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11 January 2017 Relative fitness of avermectin-resistant strain of Neoseiulus cucumeris (Oudemans) (Acari: Phytoseiidae)
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Abstract

The predacious mite Neoseiulus cucumeris (Oudemans) is an effective natural enemy of pest insects and mites. To identify the relative fitness of the avermectin-resistant strain of N. cucumeris, the life history parameters of avermectin resistant (R) and susceptible (S) strains of N. cucumeris were observed under experimental conditions (25 ± 1°C, 90 ± 5% RH and L: D = 14:10 h) feeding upon Tetranychus truncatus (Ehara). Fertility, net reproductive rates (R0 /female), intrinsic rates of increase (r/day) and development durations of the two strains were compared. The abamectin resistant strain of N. cucumeris had significantly shorter developmental duration and longevity than the sensitive stain. However, the mean fecundity of the resistant strain was significantly higher than that of the susceptible strain. The net reproductive rate (R0=30.3833 offspring), the intrinsic rate of increase (r=0.2231 d-1) and the finite rate of increase (λ=1.2499 d-1) of the resistant strain were only slightly higher than those of the susceptible strain (R0=29.5333 offspring, r=0.2130 d-1, λ=1.2373 d-1); the differences were not significant. However, the mean generation time (T=15.1768 d) of the resistant strain was significantly shorter than that of the susceptible strain (T=16.0314 d).

Introduction

Relative fitness is an important index to evaluate biological changes in populations of pesticide resistant strains and is used to measure the adaptability of insects to pesticides. Relative fitness is calculated as the net reproductive rate (R0) of resistant populations divided by the net reproductive rate of susceptible populations (Liu & Lu 2016). Compared to the sensitive strain, pesticide resistant strains of arthropods usually have lower fertility and longer development periods (Georghiou 1972; Janmaat and Meyers 2011). There is much research concerning the relative fitness of important agricultural pests and the health of pesticide resistant populations (Meng et al. 2007; Feng et al. 2009; Chen et al. 2011a; Abbas et al. 2012, 2014; Mansoor et al. 2013; Zhon et al. 2015).

The predacious mite Neoseiulus cucumeris (Oudemans) is an effective natural enemy of pest insects and mites (Gillespie, 1988; Zhang et al. 2006; Zhang, 2006; McMurtry et al. 2013). However, this predatory mite is very susceptible to insecticides (Chen et al. 2004, 2005, 2006, 2007a, 2007b, 2010; Zhang et al. 2011). This shortcoming has severely restricted its scope of use and effectiveness in pest control. We had bred an avermectin-resistant strain of N. cucumeris; the LC50 of susceptible strain was only 2.5270 mg/L, whereas that of the resistant strain was increased to 163.2930 mg/L.

The resistant multiple of resistant strain was 64.62-fold compared to susceptible strain. Routine use concentration of avermectin was 3.60–18.00 mg/L. The LC50 of chlorpyrifos to susceptible strains and resistant strains were 7.4116 mg/L and 205.6392 mg/L respectively, and the resistance multiple was 26.75-fold. The LC50 of imidacloprid to susceptible strains and resistant strains were 132.5151 mg/L and 2497.8167 mg/L respectively, and the resistance multiple reached to 17.85-fold (Chen et al. 2011b, 2013). To date, we have not reported on the relative fitness of the resistant strain of N. cucumeris. Thus, we compare the life history parameters between the resistant strain and the susceptible strain, to identify the relative fitness of the avermectin-resistant strain of N. cucumeris. Predatory mites with pesticide resistance will be employed to improve the biological control performance and the coordination of chemical control with biological control.

Materials and Methods

Mites

The susceptible (S) strain of N. cucumeris was purchased from BCP (BCP Certis©, UK) and was reared in the laboratory for at least ten years with Aleuroglyphus ovatus Troupeau supplied as prey at 25 ± 1°C, 90 ± 5% RH and a 14:10 h (L:D) photoperiod at the Institute of Plant Protection, Fujian Academy of Agriculture Sciences, China. The avermectin-resistant (R) strain of N. cucumeris was established after 60 generations selection of the susceptible strain (S) by using avermectin. By then, the LC50 (median lethal concentration) of resistant strain was 64.62-fold compared to susceptible strain (Chen et al. 2011b). Tetranychus truncatus Ehara was collected from a tomato garden in Fuzhou, Fujian Province, China, and was reared on bean plants (Phaseolus vulgaris L.) in the laboratory for at least two years.

Experimental cage

Each experimental cage was constructed from an acrylic plate (30.0×25.0×1.5 mm) with a hole (6.0 mm in diameter) in the center, a transparent glass plate (30.0×30.0×1.0 mm) and a sheet of black nylon screen mesh (800-mesh). The nylon screen mesh was melted and bonded onto the hole of the acrylic plate with heat-sealing. The acrylic plate and the transparent glass were clamped together with two clips on either side of the acrylic plate with a rearing space for the predatory mites (Toyoshima & Amano 1998; Ji et al. 2015a; Ji et al. 2015b).

Developmental duration

A single egg (approx. 8 h old) of each strain of N. cucumeris was introduced into an experimental cage together with T. truncates, and each strain had 60 replicates. The experiments were conducted in a rearing chamber under a 14:10 h (L : D) photoperiod at 25± 1 °C and 90±5% RH. The development of the mites was observed twice daily, at 8 a.m. and 5 p.m., and the stage of development was recorded at each observation. More fresh T. truncatus were added if the food in cages became scarce during the observation period.

Life table study

A newly emerged female of each strain from the development experiment (several females reared in parallel to the developmental duration experiment) was mated with an unmated male (3 days old) for one day in the experimental cage. The male was removed the following day. Five days later, the female was again allowed to mate with another unmated male (3 days old) for one day (Ji et al. 2015b). The predators were provided sufficient amounts of T. truncatus eggs daily. The oviposition and survival of the predatory females were observed daily until death. The sex ratio of the offspring was determined by rearing all eggs deposited by the predator females to adulthood with T. truncatus as prey. The experiments were maintained in rearing chambers under a 14:10 h (L: D) photoperiod at 25±1°C and 90±5% RH. The experiments were replicated 35 times for the susceptible strain and 32 times for the resistant strain. A two-sample t-test were used to examine the means (±SE) of two strains are significantly different from one another (p=0.05).

Life table data analysis

The raw life history data for survival, longevity and female daily fecundity of N. cucumeris individuals were analyzed using the TWOSEX-MSChart (Chi 2015) program, based on the agestage, two-sex life table theory and methods described by Chi and Liu (1985) and Chi (1988). The TWOSEX-MSChart program is available at  http://140.120.197.173/ecology/. The survival rate (sXj) (x = age, J = stage), which is the probability that a newly laid egg will survive to age x and stage j, and fecundity fXj, which is the number of hatched eggs produced by a female adult at age x were calculated. According to Chi and Liu (1985), the specific survival rate (lx) is then calculated as:

e01_184.gif

where m is the number of stages. To take individuals of different stages at age x into account, the age-specific fecundity (mx) is calculated as:

e02_184.gif

The total number of offspring that an individual can produce during its lifetime, i.e., the net reproductive rate (R 0), is calculated as:

e03_184.gif

The intrinsic rate of increase (r) using the Lotka-Euler equation with age indexed from zero (Goodman 1982) is calculated as:

e04_184.gif

The mean generation time (T) represents the period that a population requires to increase to R0fold of its size as time approaches infinity and the population growth rate settles down to the intrinsic rate and finite rate. Mean generation time is calculated as:

e05_184.gif

The standard errors of developmental time, longevity, fecundity, and population parameters were calculated by using the bootstrap method with 200,000 bootstrap replicates (Efron and Tibshirani 1993, Huang and Chi 2012). Differences between treatments were compared using the paired bootstrap test (Efron and Tibshirani 1993, Smucker et al. 2007, Polat Akköprü et al. 2015).

Results

The developmental times of the egg, larval and protonymph stage of the resistant strain of N. cucumeris were significantly shorter than that of the susceptible strain (Table 1). However, there were no significant differences in the developmental times of deutonymph stage and adult stage between two strains (Table 1). The total developmental time for the preadult stages was 5.79 d in resistant strain, which was significantly shorter than 6.72 d in susceptible strain.

TABLE 1.

Developmental time, APOP, TPOP, longevity, survival, and fecundity (mean± SE) of resistant (R) and susceptible strains (S) of Neoseiulus cucumeris with prey Tetranychus truncatus.

t01_184.gif

There was no significant difference in adult pre-oviposition period (APOP) between resistant and susceptible strains. However, there was significant difference in the total pre-oviposition period between two strains. There were also significant differences in mean longevity and male total longevity between resistant and susceptible strains. However, the female total longevities and preadult survival were not significantly different between resistant and susceptible strains (Table 1). The fecundity of the resistant strain was significantly higher than that of the susceptible strain (Table 1).

The detailed age-stage-specific survival rates (sxj of the resistant and susceptible strains of N. cucumeris are plotted in Figs. 1 and 2. The parameter sXJ represents the probability that an egg of N. cucumeris will survive to age x and stage j. Overlapping among stages were observed. The probability that an individual surviving to the egg and larva stage of resistant strains were lower than susceptible strains, which is also consistent with the lower total longevities (51.78 d for female and 48.28 d for male) in resistant strains shown in Table 1.

FIGURE. 1

Age-stage specific survival rate (sxj) of susceptible strains of N. cucumeris.

f01_184.jpg

FIGURE. 2

Age-stage specific survival rate (sxjj) of resistant strains of N. cucumeris.

f02_184.jpg

FIGURE. 3

Age-specific survival rate (l x) of resistant and susceptible strains of N. cucumeris.

f03_184.jpg

FIGURE. 4

Age-specific fecundity (mx) of resistant and susceptible strains of N. cucumeris.

f04_184.jpg

When the survival rates sXJ of different stages are pooled, the age-specific survival rate (lx) produced a simplified overview of the survival history of the entire population (Fig. 3). The survival rates of the female of resistant and susceptible strains of N. cucumeris were similar.

In resistant strains, the first reproduction occurred at age 7 d and reached its peak between 8∼28 d; however, in susceptible strains reproduction began on age 8 d and reached peak fecundity at age 9∼27 d. The detailed age-stage-specific fecundity (mx) of the resistant and susceptible strains of N. cucumeris is plotted in Fig. 4; they were similar.

TABLE 2.

Life history parameters of resistant (R) and susceptible (S) strains of Neoseiulus cucumeris with prey Tetranychus truncates.

t02_184.gif

The life history parameters of the resistant and susceptible strains of N. cucumeris are shown in Table 2. The net reproductive rate (R0=30.3833 offspring), the intrinsic rate of increase (r=0.2231 d-1) and the finite rate of increase (λ=1.2499 d-1) of the resistant strain were only slightly higher than those of the susceptible strain (R0=29.5333 offspring, r=.2130 -1, λ=1.2373 d-1); the differences were not significant. However, the mean generation time (T=15.1768 d) of the resistant strain was significantly shorter than that of the susceptible strain (T=16.0314 d).

Discussion

Fitness is a biological response to the external environment conditions. Pest insects evolve resistance in order to survive pesticides. As opposed to the rest of the population, the mites that have developed resistance pass along the genes that improve the survival of their offspring. In most cases, increasing the survival rate will decrease the fitness of the resistance stain. They will be less competitive; they will show longer developmental duration, higher mortality rate, lower fertility and lower overwinter survival (Li 2000; Meng 1998). In general, arthropods that have developed resistance to insecticides will have reduced fitness (Denholm 1992; Carrire 2003). Moreover, when reared at the same temperature, the abamectin resistance strain of T. cinnabarinus had longer developmental duration and lower fertility than the susceptible stain (He et al. 2008). However, fitness cost can't always be observed among all the resistant strains (Wu 1994). When compared to the susceptible strain, the intrinsic rate of increase (rm), and net reproduction rate (R0) of the propargite-resistant strain of T. cinnabarinus, were 0.24 and 25.34 for susceptible strains, and 0.26 and 28.99 for resistant strains, respectively (Luo et al. 2015). Furthermore, the relative fitness of resistance strains was 1.14, which showed an advantage over the susceptible strain (Luo et al. 2015).

This study demonstrated the advantages of using the age-stage, two-sex life table theory in describing demography (Chi 1988, Yu et al. 2005). Our results indicate that, when reared at the same temperature, the abamectin resistant strain of N. cucumeris had significantly shorter developmental duration and higher fertility than the susceptible strain, contrary to the pattern in abamectin resistant strain of T. cinnabarinus (He et al. 2008). However, the longevity of the resistant strain was significantly shorter than that of the susceptible strain. The mean generation time (T) of the resistant strain of N. cucumeris was significantly shorter than that of the susceptible strain. However, other parameters (the net reproductive rate, the intrinsic rate of increase and the finite rate of increase) were not significantly different between the two strains.

Since the traditional female age-specific cannot describe the stage differentiation and ignores the male population, the practical applications of traditional female age-specific life tables in population ecology and pest management are limited. The problems associated with the traditional female age-specific life table are discussed in detail in Huang and Chi (2011).

N. cucumeris is one of the main products of natural enemies among international biocontrol companies and is mainly used to control the thrips, mites and other pests (Gillespie, 1988; Zhang et al. 2006). Now, N. cucumeris has been widely used in China to control spider mites and other pests on bamboo, citrus, tea, apple, cotton, strawberry, loquat, and peach crops with remarkable results (Zhang et al. 2006; Zhang, 2006).

We have compared the predation rates between resistant strains and susceptible strains and also measured potency detoxification enzyme activity to reveal the biochemical mechanism of N. cucumeris resistance to abamectin. The results will be presented in another article. The resistant strain, which was mass-reared in the laboratory and applied in the field, can reduce the conflict between biological control and chemical control. Predatory mites will be employed for rational and efficient use to improve the biological control performance, and the coordination of chemical control with biological control in integrated pest management programs.

Acknowledgements

We are grateful to Dr. Zhi-Qiang Zhang (Landcare Research, Auckland, New Zealand) who kindly edited the English and two anonymous reviewers for comments. Sincere thanks are also due to Dr. Hsin Chi (Department of Entomology, National Chung-Hsing University, Taichung, Taiwan, Republic of China) for supplying the software to analyze the twosex life table, and giving valuable guidance and suggestions for this research. We also thank Meng-Zhu Shi for assistance. This study was partly supported by the National Natural Science Foundation of China (31301722), Fujian Council Fund for Scientific Research in the Public Interest (2015R1024-3), Fujian Council Fund for Scientific Research in the Public Interest (2014R1024-3) and Fujian Academy of Agricultural Sciences PI innovation team project (2016PI-19).

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© Systematic & Applied Acarology Society
Xia Chen, Yan-Xuan Zhang, Yu-Ping Zhang, Hui Wei, Jian-Zhen Lin, Li Sun, and Feng Chen "Relative fitness of avermectin-resistant strain of Neoseiulus cucumeris (Oudemans) (Acari: Phytoseiidae)," Systematic and Applied Acarology 22(2), 184-192, (11 January 2017). https://doi.org/10.11158/saa.22.2.3
Received: 30 October 2016; Accepted: 1 December 2016; Published: 11 January 2017
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