Introduction
Predatory thrips are beneficial insects that have varying degrees of feeding specialisation on mites. Among them, Scolothrips (Thysanoptera: Thripidae) species are known to be highly specialised in preying on Tetranychus turkestani Ugarov and Nikolski (Trombidiformes: Tetranychidae) (Gheibi and Soleymannejadian, Reference Gheibi and Soleymannejadian2009), a significant pest of several economically important crops. Various species of Scolothrips, including S. sexmaculatus (Pergande) (Coville and Allen, Reference Coville and Allen1977), S. takahashii Priesner (Gotoh et al., Reference Gotoh, Yamaguchi, Makiko and Mori2004), S. indicus Priesner (Ho and Chen, Reference Ho and Chen2001a, Reference Ho and Chen2001b) and S. longicornis (Pakyari, Reference Pakyari2022), have been evaluated for their potential in controlling T. turkestani. Scolothrips longicornis is a natural enemy species that is native to different oriental regions (Pakyari et al., Reference Pakyari, Fathipour and Enkegaard2011a), and is commonly found in eggplant, bean and cucumber fields (Pakyari et al., Reference Pakyari, Fathipour and Enkegaard2011b). Scolothrips longicornis has been identified as an important natural enemy of various phytophagous mites, including T. turkestani, as demonstrated in previous studies (Chazeau, Reference Chazeau, Helle and Sabelis1985; Gheibi and Soleymannejadian, Reference Gheibi and Soleymannejadian2009). Recently, several aspects of its biology, such as functional response characteristics, predation rate, life table, and the influence of temperature on biology and oviposition, have been documented on T. urticae but on T. turkestani is scarce (Gheibi and Soleymannejadian, Reference Gheibi and Soleymannejadian2009; Pakyari et al., Reference Pakyari, Fathipour and Enkegaard2011a, Reference Pakyari, Fathipour and Enkegaard2011b; Pakyari and Enkegaard Reference Pakyari and Enkegaard2012). However, no information is currently available on its population growth performance and age-stage, two-sex life table of S. longicornis on T. turkestani.
Life tables are a critical component of insect population ecology, as they provide detailed information on the development, reproduction and survivorship of a population. The significance of life table methodology and theory in understanding populations has been well demonstrated in ecology, as evidenced by previous studies (Carey, Reference Carey1993). Collecting life history data of species at different trophic levels in a food chain is a crucial task for protecting species (Bevill and Louda, Reference Bevill and Louda1999) and controlling pest populations (Qayyum et al., Reference Qayyum, Aziz, Iftıkhar, Hafeez and Atlihan2018; Satishchandra et al., Reference Satishchandra, Chakravarthy, Özgökçe and Atlihan2019; Zhang et al., Reference Zhang, Guo, Atlihan, Chi and Chu2019). In prey–predator systems, the age structure of predators often undergoes changes due to the presence of non-predatory stages, such as egg and pupal stages. Therefore, it is important to incorporate stage-specific consumption rate and life table information into prey–predator models to understand prey–predator dynamics. This information is also valuable in applying predation theory to biological pest control.
In a study on prey–predator interactions, Hassell (Reference Hassell1978) demonstrated that incorporating the age structure of prey and predator species is a crucial step in understanding the prey–predator relationship at any given time. However, many life tables only consider female individuals (Carey, Reference Carey1993), neglecting the population of males and their prey consumption rates. The traditional life table does not account for stage differentiation. To address this limitation, Chi (Reference Chi1988) developed the age-stage, two-sex life table theory, which considers both males and females as well as changes in development rates between individuals. Determining the demographic parameters in detail is crucial for planning an efficient and cost-effective insect rearing and mass production system for S. longicornis. The main objective of this study was to investigate the temperature-specific effects on S. longicornis and construct an age-stage, two-sex life table under different temperature regimes in laboratory conditions. Additionally, we demonstrated a mass rearing system for S. longicornis, consistent with the approach outlined by Chi and Getz (Reference Chi and Getz1988). The findings of this study are significant, as the age-stage, two-sex life table can be utilised to evaluate the population growth of S. longicornis and provide a useful tool and framework for identifying the optimal temperature range for the mass rearing and production of beneficial insects. This information could also be applicable to other insect species utilised in the biological control of pests, making it an important contribution to the field of insect ecology and biological control-based pest management.
Materials and methods
Rearing of T. turkestani
A colony of T. turkestani individuals were collected from cucumber fields in Pakdasht Tehran province and transported to the laboratory. Freshly cut cucumber leaves were used to rear the mites, which were placed upside down on a layer of damp tissue paper inside a plastic container measuring 15 × 10 × 5 cm in diameter. The lids of plastic containers used for rearing S. longicornis and T. turkestani were modified to include a 2 cm diameter hole covered with fine cloth mesh to provide ventilation. The containers were maintained in a growth chamber at a temperature of 26 ± 0.5°C, relative humidity of 60 ± 10% and a 16:8 (L:D) hour photoperiod.
Rearing of Scolothrips longicornis
A laboratory colony of S. longicornis was initiated using adult collected from the same cucumber field. A single cucumber leaf was put in a petri dish (15 cm in diameter) as explained above, and kept in another growth chamber with similar conditions as above. Scolothrips longicornis population was transferred to fresh cucumber leaves every two days. The predatory thrips colony on T. turkestani was maintained for three months before being used in the experiments.
Test arena
Leaf discs with thin veins from beans (Phaseolus vulgaris L. cv. Sunray) measuring 3 cm in diameter were selected to serve as food for T. turkestani. Each leaf disc was placed upside down on a layer of dampened cotton in a plastic container measuring 6 cm in diameter and 1 cm deep. Ventilation was provided in each container by modifying the container lids as described in the mass rearing and production section above.
Life table study
The experiments were carried out in a laboratory setting at six constant temperatures (±0.5°C), namely 15, 20, 26, 30, 35, and 37.5°C, under a 16:8 h (L:D) photoperiod (Binder KBWS 240) and 60 ± 10% RH. To determine the impact of temperature on the development of S. longicornis, a total of 60 eggs laid by 20 pairs of adults within one day were collected and transferred individually to the test arena. The test containers were kept in the incubator under the aforementioned environmental conditions. Every day, larvae were transferred to individual test arenas and supplied with 30 eggs of T. turkestani as prey (the number of offered preys was determined from preliminary feeding tests). The survival and development rates of S. longicornis were recorded daily. After reaching adulthood, males and females were paired in each test arena. Each pair was provided with 100 eggs of T. turkestani as food daily, and their fecundity and survival rates were recorded until all the predatory thrips died.
Data analysis and S. longicornis population projection for mass rearing
The computer program TWOSEX-MSChart (Chi et al., Reference Chi, You, Atlihan, Smith, Kavousi, Ozgokçe, Guncan, Tuan, Fu, Xu, Zheng, Ye, Chu, Yu, Gharekhani, Saska, Gotoh, Schneider, Bussaman, Gökçe and Liu2020) was used to analyse all datasets according to the age-stage, two-sex life table theory (Chi and Liu, Reference Chi and Liu1985). To estimate the standard errors and variances across biological features and population parameters, a bootstrap resampling method with 100,000 iterations was applied (Huang and Chi, Reference Huang and Chi2012). The paired bootstrap test was utilised to assess the differences between treatments. Table 1 provides the population parameters, corresponding equations used in computation, and definitions of technical terms. The population projection of S. longicornis at different temperatures was performed using the TIMING-MSChart computer program (Chi, Reference Chi2019). Furthermore, the results of the life history study (including fecundity and age-stage-specific survival rates) of S. longicornis were utilised to explore the feasibility of a mass rearing and production system consistent with the approach described by Chi and Liu (Reference Chi and Liu1985).
Table 1. Population and mass production parameters, their definitions and equations used in their calculations
Results
The development time, longevity, survival rate, total preoviposition period (TPOP) and adult preoviposition period (APOP) for each stage of S. longicornis at different temperatures are presented in table 2. The data show that temperature had a significant impact on the development of each stage of S. longicornis. Specifically, the pre-adult development time decreased as the temperature increased and reached its minimum value at 35°C. However, the development time significantly increased beyond 35°C temperature. At 15 and 35°C, the pre-adult development time for S. longicornis was 46.44 and 8.48 days, respectively. The longevity of male and female adults exhibited significant variations across all the temperature regimens, with the longest lifespan observed at 15°C (37.35 and 33.17 days for females and males, respectively) and the shortest at 37.5°C (3.88 and 3.50 days for females and males, respectively). The pre-adult survival rates (Sa) were lower overall (≥0.75) between 15 and 30°C, and significantly decreased at 37.5°C.
Table 2. Mean (±SE) of the development time, total pre-adult duration, pre-adult survival rate (Sa), longevity, fecundity (F), total preoviposition period (TPOP) and adult preoviposition period (APOP) of Scolothrips longicornis reared on eggs of Tetranychus turkestani at six temperatures
Values followed by different letters within the same row are significantly different (paired bootstrap test, P < 0.05). Values in parentheses are number of individuals survived to the next stage.
The total lifespan of both male and female S. longicornis exhibited significant differences across the temperature range evaluated in this study. The longest total lifespan was recorded at 15°C (86.09 and 77.25 days for females and males, respectively), while the shortest lifespan was observed at 37.5°C (13.24 and 11.08 days for females and males, respectively) (table 2). Both the adult preoviposition period (APOP) and total preoviposition period (TPOP) showed significant differences across different temperature ranges and decreased progressively with increasing temperature. The highest value recorded for TPOP was 54.33 days at 15°C, while the shortest was 8.91 days at 35°C. The fecundity of S. longicornis was significantly higher at 26°C (53.32 eggs) compared to other temperatures (table 2). The maximum number of oviposition days (21.31 days) was observed at 15°C, while the minimum (2.65 days) was recorded at 37.5°C. The highest proportion of females (0.67) was observed at 30°C.
The life table parameters of S. longicornis under six different temperature treatments are presented in table 3. The intrinsic rate of increase (r) and the finite rate of increase (λ) were highest at 35°C. The net reproductive rate (R 0) was highest at 26 and 30°C, whereas the lowest was recorded at 37.5°C. The gross reproductive rate (GRR) of S. longicornis showed a nearly linear increase with temperature until 30°C, but then decreased at 35 and 37.5°C. The mean generation time (T) was lowest at 35 and 37.5°C, and highest at 15°C. The expected population growth of S. longicornis over a 60-day period at various temperatures is shown in fig. 1. The second generation of S. longicornis appeared after 50 days at 15°C, whereas at 20, 26, 30, 35 and 37.5°C, eggs of the second generation hatched after 23, 13, 10, 8 and 9 days, respectively, and developed into larvae 1, larvae 2, prepupa and pupa within 60 days. Figure 1 shows the predicted population projection of S. longicornis starting from ten eggs at different temperatures for 60 days. The highest population size was predicted at 30°C, with a total of 772,738 individuals consisting of 529,366 eggs, 59,465 larvae 1, 53,336 larvae 2, 27,167 prepupae, 22,126 pupae, 62,186 females and 19,089 males. The sxj values for S. longicornis showed overlapping ranges at different temperatures, indicating variations in its development rates within and among different stages (fig. 2). The sxj values represent the probability of an individual's survival to age x and stage j. The lx, mx, lxmx and fxj values for different temperatures are presented in fig. 3. The maximum oviposition period was recorded at 15°C, while the highest mx value was observed at 26°C treatment (fig. 3). The exj values of S. longicornis, which represent the expected remaining lifetime of an individual at age x and stage j, were projected to vary across different temperature treatments. The life expectancy of both male and female S. longicornis decreased with increasing temperature up to 37.5°C (fig. 4). The maximum reproductive value of S. longicornis observed was 21.61 at 26°C. The maximum reproductive value of S. longicornis was observed at day 16 under the 26°C treatment. In contrast, the minimum vxj was observed at day 9 under the 37.5°C treatment (fig. 5).
Table 3. The population parameters (±SE) of Scolothrips longicornis reared on eggs of Tetranychus turkestani at six temperatures
Values followed by different letters within the same row are significantly different (paired bootstrap test, P < 0.05).
Figure 1. Population projection over a 60-day period for Scolothrips longicornis reared on eggs of Tetranychus turkestani at six temperatures.
Figure 2. Age-stage specific survival rate (sxj) of Scolothrips longicornis reared on eggs of Tetranychus turkestani at six temperatures.
Figure 3. Age-specific survival rate (lx), age-specific fecundity (mx), age-specific maternity (lxmx) and age-stage-specific fecundity (fxj) of Scolothrips longicornis reared on eggs of Tetranychus turkestani at six temperatures.
Figure 4. Age-stage-specific life expectancy (exj) of Scolothrips longicornis reared on eggs of Tetranychus turkestani at six temperatures.
Figure 5. Age-stage-specific reproductive values (vxj) of Scolothrips longicornis reared on eggs of Tetranychus turkestani at six temperatures.
Table 4 provides information on the stage structure and life table data required for mass rearing and production of S. longicornis to achieve a daily harvest rate of 1000 eggs, based on the estimated number of daily recruits needed for each stage. The maximum daily harvest rate of adults was recorded at 26 and 30°C, with the latter requiring the smallest population size of 686 individuals (consisting of 163 eggs, 40 larvae 1, 50 larvae 2, 34 prepupae, 36 pupae, 293 females and 70 males) among all temperature treatments (table 4).
Table 4. Stage structure (Tj), daily recruits to each stage (Nj), harvest rate (h), daily harvest adult (HA) and total individuals in mass-rearing system (∑ Tj) for sustainable mass production system with daily harvest rate of 1000 eggs (HE = 1000) of Scolothrips longicornis reared on eggs of Tetranychus turkestani at six temperatures
Discussion
The results of this study offer a comprehensive analysis of the demography and population growth and provide new information on projected populations (in a mass production scenario) of S. longicornis, which were fed on strawberry spider mites at different temperatures. The age-stage, two-sex life table was utilised during data analysis to obtain more precise results as it considers stage differentiation and includes both females and males. In contrast to the age-stage, two-sex life table technique, Huang and Chi (Reference Huang and Chi2012) observed that the female age-specific method yields a non-normal distribution and increases variances. Additionally, they noted that this method may overestimate the variability of population parameters, as previously pointed out by Huang and Chi (Reference Huang and Chi2012). Similarly, Chi et al. (Reference Chi, You, Atlihan, Smith, Kavousi, Ozgokçe, Guncan, Tuan, Fu, Xu, Zheng, Ye, Chu, Yu, Gharekhani, Saska, Gotoh, Schneider, Bussaman, Gökçe and Liu2020) demonstrated that errors may arise when using the female age-specific life table in data analysis. In contrast to the findings of this study, Pakyari et al. (Reference Pakyari, Fathipour and Enkegaard2011b) used the female age-specific life table and reported higher values for r = 0.201 d−1, λ = 1.22 d−1, R 0 = 31.09 offsprings/individual, and T = 17.04 days for S. longicornis predator fed on T. turkestani at 26°C. These results reinforce the earlier assertions regarding the discrepancies between the age-stage, two-sex life table, and the conventional female-based age-specific life table. According to the age-stage, two-sex life table method as used in this study, S. longicornis displays varying susceptibility to temperatures. The values of parameters r and λ exhibited a significant increase from 15 to 35°C, while T demonstrated a substantial increase with increasing temperature from 15 to 30°C. The R 0 was similar at 26 and 30°C; however, the GRR of S. longicornis differed significantly between these two temperatures. Yu et al. (Reference Yu, Chi and Chen2005) established the relationship between GRR and R 0 using mathematical evidence. As the GRR parameter does not account for age-specific survival rates, it may not be a suitable population parameter for comparing different treatments such as presented in this study.
The pre-adult development of S. longicornis was observed to decline with rising temperatures. Likewise, in other species, such as S. takahashii Priesner, immature development decreased as temperature increased from 15 to 30°C (Gotoh et al., Reference Gotoh, Yamaguchi, Makiko and Mori2004). These results align with previous research demonstrating that S. sexmaculatus (Pergands) could have a faster development rate at 35°C (Coville and Allen, Reference Coville and Allen1977). Farazmand (Reference Farazmand2020) has reported that the development time for T. turkestani immature stages decreases as the temperature increases. Likewise, this study reveals that the development time of T. turkestani is influenced by temperature. This information could prove valuable in devising effective strategies for the biological control of strawberry spider mites in both field and greenhouse settings. The findings of this study suggest that higher populations of S. longicornis can be generated at low-temperature treatments. This indicates that S. longicornis could be a suitable candidate for controlling strawberry spider mites in low-temperature conditions, such as in the early season or in both indoor and outdoor crops. Additionally, the proportion of female predators produced more females than males across all temperatures tested. As female predators are typically more effective than males (Ling et al., Reference Ling, Xia, Li, Su, Zhong and Li2008), suggesting that a temperature of 30°C may be more effective in controlling T. turkestani using S. longicornis.
Temperature can have a significant impact on the oviposition of predatory thrips. For example, S. takahashii produced more eggs at 25°C (Gotoh et al., Reference Gotoh, Yamaguchi, Makiko and Mori2004), while the maximum fecundity of S. sexmaculatus was recorded at 30°C (Coville and Allen, Reference Coville and Allen1977). Consistent with these findings, the current study showed that the fecundity of S. longicornis was significantly higher at 26 and 30°C, suggesting that these temperatures may be optimal for the oviposition of S. longicornis. Temperature is a well-established factor that can affect various physiological processes in insects, including feeding rate (Pakyari and Enkegaard, Reference Pakyari and Enkegaard2012), body size (Wonglersak et al., Reference Wonglersak, Fenberg, Langdon, Brooks and Price2020), mating behaviour (Conrad et al., Reference Conrad, Stöcker and Ayasse2017), and development and reproduction (Pakyari et al., Reference Pakyari, Fathipour and Enkegaard2011a, Reference Pakyari, Fathipour and Enkegaard2011b). However, the reproduction and development of insects are also influenced by other factors, such as humidity, photoperiod, food availability and larval diapause (Shintani et al., Reference Shintani, Hirose and Terao2011, Reference Shintani, Terao and Tanaka2017). To overcome the challenges associated with studying the complex interactions between various factors affecting insect development and reproduction, the age-stage, two-sex life table method is a useful tool. This method allows for the consideration of all aforementioned factors and strengthens our understanding of these parameters. This new information can be useful in establishing potential rearing and mass production systems. The findings of this study suggest that temperature plays a significant role in promoting the rate of development and reproduction of S. longicornis, and a temperature range of 26–30°C could be considered optimal for mass rearing purposes. A similar approach based on age-stage, two-sex life table can be applied in the development of mass production systems for natural enemy species.
Acknowledgments
The authors thank for the assistance supplied by the Islamic Azad University, Takestan Branch, Iran in managing this research.
