Differential effects of two plant viruses on performance and biocontrol efficiency of Encarsia formosa fed on Bemisia tabaci

Biological Control 142 (2020) 104166

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Differential effects of two plant viruses on performance and biocontrol efficiency of Encarsia formosa fed on Bemisia tabaci Jie Li, Tianbo Ding, Dong Chu

T

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Key Laboratory of Integrated Crop Pest Management of Shandong Province, College of Plant Health and Medicine, Qingdao Agricultural University, Qingdao 266109, China

G R A P H I C A L A B S T R A C T

A R T I C LE I N FO

A B S T R A C T

Keywords: Encarsia formasa Bemisia tabaci Tomato yellow leaf curl virus Tomato chlorosis virus Life table Performance Biocontrol

The consequences of infection by plant virus on the efficacy of parasitoid wasps are poorly understood. In the current study, an age-stage, two-sex life table and the CONSUME-MSChart computer program were used to test the performance of Encarsia formosa (Hymenoptera: Aphelinidae) on the whitefly, Bemisia tabaci Mediterranean (MED) species, occurring on healthy tomato plants compared to tomato plants infected with Tomato chlorosis virus (ToCV) and Tomato yellow leaf curl virus (TYLCV). The results showed that the intrinsic rate of increase (r) of E. formosa was 0.2051 d−1 on tomato plants infected with only TYLCV. This was similar to the rate on healthy tomato plants, but was significantly higher than the rate on tomato plants infected only with ToCV (0.1965 d−1) and on tomato plants co-infected with both TYLCV and ToCV (0.1772 d−1). Similar differences, consistent with the r values, were found in the net reproduction rate (R0) and finite rate of increase (λ) of E. formosa reared on B. tabaci MED infesting the three different tomato plant/virus combinations. Population growth projection predicted that E. formosa populations would increase faster on B. tabaci MED whiteflies fed on TYLCV-infected tomato plants than that on plants infected with ToCV. Projections of the total mortality rates also predicted that E. formosa were more lethal to B. tabaci MED on TYLCV-infected tomato plants than on ToCV-infected tomato plants. The lowest population growth and mortality potential of E. formosa occurred in B. tabaci MED fed on TYLCV and ToCV co-infected tomato plants. Our findings demonstrate that E. formosa are more effective in controlling B. tabaci on TYLCV-infected tomato plants, than on ToCV-infected and TYLCV and ToCV co-infected tomato plants. The latter two combinations have an apparant negative impact on the survival and parasitization of E. formosa.

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Corresponding author. E-mail address: [email protected] (D. Chu).

https://doi.org/10.1016/j.biocontrol.2019.104166 Received 8 June 2019; Received in revised form 3 December 2019; Accepted 16 December 2019 Available online 19 December 2019 1049-9644/ © 2019 Published by Elsevier Inc.

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1. Introduction

the difference in the performance and control efficiency of E. formosa reared on B. tabaci MED individuals fed on tomato plants infected with different viruses, we conducted demographic comparisons of E. formosa reared on B. tabaci MED fed on tomato plants infected with the viruses ToCV, TYLCV, and co-infected, using the two-sex life table and the CONSUME-MSChart computer program. The results should increase our understanding of the fitness and ability of E. formosa to control B. tabaci MED on TYLCV or ToCV infected tomato plants.

The whitefly, Bemisia tabaci (Gennadius) (Hemiptera: Aleyrodidae), is a major, agricultural and economically important pest worldwide (De Barro et al., 2011). This pest causes severe damage to a large assortment of crops, herbs, and ornamentals directly by sucking phloem, and indirectly by causing sooty mould via honeydew secretion, and most importantly, by the transmission of a multitude of plant viruses belonging to several virus family including Begomovirus, Crinivirus, Torradovirus, and Ipomovirus (Jones, 2003; Polston et al., 2014; Gilbertson et al., 2015). B. tabaci is a species complex comprised of at least 44 morphologically indistinguishable cryptic species of whiteflies (Kanakala and Ghanim, 2019) that have been recorded from over 1000 plant species (Abd-Rabou and Simmons, 2010). Over the past two decades, combinations of B. tabaci and Begomovirus species, have been considered one of the most economically important vector-virus complexes, threatening the output of many major vegetable and ornamental enterprises. Among these, B. tabaci Mediterranean (MED) has become the dominant B. tabaci species in China, due to its greater virus transmission efficiency and higher insecticide resistance (Luo et al., 2010; Liu et al., 2013; Xie et al., 2014). Although chemical pesticide applications remain the primary means of whitefly management, the overuse of these pesticides has resulted in strong chemical resistance and outbreaks of this pest (Cuthbertson et al., 2012; Basit et al., 2013). An environmentally friendly method of controlling whiteflies is to use a classical biological control approach involving parasitoids, which plays an important role in sustainable pest control (Gerling et al., 2001). Recent studies have listed over 80 described species of parasitoids of whiteflies. Of these, Encarsia formosa (Gahan) (Hymenoptera: Aphelinidae) is one of the most important and well-known parasitoid species. E. formosa has been widely used for commercial control of whiteflies on many vegetables crops as well as on ornamental plants in greenhouses (Van Lenteren et al., 1996; Van Lenteren, 2000; Gerling et al., 2001; Bacci et al., 2007; Li et al., 2011; Lahey and Stansly, 2015; Liu et al., 2016). B. tabaci MED, which has been listed as the major invasive pest during the past decade in China, can readily transmit Tomato yellow leaf curl virus (TYLCV), threatening the production of vegetables and ornamentals. During recent years, another newly established Crinivirus, Tomato chlorosis virus (ToCV), has also begun to spread (Pan et al., 2012; Li et al., 2018). In so doing, the co-occurrence of ToCV and TYLCV on tomatoes has become widespread in many provinces of China following the outbreak and spread of B. tabaci MED (Dai et al., 2017; Liu et al., 2018). Parasitoid wasps have historically been considered as an important factor in biological control of B. tabaci. During host feeding and oviposition, individual parasitoid wasps may encounter a multitude of adverse factors such as competing insect species and insect-borne pathogens that would complicate the successful completion of these processes (Christiansen-Weniger et al., 1998; Pope et al., 2002; Liu et al., 2014a,b, 2017). Recent studies have suggested that vectorborne pathogens can exert their impact on a parasitoid through the vector. For example, TYLCV may affect the adult longevity and developmental time of E. formosa reared on B. tabaci MED (Liu et al., 2014a,b). In addition, the TYLCV-infected tomato plants may also increase the attraction to E. formosa (Liu et al., 2017). As host-mediated effects of plant viruses on parasitism vary across different host species, it is important to compare the development of parasitic wasps that utilize a host species feeding on plants that are infected with different viruses in order to gain insight into possible effects the plant viruses may have on the wasps (Mauck, 2016). Little information is currently available on the consequences to major biological parameters in the parasitoid, E. formosa, after parasitizing B. tabaci MED that have developed on host tomato plants infected with different virus species. Life tables are often used to comprehensively describe and analyze the overall effect of one or more biotic factors on the development, survival, and reproductive success of a target population. To investigate

2. Material and methods 2.1. Insects and parasitoid cultures The Bemisia tabaci MED population was originally collected from infected tomato fields in Jinan, China in 2012, and subsequently cultured on cotton plants, Gossypium hirsutum M. cv. Lu-Mian 28, a common host plant of the MED population. The experimental MED population was maintained on tomato plants in a growth chamber set at 27 ± 2 °C, 60 ± 10% RH and a photoperiod of 16:8 (L:D) hr, and reared for five generations prior to being used. Their purities were confirmed by the Vsp I-based mtCOI PCR-RFLP method every 30 days (Chu et al., 2012). The Encarsia formosa culture was a gift from the Institute of Plant Protection, Shandong Academy of Agriculture, China in July 2017. The parasitoid was maintained on B. tabaci MED nymphs, reared on cotton plants, Gossypium hirsutum M. cv. Lu-Mian 28. The parasitic wasps had been maintained on B. tabaci MED feeding on tomato plants for more than three generations (from March to June 2018) in a growth chamber set at 26 ± 2 °C, 60 ± 10% RH and a photoperiod of 16:8 (L:D) hr. 2.2. Plants, TYLCV and ToCV Tomatoes (Solanum lycopersicum Mill. Cv. Zhongza 9) were used as the host plant for B. tabaci MED. The tomato plants were grown in a growth chamber and covered with 200-mesh insect-proof screen to exclude whiteflies, parasitoids and other pests. TYLCV-infected and ToCV-infected tomato plants were obtained by B. tabaci MED inoculation. Twenty viruliferous male whiteflies (all emerged within a 48 h period and allowed to feed for 48 h on TYLCV- or ToCV-infected tomato plants) were transferred to healthy tomato plants using a clip-on cage at the 3 true-leaf stage for a 10-day inoculation access period. Using a similar method, TYLCV + ToCV co-infected tomato plants were obtained by inoculating healthy tomato plants with 20 ToCV-viruliferous and 20 TYLCV-viruliferous male whiteflies. After inoculation, plants were maintained in a greenhouse at 27 ± 2 ℃ under a photoperiod of 16:8 (L:D) hr, and grown for an additional 28 days. TYLCV and ToCV infected tomato plants were confirmed using TYLCV primers TYLCV-F/TYLCV-R (Pico et al., 1998) and ToCV primers ToC-5/ToC-6 (Dovas et al., 2002) independently. B. tabaci MED populations were maintained on non-infected, TYLCV-infected, ToCV-infected, and TYLCV + ToCV co-infected tomato plants, respectively, when host plants reached the 7–9 true-leaf stage. 2.3. Life table and Encarsia formosa’s parasitism on Bemisia tabaci MED occurring on virus-infected tomato plants Tomato plants of approximately 50 cm height with 7–9 true-leaf were selected for the experiments. 30–40 whitefly adults were placed into a rearing container (Li et al., 2018) with a single true leaf (the 3rd–7th true-leaf from the bottom) and allowed to oviposit, the true leaf was detached from the tomato seedling, and the stem of the true leaf immersed in 1-naphthylacetic acid (50 ppm) for 10 min, rinsed with water and then maintained in a separate container with nutrient solution (Lv et al., 2010). Five days later, all adults were removed from the container, a second group of 30–40 whitefly adults were placed into a new rearing container with a single true leaf and allowed to oviposit for 2

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a further five days, then removed as before and the tomato plants were maintained for another 10 days. When the first group reached the third nymphal instar and the second group of whitefly eggs began to hatch, 10 E. formosa females were introduced into each rearing container and allowed to oviposit for 24 h. The seedlings in the rearing containers were checked daily for newly emerged E. formosa adults beginning at the 14th day (corresponding to the day prior to eclosion). The dates for the pre-adult duration and pre-adult survival were recorded for all individuals. Newly emerged female adults (< 12 h) were transferred to a new rearing container with one tomato leaf and allowed to oviposit. The adult E. formosa individuals was checked daily for survival. To record parasitism (egg production), each E. formosa female was transferred into a new rearing container with about 100 third instar whitefly nymphs to allow host feeding and ovipositing every five days. New rearing container with about 100 third instar whitefly nymphs were supplied every 5 days until the female E. formosa died, the longevity of each E. formosa adult was recorded. Host feeding was examined under a stereoscopic microscope while transferring the E. formosa individuals; parasitism was examined under a stereoscopic microscope 10–15 days after the removal of E. formosa. The daily parasitism was calculated as the mean of parasitism laid within each 5-day period. All experiments were conducted and maintained at 26 ± 2℃ and 60% ± 10% RH with a photoperiod of 16:8 (L:D) hr.

To evaluate the biological control efficiency of a parasitoid, it is often necessary to take both host-feeding rate and parasitism rate into account. Thus, we define the kill rate as the number of whiteflies killed by each E. formosa through both host-feeding and parasitism (Chi and Yang, 2003; Yu et al., 2005). The age-specific whitefly-kill rate (u x ) was calculated as: β

ux =

∑ j = 1 sxj pxj β

∑ j = 1 sxj

(6)

Accounting for the age-specific survival rate, the age-specific net whitefly-kill rate (wx ) was calculated as: (7)

wx = l x u x

The cumulative kill rate (Zx ) is the total number of whiteflies killed by an E. formosa from birth to age x, while the net kill rate (Z0 ) is the total number of whiteflies killed by an individual E. formosa during its lifespan. These values were calculated as: ∞

x

Zx =

∑ li ui

and Z0 =

i=0

∞

β

∑ lx ux = ∑ ∑ sxj pxj x=0

= R 0 + C0

x=0 j=1

(8)

The age-specific host-feeding rate (k x ) was calculated as: β

∑ j = 1 sxj cxj

2.4. Life table data analysis

kx =

The raw data on the development, longevity, survival rate, and daily parasitism (fecundity) of individual E. formosa females were analyzed according to the age-stage, two-sex life table (Chi and Liu, 1985; Chi, 1988) procedure using the computer program TWOSEX-MSChart (Chi, 2018b). Data on daily host-feeding rates and whitefly-mortality rates were analyzed using the computer program CONSUME-MSChart (Chi, 2018a). Following Chi and Liu, the age-stage-specific survival rate (sxj) (x = age; j = stage), age-specific survival rate (lx), age-specific fecundity (mx), age-stage-specific fecundity (fxj), intrinsic rate of increase (r), reproductive rate (R0), mean generation time (T), and finite rate of increase (λ) were calculated. In the age-stage, two-sex life table, the age-specific fecundity (mx) is calculated as:

where cxj is the age-stage-specific host-feeding rate of individual female E. formosa at age x and stage j (Chi and Yang, 2003; Yu et al., 2005). Accounting for the age-specific survival rate, the age-specific net hostfeeding rate (qx ) was calculated as:

∞

∞

β

x=0

x=0 j=1

(2)

p (t ) =

The mean generation time (T) and the finite rate (λ) were calculated as follows:

ln(R 0) r

(4)

λ=

er

(5)

∞

∑ ⎛⎜ ∑ pxj nxj (t )⎞⎟ j=1

(3)

T=

(11)

⎝ x=0

⎠

(12)

where pxj is the whitefly kill rate of E. formosa at age x and stage j. The population projections of E. formosa were started with ten eggs. Because E. formosa are endoparasites, in order to facilitate observation, it was necessary to combine the egg, larval, and pupae stages into a single stage (preadult stage) when observations were conducted (Xu et al., 2018; Li et al., 2018). The standard errors of all life history and population parameters were calculated using the bootstrap method with 100,000 resampling. The differences in development time, adult longevity, oviposition days, fecundity, population parameters, host-feeding rates, and killing rates among treatments were analyzed using a paired bootstrap test at the 5% significance level (Efron and Tibshirani, 1993; Huang and Chi, 2012; Polat-Akköprü et al., 2015).

∞ x=0

∑ lx kx x=0

β

The intrinsic rate of increase (r) was evaluated using the iterative bisection method and the Euler-Lotka equation with the age indexed from 0 (Goodman, 1982).

∑ e−r (x+1) lx mx = 1

and C0 =

To compare host-feeding potentials, we incorporated both the hostfeeding rate and finite rate into the finite host-feeding rate (Chi et al., 2011; Yu et al., 2013). The finite host-feeding rate (ω ), net host-feeding rate (C0) (number of individuals), stable host-feeding rate (φ ), net kill rate (Z0) (number of whiteflies), stable kill rate (θ ), finite kill rate (v), and transformation rate (Qp) were calculated according to Xu et al. (2018). The growth and potential kill rate of E. formosa were projected using the TIMING-MSChart program (Chi, 1990, 2018c). The kill potential at time t was calculated as:

(1)

∑ li mi andR0 = ∑ lx mx = ∑ ∑ sxj fxj i=0

∑ li k i i=0

β

x

∞

x

Cx =

where β is the number of life stages. The cumulative reproductive rate (Rx) is the number of offspring produced by an individual E. formosa from birth to age x, while the net reproductive rate (R 0 ) is the total offspring produced by an individual female E. formosa during her lifetime. These were calculated according to Chi and Su (2006).

Rx =

(10)

The cumulative host-feeding rate (Cx ) is the number of whiteflies killed by an average E. formosa from birth to age x, while the net hostfeeding rate (C0 ) is the total number of whiteflies killed by an average E. formosa during its lifespan. These values were calculated as:

β

∑ j = 1 sxj

(9)

qx = l x k x

∑ j = 1 sxj fxj

mx =

β

∑ j = 1 sxj

The life expectancy (exj ) was calculated according to Chi and Su (2006), and the reproductive value (vxj ) was calculated according to Tuan et al. (2014). 3

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whiteflies from the co-infected plants (0.1772 d−1), followed by the ToCV plants (0.1965 d−1), the TYLCV plants (0.2051 d−1) and the healthy plants (0.2110 d−1). The differences in the net reproductive rates (R 0 ), and the finite rate of increase (λ) for individuals reared on whiteflies feeding on the three virus-infected tomato plants were consistent with the r values. The mean generation time (T) ranged from the shortest (20.33 d) on whiteflies fed on ToCV plants to the longest (21.32) on co-infected plants (Table 2).

3. Results 3.1. Performance of Encarsia formosa reared on Bemisia tabaci MED on virus-infected tomato plants There was a significant difference in fecundity of E. formosa females reared on B. tabaci MED occurring on tomato plants infected with different viruses. The mean fecundity of E. formosa fed on B. tabaci MED was the highest (92.02 offspring per female) on TYLCV-infected tomato plants (hereafter referred to as “TYLCV plants”), the second highest (81.26 offspring per female) on healthy tomato plants (hereafter referred to as “healthy plants”), followed by ToCV-infected tomato plants (hereafter referred to as “ToCV plants”) (64.49 offspring per female), and the lowest (51.20 offspring per female) on TYLCV + ToCV co-infected tomato plants (hereafter referred to as “co-infected plants”). Both the average adult longevity and overall lifespan of E. formosa females reared on B. tabaci MED from co-infected plants were significantly shorter than those reared on whiteflies from TYLCV, ToCV and healthy plants. Both the average adult female longevity, and overall lifespan of E. formosa females reared on B. tabaci MED from tomato plants infected with only ToCV were significantly shorter than when reared on whiteflies from healthy tomato plants. No significant differences were found in the average adult longevity, and overall lifespan of E. formosa females reared on B. tabaci MED from ToCV and TYLCV plants. No significant differences were found in the average development time of the pre-adults and in the number of oviposition days among the ToCV, TYLCV, and the co-infected plants (Table 1). The survivorship and stage differentiation of individual E. formosa reared on B. tabaci MED from different virus-infected tomato plants can be observed in the age-stage survival rate (sxj ). The sxj curves were similar in all three E. formosa groups. The probability that a newly laid egg would survive to the adult stage was the lowest (0.845) on whiteflies reared on ToCV plants (Fig. 1). The peak fxj (the mean number of fertilized eggs (j) produced by E. formosa female adults at age x) values were 11.47, 11.48, 8.63, and 6.65 eggs per day on whiteflies from healthy, TYLCV, ToCV, and co-infected tomato plants, respectively. The lowest age-specific survival rate (l x ), age-specific fecundity (m x ), and age-specific maternity (l x m x ) occurred in E. formosa reared on B. tabaci MED from co-infected plants (Fig. 2). The age-stage life expectancy (exj ) of E. formosa at age zero (e01) was 31.38, 30.76, 29.48, and 29.16 after being reared on whiteflies from healthy, TYLCV, ToCV, and co-infected plants, respectively (Fig. 3). The peak vxj values (the expected contribution of an individual of age x and stage j to the future population) for individuals reared on B. tabaci MED feeding on healthy, TYLCV, ToCV, and co-infected plants occurred at 14 d (v14,2 = 48.75 d−1), 14 d (v14,2 = 49.86 d−1), 14 d (v14,2 = 37.28 d−1), and 13 d (v13,2 = 29.74 d−1), respectively. The peak reproductive values of E. formosa fed on whiteflies from co-infected plants occurred earlier and was lower than those on the other treatments (Fig. 4). There was a significant difference (P < 0.05) in the intrinsic rate of increase (r) in E. formosa females fed on whiteflies from the different treatments – the lowest r value occurred in individuals reared on

3.2. Difference in host-feeding rates of Encarsia formosa reared on Bemisia tabaci MED on virus-infected tomato plants Because the pre-adult stage of E. formosa does not host-feed, several gaps appeared in this stage in the host-feeding rates prior to adult emergence (Fig. 5). The highest daily age-specific host-feeding rates (k x ) of E. formosa were 2.29, and 2.24 whiteflies per individual on healthy, and TYLCV plants, respectively, compared to the lower values on ToCV (1.34 whiteflies per individual), and co-infected plants (1.00 whitefly per individual). The curves of the daily age-specific net hostfeeding rates (qx ) on different virus-infected tomato plants were similar to the k x values. The peak qx values were 2.00, 1.92, 1.13, and 0.86 whiteflies on healthy, TYLCV, ToCV, and co-infected plants, respectively (Fig. 5). Considering the survival rates, host-feeding rates and longevity, the net host-feeding rate (C0 ) of E. formosa was the lowest (11.20 whiteflies per individual) on co-infected plants, 13.75 whiteflies per individual on ToCV plants, 23.41 on TYLCV plants and 25.90 on healthy plants. There were significant differences between the C0 values in the TYLCV, ToCV, and co-infected tomatoes (Table 3). A stable host-feeding rate (φ) was found for E. formosa reared on whiteflies feeding on healthy and TYLCV plants (0.0738 and 0.0636, respectively). These were significantly greater than those on ToCV (0.0490) and co-infected plants (0.0466). Similarly, the finite host-feeding rates (ω ) for E. formosa reared on whiteflies from healthy and TYLCV plants (0.0906 and 0.0785, respectively) were significantly greater than those on ToCV and co-infected plants (0.0597 and 0.0556, respectively) (Table 3). 3.3. Differences in mortality rates from Encarsia formosa in Bemisia tabaci MED reared on tomato plants infected with different virus treatments The two highest peak daily age-specific kill rates (u x ) of E. formosa were 9.71, and 10.96 whiteflies per individual on healthy, and TYLCV plants, respectively, while lower rates were observed on ToCV plants (7.83 whiteflies per individual), and co-infected plants (5.51 whiteflies per individual). The curves of the daily age-specific net kill rates (wx ) of E. formosa on different virus-infected tomato plants were similar to the u x values – the peak wx E. formosa values were 8.48, 9.39, 6.62, and 4.71 whiteflies on healthy, ToCV, TYLCV, co-infected plants, respectively (Fig. 6). Considering the survival rates, host-kill rates and longevity, the net kill rates (Z0 ) of E. formosa were (in order from the lowest) 54.96 whiteflies per individual on co-infected plants, 68.22 on ToCV plants,

Table 1 The development times of different life stages and sexes, longevity, and female reproductive parameters of Encarsia formosa reared on Bemisia tabaci MED feeding on different virus-infected tomato plants (mean ± standard error). Parameter

N

Healthy tomato plants

N

TYLCV-infected tomato plants

N

ToCV-infected tomato plants

N

TYLCV + ToCV co-infected tomato plants

Pre-adult (d) Female adult longevity (d) Female overall lifespan (d) Oviposition days (d) Fecundity (eggs per female)

62 62 62 62 62

17.23 17.55 34.77 16.35 81.26

60 60 60 60 60

16.83 17.30 34.13 16.22 92.02

60 60 60 60 60

16.30 16.67 32.97 16.07 64.49

64 64 64 64 64

16.45 15.67 32.13 15.31 51.20

± ± ± ± ±

0.35a 0.19a 0.43a 0.20a 1.02a

± ± ± ± ±

0.31b 0.40ab 0.46ab 0.32ab 1.44b

± ± ± ± ±

0.27b 0.37b 0.46b 0.33ab 1.28c

± ± ± ± ±

0.24ab 0.43c 0.47c 0.43b 3.75d

Means in the same row followed by different letters represent a significant difference between Encarsia formosa parameters reared on Bemisia tabaci MED occurring on different virus-infected tomato plants (paired bootstrap test; P < 0.05). 4

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Fig. 1. Age-stage-specific survival rate (Sxj) of Encarsia formosa reared on Bemisia tabaci MED feeding on tomato plants infected with different viruses.

infected plants (0.2709 and 0.2451, respectively). Similarly, the finite kill rates (v ) of B. tabaci MED by E. formosa on healthy and TYLCV plants (0.3774 and 0.3736, respectively) were significantly greater than those on ToCV and co-infected plants (0.3298 and 0.2926, respectively) (Table 3).

96.86 on healthy plants and 102.36 on TYLCV plants. There were significant differences in the Z0 of E. formosa between each of the virus treated tomato plants (Table 3). The stable kill rates (θ) of B. tabaci MED by E. formosa on healthy and TYLCV plants (0.3074 and 0.3025, respectively) were significantly greater than those on ToCV and co-

Fig. 2. Age-specific survival rate (lx), female age-specific fecundity (fxj), age-specific fecundity of the total population (mx), and age-specific maternity (lxmx) of Encarsia formosa reared on Bemisia tabaci MED feeding on tomato plants infected with different viruses. 5

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Fig. 3. Age-stage specific life expectancy (exj) of Encarsia formosa reared on Bemisia tabaci MED feeding on tomato plants infected with different viruses.

3.4. Projection of population growth and kill potential of Encarsia formosa reared on Bemisia tabaci MED from virus-infected tomato plants

The transformation rates (Qp) of E. formosa reared on B. tabaci MED from healthy and TYLCV-infected tomato plants (1.3650 and 1.2978, respectively) were significantly greater than those on ToCV and co-infected plants (1.2517 and 1.2580, respectively) (Table 3).

The population growth and stage structure of E. formosa reared on

Fig. 4. Reproductive value (vxj) of Encarsia formosa reared on Bemisia tabaci MED feeding on tomato plants infected with different viruses. 6

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Table 2 Life table parameters of Encarsia formosa reared on Bemisia tabaci MED feeding on different virus-infected tomato plants (mean ± standard error). Parameter −1

Intrinsic rate of increase (r) (d ) Net reproduction rate (R0) (offspring) Generation time (T) (days) Finite rate of increase (λ) (d−1)

Healthy tomato plants

TYLCV-infected tomato plants

ToCV-infected tomato plants

TYLCV + ToCV co-infected tomato plants

0.2110 ± 0.0038ab 70.96 ± 3.34a 20.78 ± 0.31ab 1.2277 ± 0.0048ab

0.2051 ± 0.0039a 78.87 ± 4.03a 20.70 ± 0.28ab 1.2349 ± 0.0047a

0.1965 ± 0.0039b 54.50 ± 2.96b 20.33 ± 0.24a 1.2173 ± 0.0047b

0.1772 ± 0.0053c 43.69 ± 3.82c 21.32 ± 0.29b 1.1939 ± 0.0063c

Means in the same row followed by different letters represent a significant difference between Encarsia formosa parameters reared on Bemisia tabaci MED occurring on different virus-infected tomato plants (paired bootstrap test; P < 0.05).

Fig. 5. Age-specific host-feeding rate (kx), age-specific net host-feeding rate (qx) and cumulative host-feeding rate (Cx) of Encarsia formosa reared on Bemisia tabaci MED feeding on tomato plants infected with different viruses.

Table 3 Host-feeding rates and killing rates of Encarsia formosa on Bemisia tabaci MED feeding on different virus-infected tomato plants (mean ± standard error). Parameter

Healthy tomato plants

TYLCV-infected tomato plants

ToCV-infected tomato plants

TYLCV + ToCV co-infected tomato plants

Net host-feeding rate (C0) (number of whiteflies) Stable host-feeding rate (φ ) Finite host-feeding rate (ω ) Net killing rate (Z0) (number of whiteflies) Stable killing rate (θ ) Finite killing rate (v) Transformation rate (Qp)

25.90 ± 1.27a

23.41 ± 1.22a

13.75 ± 0.76b

11.20 ± 0.88c

0.0738 ± 0.0025a 0.0906 ± 0.0034a 96.86 ± 4.54a 0.3074 ± 0.0092a 0.3774 ± 0.0127a 1.3650 ± 0.0065a

0.0636 0.0785 102.36 0.3025 0.3736 1.2978

0.0490 ± 0.0015c 0.0597 ± 0.0021c 68.22 ± 3.71b 0.2709 ± 0.0084b 0.3298 ± 0.0115b 1.2517 ± 0.0027c

0.0466 ± 0.0018c 0.0556 ± 0.0024c 54.96 ± 4.69c 0.2451 ± 0.0114b 0.2926 ± 0.0152c 1.2580 ± 0.0045c

± ± ± ± ± ±

0.002b 0.0027b 5.23a 0.0092a 0.0127a 0.0029b

Means in the same row followed by different letters represent a significant difference among Encarsia formosa on Bemisia tabaci MED occurring on different virusinfected tomato plants (paired bootstrap test; P < 0.05). 7

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Fig. 6. Age-specific whitefly-killing rate (ux), age-specific net kill rate (wx) and cumulative kill rate (Zx) of Encarsia formosa on Bemisia tabaci MED feeding on tomato plants infected with different viruses.

ToCV plants or co-infected plants compared to the control (healthy tomato plants), but were not affected when TYLCV plants were used (Table 1). These results suggest that when B. tabaci MED occurs on a TYLCV plant it is conducive to increased numbers of E. formosa, while B. tabaci MED found on a ToCV, or co-infected plant have a negative impact on the performance of E. formosa. A similar phenomenon has been recorded by Christiansen-Weniger et al. (1998) in Sitobion avenae (Fabricius) (Hemiptera: Aphididae) found on Barley yellow dwarf virus (BYDV). The virus had a delaying impact on the larval development of the endoparasitoid, Aphidius ervi Haliday (Hymenoptera: Braconidae) when its host, S. avenae, had acquired BYDV. However, no aspects of A. ervi’s development were affected when the aphids were carrying Pea enation mosaic virus (PEMV) or when the aphids were feeding on PEMVinfected beans (Hodge and Powell, 2008). Taken together, these finding suggest that plant virus infection of a host plant can have a positive, negative, or neutral impact on the performance of parasitoids depending on the plant, plant virus and insect species. At present, the agents responsible for the differential effects plant viruses on the performance of parasitoids remain unclear. Several factors have been proposed as possible causes to explain different performance of parasitoids on their vector hosts. These include vector clonal resistance, host (vector) quality or host plant nutritional quality (Li et al., 2002; Kalule and Wright, 2005; Ode, 2006; Calvo and Fereres, 2011). Clonal resistance is not applicable in our study. It is also unlikely that the lower fecundity detected in parasitoids was a consequence of clonal resistance. In our study, we used whitefly populations susceptible to E. formosa. However, the use of a clonal E. formosa population might limit the generalisation of the results obtained since parasitoids will have to face a higher genetic variability under a field situation. The other two factors, host plant nutritional quality and vector (whitefly)

B. tabaci MED from different virus-infected tomato plants are shown in Fig. 7. It was assumed that the population from an initial 10 eggs and would undergo 60 days. The population increased faster on B. tabaci MED from TYLCV and healthy plants, while the population reared on whiteflies fed on ToCV and co-infected plants would increase much slower. The kill potential of E. formosa reared on B. tabaci MED feeding on TYLCV plants was similar to that on healthy plants, both of which were higher than those on ToCV and co-infected plants (Fig. 7). 4. Discussion It has been well documented that the development duration of natural enemies can be affected by host species, age, and size (Luo and Liu, 2011; Yang and Wan, 2011; Hu et al., 2002). In addition, plant pathogen infection of the host plants can also influence the performance of natural enemies (de Oliveira et al., 2014; Kang et al., 2018). In this study, the performance of E. formosa fed on B. tabaci occurring on ToCV or/and TYLCV infected tomato plants was determined and compared using the age-stage, two-sex life table. This study revealed a decrease in fecundity of E. formosa fed on B. tabaci MED occurring on ToCV and coinfected plants compared to that on TYLCV or healthy plants (Table 1), showing that ToCV has a negative effect on the fitness of E. formosa. The intrinsic rate of increase (r) is a key parameter in evaluating the performance of E. formosa relative to their hosts, because it reflects the physiological qualities of the insect in relation to its capacity to increase (Xu et al., 2018). The results in this study showed that the r value of E. formosa fed on B. tabaci MED occurring on TYLCV plants was significantly higher than it was on ToCV, and co-infected plants. In addition, the female lifespan and number of oviposition days of E. formosa significantly decreased when reared on B. tabaci MED feeding on either 8

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Fig. 7. Projection of population growth and total kill rate of Encarsia formosa reared on Bemisia tabaci MED feeding on tomato plants infected with different viruses. An initial population of 10 eggs was used in each projection.

virus. Pope et al. (2002) also found that female parasitoid wasps often discriminate against hosts harboring unfavorable micropathogens. We hypothesize that E. formosa may actively discriminate against B. tabaci occurring on ToCV plants. Moreover, the whiteflys’ death due to hostfeeding by E. formosa is considered as an important mortality factor. Many factors can affect the host-feeding behavior of parasitoids, such as egg load (Collier, 1995), host stage, host density (Rosenheim and Rosen, 1992; Videllet et al., 1997), and environmental variables (Hansen and Jensen, 2002). In this study, ToCV or co-infected plants significantly decreased the net host-feeding rate (C0) of E. formosa reared on B. tabaci MED compared to healthy or TYLCV plants (Table 1). Thus, we found that ToCV plants also had a negative impact on the host-feeding of E. formosa fed on B. tabaci MED, but the TYLCV plants did not influence its host feeding, suggesting that the plant virus can also be regarded as a distinct factor affecting the host-feeding behavior of parasitoids. The effect of a plant virus on the host-feeding behavior of parasitoids may be due to the release of plant volatiles infected with plant virus. For example, Liu et al. (2017) found that TYLCV-infected tomato plants actively attracted the whitefly’s parasitoid, E. formosa, by elevating the release of volatiles such as β-myrcene, β-ocimene, and β-caryophyllene from the TYLCV plants. In order to comprehensively evaluate the control efficiency of E. formosa reared on B. tabaci MED occurring on ToCV and TYLCV infected tomato plants, daily host feeding and parasitism data for B. tabaci MED were consolidated as the net whitefly-kill rate (Z0). Because Z0 and the finite kill rate (v) of E. formosa fed on B. tabaci MED occurring on TYLCV plants were significantly higher than those on ToCV, or co-infected plants (Table 3), our results demonstrated that the cumulative control efficiency of E. formosa reared on B. tabaci MED from TYLCV plants was superior. We also used computer projection to demonstrate the change of stage structure and kill rate during population growth. The predicted population growth and potential kill rate showed that E. formosa populations bred on B. tabaci MED from TYLCV plants can

performance are closely related and both can be altered by virus infection. Several viruses can change host plant physiology by altering the concentration of free aminoacids and carbohydrates available in the phloem, modifying the host plant nutritional suitability to vectors, which may have an indirect effect on parasitoids’ biology and performance (Castle and Berger, 1993; Hodge and Powell, 2008). Similarly, TYLCV benefits the development of B. tabaci MED (Maluta et al., 2014; Su et al., 2015) while the ToCV has a negative impact on the development of its vector, B. tabaci MED (Li et al., 2018). These findings indicate that the physiology of the whitefly occurring on TYLCV plants may be better adapted than that on ToCV plants and is, in some manner, beneficial to the performance of E. formosa. The effect of TYLCV and ToCV infection on nutritional status of B. tabaci merits further study, which owing to technology limitation, we could not perform. Another possible explanation is the effects on host vectors brought by virus titres. As shown by Gilbertson et al. (2015), TYLCV is able to enter the hemolymph of B. tabaci, while ToCV cannot (the potential effects of this should be further explored). In nature, parasitic wasps and insect hosts have established a very complex adaptive mechanism. In our studies, we found that ToCV infected and ToCV + TYLCV co-infected tomato plants significantly shortened overall female lifespan and decreased the fecundity of E. formosa. ToCV infection may activate the insect host’s immune defense response, which is unfavorable for the reproduction capacity of E. formosa, but is of great benefit to the development and spread of virus population. In addition, we also found that the parasitism rate of E. formosa is more effective against B. tabaci MED occurring on TYLCV plants than on ToCV plants, suggesting that E. formosa may have a preference for B. tabaci occurring on TYLCV plants. Our results were consistent with Liu et al. (2014a,b) where a vector-borne pathogen was able to manipulate the host performance of a parasitoid and hence the host-parasitoid interactions – when the life history traits of E. formosa were influenced by either a cryptic species of B. tabaci or the plant 9

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increase faster and have an elevated kill potential over those reared on ToCV plants. Furthermore, since ToCV plants can reduce the adaptability and parasitism rate of E. formosa to B. tabaci, in order to enhance the control of E. formosa over B. tabaci and ToCV disease, it would be advisable to restrict virus incidence as far as possible. Consequently, our study lays the foundation for the prevention and control of whitefly and virus diseases using E. formosa.

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Declaration of Competing Interest The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper. Acknowledgments This research was supported by grants from the National Natural Science Foundation of China (31401809), and the Taishan Mountain Scholar Constructive Engineering Foundation of Shandong. The authors thank Prof. Hsin Chi (Niğde Ömer Halisdemir University, Turkey) for his assistance with the age-stage, two-sex life table. The authors thank Dr. Cecil Smith (University of Georgia, USA) for language editing of the manuscript. Appendix A. Supplementary data Supplementary data to this article can be found online at https:// doi.org/10.1016/j.biocontrol.2019.104166. References Abd-Rabou, S., Simmons, A.M., 2010. Survey of reproductive host plants of Bemisia tabaci (Hemiptera: Aleyrodidae) in Egypt, including new host records. Entomol. News 121, 456–465. Bacci, L., Crespo, A.L.B., Galvan, T.L., Pereira, E.J.G., Picanco, M.C., Silva, G.A., Chediak, M., 2007. Toxicity of insecticides to the sweet potato whitefly (Hemiptera: Aleyrodidae) and its natural enemies. Pest Manag. Sci. 63, 699–706. Basit, M., Saeed, S., Ahmad, M., Sayyed, A.H., 2013. Can resistance in Bemisia tabaci (Homoptera: Aleyrodidae) be overcome with mixtures of neonicotinoids and insect growth regulators? Crop Prot. 44, 135–141. Calvo, D., Fereres, A., 2011. The performance of an aphid parasitoid is negatively affected by the presence of a circulative plant virus. Biocontrol 56, 747–757. Castle, S.J., Berger, P.H., 1993. Rates of growth and increase of Myzus persicae on virusinfected potatoes according to type of virus-vector relationship. Entomol. Exp. Appl. 69, 51–60. Chi, H., 1988. Life-table analysis incorporating both sexes and variable development rates among individuals. Environ. Entomol. 17, 26–34. Chi, H., 1990. Timing of control based on the stage structure of pest populations: A simulation approach. J. Econ. Entomol. 83, 1143–1150. Chi, H., 2018a. CONSUME-MSChart: computer program for consumption rate analysis based on the age stage, two-sex life table [Online]. Available: http://140.120.197. 173/ecology/ [15 November 2018]. Chi, H., 2018b. TWOSEX-MSChart: computer program for age stage, two-sex life table analysis [Online]. Available: http://140.120.197.173/ecology/ [15 November 2018]. Chi, H., 2018c.TIMING-MSChart: A Computer Program for the Population Projection Based on Age-stage. Two-sex Life Table [Online]. Available: http://140.120.197. 173/Ecology/Download/TIMINGMSChart.rar [15 November 2018]. Chi, H., Huang, Y.B., Allahyari, H., Yu, J.Z., Mou, D.F., Yang, T.C., Farhadi, R., Gholizadeh, M., 2011. Finite predation rate: a novel parameter for the quantitative measurement of predation potential of predator at population level. Nat. Proc. 6651. Chi, H., Liu, H., 1985. Two new methods for the study of insect population ecology. Acad. Sin. Bull. Inst. Zool. 24, 225–240. Chi, H., Su, H.Y., 2006. Age-stage, two-sex life tables of Aphidius gifuensis (Ashmead) (Hymenoptera: Braconidae) and its host Myzus persicae (Sulzer) (Homoptera: Aphididae) with mathematical proof of the relationship between female fecundity and the net reproductive rate. Environ. Entomol. 35, 10–21. Chi, H., Yang, T.C., 2003. Two-sex life table and predation rate of Propylaea japonica Thunberg (Coleoptera: Coccinellidae) fed on Myzus persicae (Sulzer) (Homoptera: Aphididae). Environ. Entomol. 32, 327–333. Christiansen-Weniger, P., Powell, G., Hardie, J., 1998. Plant virus and parasitoid interactions in a shared insect vector/host. Entomol. Exp. Appl. 86, 205–213. Chu, D., Hu, X., Gao, C., Zhao, H., Nichols, R.L., Li, X., 2012. Use of mitochondrial cytochrome oxidase I polymerase chain reaction-restriction fragment length polymorphism for identifying subclades of Bemisia tabaci Mediterranean group. J. Econ. Entomol. 105, 242–251.

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