Fitness of Bactrocera dorsalis (Hendel) (Diptera: Tephritidae) on four economically important host fruits from Fujian Province, China

1 Introduction

As one of the most destructive pests of Asian origin, Bactrocera dorsalis (Hendel) (Diptera: Tephritidae) can attack more than 250 host plant species belonging to 46 different families (Vargas et al. 2007), where internal feeding by larvae results in premature abscission of fruit (Vargas et al. 2015). First documented in China on Hainan island in 1934, this polyphagous pest has gradually enlarged its geographical range from southern to northern China due to rapid reproduction and high diffusion potential (Cai et al. 2020). So far, B. dorsalis has been detected in almost every region in China, where it threatens fruit production and agricultural product import and export trade (Cai et al. 2022). In southern China alone, the annual economic losses caused by this pest amount to approximately three billion USD (Wang et al. 2021).

The behavior of Bactrocera flies varies on different host plants (Moreau et al. 2017). Skin texture, shape, size, odor, and color of fruit, foliage, and twigs may influence the host selection behavior of fruit flies (Brévault and Quilici 2007; Drew et al. 2003; Ekesi et al. 2016; Rattanapun et al. 2009). In turn, these host plant differences influence the selection pressure on biological parameters in insects (Moreau et al. 2017). Fruit fly females tend to oviposit in soft-skin fruits (Pagadala Damodaram et al. 2014). Fruit fly larvae consume the flesh of fresh fruit from the inside and feeding injury promotes secondary pathogens that degrade fruit tissues (Xu et al. 2012). Studies have shown that the development and survival of fruit fly offspring were affected by the nutritional level of infested fruits, and also by different levels of toxins, latex and resin in the fruit (Pieterse et al. 2020; Syamsudin et al. 2022; Zhu et al. 2022).

Fundamental and detailed information on fruit fly survival, development and fecundity are necessary to establish reliable integrated pest management (IPM) programs, and are crucial for implementing prevention and control strategies against Bactrocera pests in orchards (Ekesi et al. 2016; Jaleel et al. 2018a). Development and survival of pests are often investigated using life table modeling, which is a tool for population dynamics and ecology research (Huang et al. 2018). To determine the fitness of B. dorsalis on different dominant fruits in southern China, a two-sex life table was applied to investigate demography on guava, mango, wax apple, jujube, pitaya, sweet orange, and pomelo in Taiwan (Huang and Chi 2014) and papaya, banana and guava in Guangdong Province (Jaleel et al. 2018b). Similarly, Zhu et al. (2022) used the two-sex life table to compare the fitness of B. dorsalis on peaches, apples, and oranges to assess the damage risk of B. dorsalis to the dominant fruits in northern China. Elevated fecundity, net reproductive rates, and intrinsic rates of increase in B. dorsalis were observed on prevalent fruits such as pomelo, guava, and peach (Huang and Chi 2014; Jaleel et al. 2018b; Zhu et al. 2022). These findings not only highlight adaptability of this pest in these regions but also underscore the historical difficulties in its management. Furthermore, these studies have demonstrated that population projections can effectively unveil population growth and stage structure. The age-stage, two-sex life table emerges as a promising and dependable tool for pest management and broader ecological studies (Huang and Chi 2014; Jaleel et al. 2018b; Zhu et al. 2022).

Well-known as the land of fruit in China, Fujian Province provides an opportunity of cultivating diverse fruit species due to its suitable climate conditions and agroecological diversity (Cai et al. 2022). However, the weather conditions in Fujian Province are also favourable for the survival, growth, and reproduction of B. dorsalis (Cai et al. 2023). Further, the space- and time-availability of the host crops in this region, as well as their quality and quantity, provide sufficient food resources for the colonization and propagation of B. dorsalis. Following an outbreak of B. dorsalis in 2005 in Fujian Province, great efforts have been attempted to study effective control methods for this pest in this region, e.g., chemical insecticides (Zhang et al. 2014, 2015], 2021]), fruit bagging (Xia et al. 2019), male annihilation technology (Gu et al. 2018; Ji et al. 2013); sprays of environmentally friendly protein bait (Wang et al. 2021), trapping technology (Lin et al. 2022, 2023]; Xia et al. 2020), sterile insect technology (Cai et al. 2018a; Zhang et al. 2021), and mass release of parasitoids (Cai et al. 2017, 2018b, 2019], 2020], 2022]; Lin et al. 2021; Yang et al. 2018). To build a solid ecologically oriented management system for a pest such as B. dorsalis, with a wide host plant range and geographical distribution, a complete ecological database of the pest characteristics on major hosts is required. However, demographic parameters of B. dorsalis on different host plants of economic importance in Fujian province have not been quantified.

The major purpose of this study was, therefore, to investigate the development, reproduction, and survival of B. dorsalis on the main fruit types typically cultivated in Fujian Province, China. These data would yield a more comprehensive understanding of this pest with the ultimate goal being to contribute to constructing an area-wide management strategy for B. dorsalis where different host plants are cultivated.

2 Materials and methods

3 Results

3.4 Impacts of different fruit species on longevity

As shown in Figure 1, both males and females reared from persimmon lived significantly longer than flies reared from navel orange, loquat or carambola (male: F _3,332 = 20.80, P < 0.001; female: F _3,332 = 87.40, P < 0.001), with a lifespan of 147.65 days and 129.70 days, respectively. The lifespan of female fruit flies and the total population that emerged from loquat was the shortest, measuring 115.95 days for females and 110.00 days for the overall population. When comparing the lifespans of male and female fruit flies reared from the same type of fruit, it was observed that females exhibited a longer lifespan than males. However, significant differences were observed on persimmon (t = 3.865, df = 72, P = 0.003), navel orange (t = −3.845, df = 78, P = 0.004), and carambola (t = −2.178, df = 81, P = 0.011).

Figure 1:

Longevity of Bactrocera dorsalis adults on different fruit species. Data are shown as mean ± SEM. Significant differences between different fruit species are indicated by different lowercase letters (P < 0.05). Asterisks indicate significant differences between female and male by an independent t-test at P < 0.05.

3.5 Impacts of different fruit species on pupal weight and adult body size

The pupal weight was significantly greater in pupae from persimmon (17.3267 mg) than from orange (16.4300 mg), loquat (15.1067 mg), and carambola (14.2217 mg) (F _3,36 = 255.00, P < 0.001, Figure 2). As shown in Figure 3, there were significant differences in the size of flies reared from different fruits: body length (BL) (female: F _3,36 = 18.054, P < 0.001; male: F _3,36 = 28.984, P < 0.001), thorax width (TW) (female: F _3,36 = 218.715, P < 0.001; male: F _3,36 = 141.441, P < 0.001), abdomen width (AW) (female: F _3,36 = 143.874, P < 0.001; male: F _3,36 = 145.70, P < 0.001) and wing length (WL) (F _3,36 = 78.157, P < 0.001). The flies with the longest bodies were those reared on persimmon (male and female) and orange (female). In the other variables (thorax width, abdomen width and wing length) the results were more varied by sex and fruit species but males reared on persimmon had a wider thorax and longer wings.

Figure 2:

Pupal weight of Bactrocera dorsalis on different fruit species. Data are shown as mean ± SEM. Significant differences between different fruit species are indicated by different lowercase letters (P < 0.05, LSD test).

Figure 3:

Morphological parameters of Bactrocera dorsalis females and males reared from different fruit species: (A) body length, (B) thorax width, (C) abdomen width, and (D) wing length. Data are shown as mean ± SEM. Significant differences between different fruit species are indicated by different lowercase letters (P < 0.05, LSD test).

4 Discussion

Life population parameters of insect pests are known to fluctuate with various biotic factors. Host plant is an important biotic factor influencing the survival, growth, development, and fecundity of herbivorous insects. Optimum host food for development of insect pests is characterized by the highest survival, shortest life cycles, and highest levels of fecundity (Awmack and Leather 2002). In this research, B. dorsalis could complete its growth, development, and reproduction on navel orange, carambola, loquat and persimmon, which are four dominant fruits of economic importance in Fujian Province. This indicated that the positive factor for the dispersal of B. dorsalis to Fujian Province, a renowned fruit-producing region in southern China, posed a significant risk to the local fruit industries. The detailed parameters of B. dorsalis on four different host fruits examined in this study demonstrated that B. dorsalis exhibited relatively high fitness on persimmon, with similar fitness levels on navel orange, carambola, and loquat. Notably, flies reared on persimmon showed short egg and pupal duration, highest hatching percentage, larval survival percentage, pupation percentage, immature survival percentage, greatest adult longevity, highest fecundity and heaviest pupal weight when compared to flies reared on other fruits. Although the suitability of other tested fruits was relatively lower, they still warrant attention as potential refuge hosts for B. dorsalis, allowing the species to survive until alternative food resource become available, particularly in mixed orchards of fruit with overlapping ripening periods. Furthermore, fruit preference was not investigated in this study and could play a major part in risk to orchards.

In this study, the use of fruit slices as surrogates for whole fruits may introduce some discrepancies when compared to real-world scenarios. Nevertheless, employing fruit slices currently stands as the most appropriate approach for evaluating the suitability of these fruits. This method offers enhanced experimental control by ensuring uniform size, ripeness, and environmental exposure among the samples (Jaleel et al. 2018b). Such consistency is crucial for isolating the effects of the independent variable on the dependent measure, specifically the fitness of the fruit fly larvae in our case. The practicality of using fruit slices is also noteworthy. Whole fruits inherently vary in size, shape, and quality, which could introduce uncontrolled variables into the experiment (Huang and Chi 2012, 2013], 2014]). Our preliminary studies indicated that fruit slices provided a reasonable approximation of larval fitness and host suitability relative to whole fruits. While this methodological choice might not entirely replicate natural conditions, it allows for a controlled assessment of the relative fitness of fruit fly larvae on different host fruits.

Developmental period, body weight, and body size are important key factors for investigating the population dynamics of insect pests, including Bactrocera fruit flies (Waseem et al. 2012). Generally, the developmental period of an insect can be described by the duration of each age-stage (such as egg stage, larval stage, pupal stage, and adult stage) (Ding et al. 2021). The development period of the immature stages seems to vary with food resource. For instance, on papaya, the egg, larval, and pupal periods were 1.72 days, 7.99 days, and 7.40 days respectively. Guava supported slightly different periods: 1.72 days for eggs, 7.72 days for larvae, and 6.07 days for pupae. Banana, on the other hand, exhibited the longest larval period at 9.54 days, with egg and pupal periods of 1.76 days and 7.97 days, respectively (Jaleel et al. 2018b). Furthermore, when B. dorsalis was reared on mandarin orange, the egg, larval, and pupal periods were 2.32 days, 7.84 days, and 10.62 days respectively. On peach, these periods were 2.40 days, 8.13 days, and 9.90 days respectively. And on apple, the periods were 2.72 days, 8.12 days, and 10.30 days respectively (Zhu et al. 2022). In this study, we noted that the egg, larval, and pupal periods of B. dorsalis differed when reared on various fruits. On navel orange, these periods were 1.47 days, 7.64 days, and 9.47 days, respectively. Carambola supported slightly different time frames: 1.40 days for eggs, 7.52 days for larvae, and 10.04 days for pupae. Loquat exhibited periods of 1.43 days, 7.47 days, and 10.25 days for the egg, larval, and pupal stages, respectively. Finally, persimmon showed the shortest egg period at 1.36 days, a larval period of 6.94 days, and a pupal period of 9.08 days. As demonstrated in the current study, differences in the developmental time of immature stages of B. dorsalis are likely due to differences in host plant suitability. The development of immature insect pests is influenced by a range of abiotic and biotic factors, including light, temperature and humidity, and food resource, predation, competition, and interaction of various factors (Chen et al. 2017; Shen et al. 2014). Specifically, when controlling for other factors, the optimal food resources for the development of insect pests are characterized by the shortest life cycles (Awmack and Leather 2002).

Additionally, the pupal weight and body size of fruit flies are considered as an indicator of reproductive capacity. Previous studies have demonstrated a positive correlation between pupal body weight and female fecundity in various tephritid species (Brévault et al. 2008; Duyck et al. 2008; Jaleel et al. 2018c), which is consistent with our findings. In our study, we discovered that fruit flies reared on persimmon exhibited a notably higher pupal weight and laid a greater total number of eggs when fed on this particular fruit. In this study, differences were observed in the body length and width of B. dorsalis reared from four different host fruits, further confirming the influence of varying rearing mediums and food resources. Significant differences in adult longevity between males and females reared from fruit when food was not restricted have been documented elsewhere, where females tend to live longer than males (Huang and Chi 2014; Jaleel et al. 2018b, 2018c; Zhu et al. 2022). This is consistent with our study, where we found that the lifespan of female B. dorsalis reared on persimmon, orange, and carambola was significantly longer than that of male counterparts. The difference might be due to greater energy consumption by males during courtship-calling and mating (Carey et al. 2008).

The oriental fruit fly, an important pest in the genus Bactrocera, typically chooses to oviposit its eggs in fruits, resulting in the hatching larvae feeding on the fruit pulp, leading to the softening and browning of the flesh, ultimately causing fruit to become unmarketable and causing potential economic losses (Zhang et al. 2021). Thus, the parameters of immature duration (particularly larval duration) on different host fruits are important indicators of the direct damage attributed to the fruit-borer insect (Clavijo McCormick et al. 2019). Our research suggests that the larval developmental success of oriental fruit fly differed among fruit types that occur within its host range, which also has been demonstrated with other fruit fly species such as Bactrocera zonata (Saunders), Ceratitis catoirii (Guérin-Méneville), Ceratitis rosa (Karsch), Ceratitis capitata (Wiedemann), Zeugodacus cucurbitae (Coquillett), Dacus demmerezi (Bezzi), and Neoceratitis cyanescens (Bezzi) (Hafsi et al. 2016). In this study, persimmon provided the best larval environment compared to other fruit species considering the numbers of larvae, pupae and adults produced and the immature survival.

Hafsi et al. (2016) suggested that the larval development of polyphagous fruit flies was influenced by the nutritional contents of fruit, especially the content of carbohydrates, lipids, and fiber. Moreover, an earlier study found that lipid and protein were constantly used in different phases of larval-adult transition for C. capitata (Nestel et al. 2003). Therefore, we speculate that this also likely would be the case for oriental fruit fly. Furthermore, it has been reported that the growth, development, and survival of fruit flies are inhibited by some nutrients, toxins, resin, and latex in the fruit (Birke and Aluja 2018; Dominiak and Follett 2024; Rattanapun et al. 2009). For instance, the presence of phenol in the resin in immature fruits of Anacardiaceae was found to reduce the survival of B. dorsalis immatures (Rattanapun et al. 2009). Also, the phenolic components in fruit have been shown to reduce larval development of Anastrepha ludens (Loew) through imposing an anti-nutritive effect (Birke and Aluja 2018). However, the specific effects of the substances in host fruits on B. dorsalis remains largely unknown, and future studies such as composition detection of fruit substances, feeding assays, and molecular studies are needed to enhance our understanding of the factors driving differences in fitness of B. dorsalis on different host plants.

Fitness of flies reared from the four hosts differed, based on the five life table parameters (R _m, λ, R ₀, T, DT). A possible explanation for this result is that the first oviposition attempt and oviposition peak value of B. dorsalis adults on these four tested host fruits varied. Based on demographic theory, if the intrinsic rate of increase (R _m) is greater than zero (0), then it might be the most accurate population parameter to measure the adaptation of an insect to a host food (Southwood and Henderson 2009), which was supported by our results. Greater R _m values also describe the susceptibility of a host to insect attacks, and vice versa (Musa and Ren 2005). The net reproductive rate (R ₀) is an important indicator of population development, where the highest population increase rate is predicted by the number of eggs laid and the fecundity, development and survival of the insect (Huang and Chi 2012). In this study, significantly higher net reproductive rates were observed when fruit flies were reared on persimmon.

The detailed demographic parameters of B. dorsalis on four host fruits confirmed that this pest can successfully complete its life cycle on the four host fruit tested (persimmon, navel orange, loquat, carambola), but the suitability was different. Among these tested fruits, B. dorsalis reared from persimmon displayed relatively high fitness compared to other tested fruits. Persimmon, being extensively cultivated fruits in China, have a high likelihood of becoming new potential host plants for B. dorsalis in the country. Consequently, it is necessary to enhance the monitoring of B. dorsalis in China and conduct further research to investigate the fitness of B. dorsalis on other economically significant host plants, both locally and in other regions. This research endeavor aims to elucidate the mechanisms behind the continuous proliferation of B. dorsalis in recent decades. By doing so, a theoretical foundation can be established for the implementation of integrated pest management of B. dorsalis in orchards.