldhaar 2011; Jang and Kikuchi 2020). Bacteria are important symbionts of insect gut microbes, and their diversity is primarily influenced by host diet, developmental stage and environmental habitat (Yun et al. 2014; Luo et al. 2018). Forty-one species of Enterobacteriaceae bacteria were obtained from the intestinal bacteria of sexually mature Z. tau adults. Enterobacter, Providencia and Serratia were identified in the guts of male and female adults. All of the tested autoclave liquids had a significant attraction effect on Z. tau, and four strains of Enterobacterium had a good attraction effect on 8-day-old and sexually mature Z. tau (Luo 2016). Noman et al. identified intestinal bacteria in larvae, pupae, and male and female adults of Z. tau. Proteobacteria was the most representative phylum in each stage except larvae, and Firmicutes was the dominant phylum in larval stage. Enterobacter, Providencia, Klebsiella and Pseudomonas were identified in male and female adults, and Enterobacter was the main genus and had a positive impact on survival and reproduction of Z. tau (Noman et al. 2021). Wolbachia, which can kill males, feminize, induce parthenogenesis, and induce cytoplasmic incompatibility, can also infect Z. tau. Further exploration of the relationships between Wolbachia and Z. tau will reveal more symbiotic bacteria for the control of fruit fly (Liu et al. 2006; Kitthawee and Dujardin 2010; Mateos et al. 2020; Zheng et al. 2022).

Sterile insect technique

Since Knipling showed that the release of large numbers of sterile males effectively suppressed the natural Cochliomyia hominivorax population, the usefulness of the irradiation-based sterile insect technique (SIT) in the field of pest control has been gradually examined (Knipling 1955). Studies on the use of SIT for controlling Bactrocera dorsalis, B. tryoni, Ceratitis capitata and Z. cucurbitae were performed earlier and in larger numbers (Steiner et al. 1965, 1970; Andreawartha et al. 1967; Harris et al. 1986). The results of related studies on Z. tau showed that the proportion of infertile and malformed flies increased with increasing radiation dose. When virgin females mated with irradiated males at a certain proportion, the quality of offspring gradually deteriorated as the proportion of irradiated males increased (Islam et al. 2012). The radiation tolerance of Z. tau increased with increasing age and developmental stage (Zhan et al. 2015). Pan et al. showed that the irradiation effect of 60Co at 100 Gy on the pupae of Z. tau 2 days before emergence was ideal for SIT (Pan 2013; Du et al. 2016). The fecundity and egg hatching rate of female Z. tau adults were significantly decreased by irradiation with 60Co-γ above 150 Gy, and the ovaries and fallopian tubes of female adults became smaller. When the eggs, first- and third-instar larvae and pupae of Z. tau were treated with 250–350 Gy of 60Co-γ, complete F1 sterility was achieved. Total F1 death was achieved in all ages of Z. tau treated with 400 Gy (Cai et al. 2018a; Yang et al. 2018).

Chemical control

Organophosphates, neonicotinoids and pyrethroids exhibited good controlling effects on Z. tau (Ao et al. 2019). Using dipping method, Mao et al. determined the virulence of 12 insecticides against Z. tau pupae and the effect of bivalent mixture. The test showed that dipterex and phoxim (1:9) and phoxim and chlorpyrifos (9:1) significantly controlled Z. tau (Mao et al. 2012). Cai et al. tested the activity of 10 pesticides single agents and 5 mixed preparations against Z. tau and determined that the activities of organophosphorus, microbial-derived insecticides, emamectin benzoate and phoxim mixtures were greater (Cai et al. 2014). According to the type, dosage form and concentration of insecticides, there are a variety of combinations to select in Z. tau control system (Table 3). To prevent the development of pest resistance to pesticides, different types of pesticides can be applied alternately. For centralized and continuous vegetable gardens, vegetable farmers can be organized to try large-scale joint prevention and treatment (Hasyim et al. 2007; Zhang and Chen 2018; Mao et al. 2020). It is worthwhile to mention other side effects of irrational use of those broad-spectrum pesticides such as organophosphates, e.g. pollution to environment, non-target effects to natural enemies, and thus stress potential pesticide risk to be reduced or avoided.

Table 3 Guidelines for the use of alternative agents for the chemical control of Zeugodacus tau

Biological control

Fungi

Entomogenous fungi first appeared in ancient Greek mythology, and China was one of the first countries to apply these resources (Wang et al. 2005). As an important pathogen of crop pests, entomopathogenic fungi have the advantages of a wide host range, numerous species, easy culture, safety and effectiveness, sustained damage control, no damage to natural enemies, and low resistance (Shah and Pell 2003; Li et al. 2017b; Liu 2017). The fungi Beauveria, Metarhizium and Verticillium lecanii play important roles in control of fly pests (Sookar 2013; Faye et al. 2021). Sun et al. tested the virulence of the MZ041024 strain of V. lecanii against three stages of Z. tau in laboratory and confirmed that the strain was most virulent to Z. tau adults, followed by pupae, and was the least virulent to larvae (Sun et al. 2013). Yuan et al. used the Beauveria bassiana strain XD0104015 to test the pathogenicity of Z. tau in laboratory and showed that the tested B. bassiana strain had strong pathogenicity against larvae, pupae and adults of Z. tau (Yuan et al. 2015b).

Predators

Compared to the presence of Oecophylla longinoda, fruit flies preferred to spend more time landing on trees without O. longinoda. Under greenhouse conditions, ant pheromones significantly affected the number of eggs laid and the number of pupations of flies on fruit (Adandonon et al. 2009). The activity of O. longinoda and O. smaragdina may reduce the damage of fruit flies (Ativor et al. 2012). Wong et al. found that each larva of C. capitata could be attacked by seven Iridomyrmex humilis species in laboratory, with a fatality rate of 50% (Wong et al. 1984). Campolo et al. showed that Tapinoma nigerrimum was influenced by larval movement and olfaction cues when it preyed on the larvae of C. capitata (Campolo et al. 2015). Therefore, as social predators, ants have a certain biological control potential for fruit fly pests, and further research on predatory ants and Z. tau is needed (Peng and Christian 2006; Mele et al. 2007; Sinzogan et al. 2008).

In rainy, low-temperature and high-humidity years, from July to September, when the temperature is approximately 23 °C, the humidity is greater than 75%, and the monthly sunshine is less than 131 day degrees, the number of spiders in the field is large, the activity is frequent, and the desire to hunt is strong. Manager may create a habitat for spider activity by planting straw and hanging grass and promote the construction of a web for spider mites to prey on target fly pests and reduce the possible damage due to Z. tau adults and larvae (Fan 2011). Other predatory enemies, such as bugs, mites, ladybugs, earwigs, lacewings, and vertebrates, including birds and frogs, should also be explored for the prevention and control of Z. tau (Chen et al. 2023).

Parasitoids

Diachasmimorpha anshunensis is a larval dominant parasitoid that is suitable for rearing on honey at 22–25 °C. Diachasmimorpha anshunensis prefers to parasitize Z. tau larvae at three instars, with a recommended duration of eight hours. The peak egg-laying period for D. anshunensis females was 2–7 days after emergence, and the average daily egg-laying capacity of D. anshunensis females was the highest (18.71 eggs per female) three days after emergence. This newly discovered native larval parasitoid is highly important for the control of Z. tau in China (Shi 2022).

Spalangia endius is a multi-host parasitoid that has a good parasitic effect on fruit fly pupae. The adults lay eggs on Z. tau pupae of different ages and develop into adults, but the parasitism rate of S. endius decreased with increasing of Z. tau ages. Three- and four-day old pupae of Z. tau were used as hosts to develop into adults, which had a shorter developmental duration and a longer lifespan of female offspring (Liu et al. 2016b).

The ability to select and adapt to multiple hosts is a necessary prerequisite for survival and reproduction of polyparasitic parasitoids, and host selection behaviour is result of long-term adaptation to each host (Liu et al. 2016a). After switching hosts, S. endius feeding on Z. cucurbitae preferred to parasitise Z. tau, and S. endius feeding on Z. tau and Z. cucurbitae were more easily adapted to Z. cucurbitae and Z. tau, which suggests that S. endius prefers hosts with overlapping ecological niches when switching hosts (Li et al. 2022). For both hosts with overlapping ecological niches, more studies of S. endius have been performed on the control and prevention of Z. cucurbitae, and more in-depth assessments of relevant aspects of Z. tau are urgently needed (Beddington et al. 1978; Li 2016; Li et al. 2021).

Summary and prospects

From Dacus to Bactrocera, and then to Zeugodacus, the taxonomic status of Z. tau has been continuously adjusted at the genus level, while Zeugodacus was a subgenus before it became a genus. In terms of both geographical distribution and morphological characteristics, the three genera exhibit a high degree of similarity. However, due to regional differences, the abundance of different genera varies, and the host plant preferences of fruit flies from different genera are also distinct. Most of the current research focused on the genera Bactrocera, such as B. dorsalis and B. tryoni. There are relatively few studies on the other two genera. Systematically organizing their biological knowledge and fully understanding and mastering their distribution, damage, and morphological characteristics will help formulate more comprehensive and targeted pest management strategies (Suckling et al. 2014; Khan et al. 2016).

Economic and practical trapping and killing strategies play important roles in the monitoring and control of Z. tau. With the continuous development of trapping technology, compared to the original single-liquid trapping agent using simple transparent plastic bottles, the current types of traps and lures are increasingly diversified. The possibility of joint use of various control technologies has made the construction of IPM systems a development trend (Abd-Elgawad 2021). In future agriculture, unmanned, intelligent, digital, intensive, large-scale and mechanised pest control programs with unified leadership and overall planning will aid in the integrated management of fly pests (King 2017).

As an uninjurious long-term pest control strategy, biological control is highly important for the establishment of an IPM system (Waage and Greathead 1988; Bailey et al. 2010; Barratt et al. 2018). There are only a few reports on the application of fungi and parasitic and predatory natural enemies for biological control of Z. tau, and more in-depth studies are needed to investigate the possible application of entomopathogens (bacteria, viruses and nematodes) and natural enemies (bugs, mites, lacewing, ladybugs, and earwigs) for the green control of Z. tau (Lacey et al. 2015).

Notably, Z. tau, which is famous for damaging melon crops, has been the subject of fewer research reports than Z. cucurbitae, which also prefers melons. To a certain extent, successful cases of Z. cucurbitae control can guide the management of Z. tau (Dhillon et al. 2005; De Meyer et al. 2015; Diksha et al. 2022). Therefore, the author suggests that more in-depth research and comprehensive management of Z. tau be performed from the following aspects. First, based on the prediction of suitable areas, risk analysis and real-time monitoring, the distribution and spread of Z. tau should be updated in a timely and effective manner, and a regional real-time monitoring and reporting system for Z. tau should be established. Second, we summarised and integrated important information on the biology and ecology of different geographic populations of Z. tau to pave the way for formulating of more targeted management measures. Third, based on existing control methods and control experience of other Tephritidae pests, novel ideas are constantly integrated into control strategies for Z. tau to achieve long-term goal of establishing and improving an integrated control system. Last but not least, there is a sincere hope that the integrated management of Z. tau can take advantage of the rapid development of big data and artificial intelligence to provide an example for building a new era of intelligent pest management and service platforms.

Availability of data and materials

The data used to support the findings of this study are included in the article.

Abbreviations

IPM:

Integrated pest management

CMVFF:

Computer model on viability of fruit fly

AQSIQ:

General administration of quality supervision, inspection and quarantine of the People’s Republic of China

IPPC:

International Plant Protection Convention

CL:

Cue lure

RK:

Raspberry ketone

ZG:

Zingerone

SIT:

Sterile insect technique

EC:

Emulsifiable concentrate

SP:

Soluble power

CT:

Crystal

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This work was funded by the National Key Research and Development Program of China (2023YFD1400700) and the International Atomic Energy Agency Coordinated Research Project (IAEA CRP D41027).

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Liu, X., Ji, Q. Review of Zeugodacus tau (Walker) (Diptera: Tephritidae): biological characteristics and control strategy. CABI Agric Biosci 5, 90 (2024). https://doi.org/10.1186/s43170-024-00284-5

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