Systematic & Applied Acarology 22(7): 1059–1068 (2017) ISSN 1362-1971 (print) http://doi.org/10.11158/saa.22.7.13 ISSN 2056-6069 (online)

Article Functional response of two species preying on Koch

YUAN ZHENG1, PATRICK DE CLERCQ2, ZI-WEI SONG1*, 2, DUN-SONG LI1*& BAO-XIN ZHANG1 1 Guangdong Provincial Key Laboratory of High Technology for Plant Protection/Plant Protection Research Institute, Guangdong Academy of Agricultural Sciences, 7 Jinying Road, Tianhe District, Guangzhou 510640, China 2 Laboratory of Agrozoology, Department of Crop Protection, Ghent University, Coupure Links 653, B-9000 Ghent, Belgium *corresponding author: [email protected]; [email protected]

Abstract

Neoseiulus californicus and N. cucumeris are both potential candidates for the biological control of key pests in China. Whereas N. californicus has mainly been used to control spider , N. cucumeris has been released for the control of thrips and spider mites. To understand the potential of the combined use of N. californicus and N. cucumeris to suppress outbreaks of Tetranychus urticae, the predatory performance of these Neoseiulus species against different stages of T. urticae, either separately or in combination, was evaluated by assessing their functional responses in the laboratory. The values of the attack rate coefficient (α) of N. californicus to each stage of T. urticae exceeded those of N. cucumeris, whereas the handling time (Th) of N. californicus was longer than that of N. cucumeris, except when attacking the larvae of T. urticae. Especially at the higher prey densities, N. cucumeris consumed more eggs per day than N. californicus, whereas N. californicus consumed more larvae. Both predators killed similar numbers of nymphs at each density when tested singly. The searching efficiency of the Neoseiulus species decreased with increasing prey densities, and for all stages of T. urticae, the searching efficiency of the Neoseiulus species tested singly was lower than when they were tested together. The study indicates the potential of mixed releases of N. californicus and N. cucumeris for the management of spider infestations.

Key words: two-spotted spider mite; ; ; searching efficiency

Introduction

The two-spotted spider mite (TSSM), Tetranychus urticae Koch (: Tetranychidae), is one of the most polyphagous herbivores, feeding on more than 1100 plant species, including more than 150 species of economic value and belonging to more than 140 different plant families (Pavela, 2017). This mite has become a serious problem due to the large scale use of chemical insecticides. Widespread acaricide usage has eliminated many of the natural enemies of spider mites, resulting in a reduction in predation pressure on the mite (Wu et al. 2016). Further, because of its rapid developmental rate and high net reproduction, this mite species rapidly develops resistance to acaricides, even after only a few applications (Uddin et al. 2017). As a result, the augmentative release of biological control agents such as predatory mites has become a popular option for managing spider mite outbreaks (Amoah et al. 2016; Gigon et al. 2016; Seiedy et al. 2017; Uddin et al. 2017). Neoseiulus californicus (McGregor) and N. cucumeris (Oudemans) are among the most important predators used in augmentative biological control against mites and thrips (Mendel &

© Systematic & Applied Acarology Society 1059 Schausberger 2011). However, these mites have very different life styles. Neoseiulus californicus shows adaptations for living in spider mites colonies with heavy webbing, and this species belongs to the type II selective predators of tetranychid mites according to the classification of McMurtry et al. (2013). This species has been widely used to control TSSM (Canlas et al. 2006; Barbosa & de Moraes 2015; Liu et al. 2016), but was not a suitable biological control agent for the thrips Caliothrips phaseoli Hood (Thysanoptera: Thripidae) (Toldi et al. 2016). Neoseiulus cucumeris is a generalist phytoseiid mite, which prefers other prey than spider mites, and belongs to the type III predator species (McMurtry et al. 2013). It is commonly used to control thrips on horticultural plants (Xu et al. 2011; Li & Zhang 2016). Due to its inability to cope with the dense spider mite webbing, relatively little attention has been paid to its potential for controlling spider mites; however, with the widening commercialization of N. cucumeris, it is also being applied to control spider mites on fruit trees, cotton and other crops (Li & Zhang 2016; Zhang et al. 2016). The functional response concept has been widely utilized to evaluate effectiveness of predators, and has been used to predict the potential effectiveness of candidates for biological control. Handling time is a good indicator of consumption rate and predator efficacy because it reflects the cumulative time required to capture and kill a prey (Ali et al. 2011). Previous studies have indicated that N. californicus displays high predation rates on the larvae and nymphs of T. urticae (Song et al. 2016), whereas N. cucumeris could develop to the adult stage when offered sufficient fresh eggs of T. urticae (Li & Zhang 2016). To further understand the predatory abilities of N. cucumeris against the immature stages of T. urticae, and to assess the potential of the combined use of N. californicus and N. cucumeris for the control of T. urticae, we evaluated functional responses of these two Neoseiulus species against different life stages of T. urticae, both singly and when combined.

Materials and methods

Mite cultures The initial populations of N. californicus and T. urticae were collected from Carica papaya L. at Guangzhou, China in 2011. Neoseiulus californicus was maintained using mixed stages of T. urticae on bean (Phaseolus vulgaris L.) leaves placed on water-saturated sponges (10 cm in diameter, 3 cm thick) in plastic boxes (15 cm ×15 cm ×6.5 cm). N cucumeris was reared on (Schrank) which was collected from wheat bran and colonies were set up in petri dishes (9cm in diameter) with dry yeast; the petri dishes were placed on water-saturated sponges (13cm in diameter, 3 cm thick) in plastic circular boxes (20 cm in diameter) with water. All cultures were kept in climatic incubators (25±1 °C, 65±10% RH and 16:8 h L:D). The stock colony of T. urticae was maintained on bean leaves under similar conditions.

General experimental conditions The experimental unit consisted in a bean leaf disc (3.5cm diameter) placed upside down on a water- saturated sponge (3.5cm diameter). The leaf discs were surrounded with strips of absorbent paper in order to minimize the escape of individual mites and provide moisture. Individuals trapped in the wet paper surrounding the leaf discs were excluded from data analysis. Every four test units were treated as one test group, and each test group was maintained in a square plastic box as described above. The plastic boxes were filled with water until the water level was just below the leaf disc, and water was added every day. All experiments were conducted at 25 ± 1°C, 65 ± 10% RH and a photoperiod of 16 h : 8 h (L: D). Adult females (< 24 h old) of each predator species were randomly taken from the stock culture; they were isolated from the stock colony before reaching the adult stage in order to

1060 SYSTEMATIC & APPLIED ACAROLOGY VOL. 22 obtain females of uniform age. Then the females were allowed to mate with males for 24h, after which they were starved for another 24h. Each mite was transferred with a fine hair brush to the experimental units for the functional response experiments, and any individuals injured during the transfer were excluded from the experiments.

Functional response experiments Six densities of eggs, larvae, protonymphs and deutonymphs of T. urticae were offered to single adult females of N. californicus or N. cucumeris, and to a combination of one N. californicus female with one N. cucumeris female. The tested densities of eggs and larvae of T. urticae were 10, 20, 30, 40, 50 and 60 per unit; the densities of protonymphs and deutonymphs of T. urticae were 5, 10, 15, 20, 30 and 40 per unit. The different densities of prey eggs were obtained as follows: 5−15 adult females of T. urticae from the stock culture were introduced onto bean leaf discs and allowed to lay eggs for about 24 h under the experimental conditions, after which the females were removed. The numbers of prey eggs were adjusted for each test density by removing excess eggs with a fine brush. For prey larvae and nymphs, sufficient numbers of adult females (about 50) of T. urticae from the stock culture were introduced onto a new bean leaf disc, and allowed to lay eggs for 6 h, after which the females were removed. The discs with eggs were then allowed to develop in a climatic incubator at 25°C. As soon as the larvae or nymphs (protonymphs and deutonymphs) were observed, they were transferred to the experimental units using a fine brush. For each treatment, 10 replicates were done. After 24 h, the number of prey eaten was determined by counting intact eggs and the carcasses of larvae or nymphs.

Data analysis The data from the functional response experiments were analyzed in two steps (Juliano 2001). First, a logistic regression of the proportion of prey consumed (Ne/N0) as a function of initial density (N0) was used to determine the shape of the functional response. The data were fitted to a polynomial function that describes the relationship between the proportion of prey consumed (Ne/N0) and initial density (N0): 2 3 2 3 Ne/N0 = exp(P0 + P1N0 + P2N0 +P3N0 )/[1+exp(P0 + P1N0 + P2N0 +P3N0 )] (1)

where (Ne/N0) is the probability a prey will be consumed, and P0, P1, P2 and P3 are the maximum likelihood estimates of the intercept, linear, quadratic and cubic coefficients, respectively. The values of P0, P1, P2 and P3 were estimated by using a cubic mathematical function for curve estimation (Table 1). The type of functional response was determined by fitting data to the model

(1). The sign of P1 and P2 was used to distinguish the shape of the curves. When the sign of P1 is negative, the predator displays a Type II functional response indicating that the proportion of prey consumed declines monotonically with the initial number of prey. When a positive density- dependent result for the proportion of prey consumed (P1 > 0 and P2 < 0) is obtained, the predator displays a Type III functional response (Juliano 2001; Song et al. 2016). Second, the handling time and the attack rate coefficients of a type II response were estimated using the random predator equation: α Ne = N0{1−exp[ (ThNe−T)]} (2)

where Ne is the number of prey killed; N0 is the initial number of prey; Th is the handling time; and T is the total time available for the predator (24 h). The data was analyzed using SAS software (SAS 2007). The NLIN procedure in SAS was used to estimate the attack rate (α) and handling time

(Th) parameters.

2017 ZHENG ET AL.: FUNCTIONAL RESPONSE OF NEOSEIULUS ON TETRANYCHUS URTICAE 1061 Based on the estimated parameters of the functional response (2), the searching efficiency (E) α α was calculated by the equation: E = / (1+ ThN0) (Beddington 1975). The effect of prey density on the daily consumption by single and combined Neoseiulus species was analyzed by one-way ANOVA followed by Tukey’s test (P=0.05) (SAS 2007).

Results

The linear coefficient (P1) of Equation (1) was negative (Table 1), indicating that the functional response of the studied Neoseiulus species in the single or combined treatments was type II for all life stages of T. urticae. Thus, the “random predator equation” (2) for Type II was used to estimate α the attack rate ( ) and the handling time (Th) (Tables 2 to 4).

TABLE 1. Maximum likelihood estimates (±SE) from a logistic regression of the proportion of Tetranychus urticae in different life stages consumed as a function of initial prey densities by female adults of Neoseiulus californicus and N. cucumeris, both singly and combined.

Neoseiulus californicus Neoseiulus cucumeris Combined species

Prey Para Estimate(±SE) χ2 P Estimate(±SE) χ2 P Estimate(±SE) χ2 P stage meter

Egg P0 4.0514±0.7134 32.25 <0.0001 1.859±0.6209 8.92 0.0028 4.3457±0.8237 27.83 <0.0001

P1 -0.3088±0.0676 20.83 <0.0001 -0.1005±0.0598 2.83 0.0927 -0.2708±0.0743 13.29 0.0003

-3 -3 -3 -3 -3 -3 P2 6.54×10 ±1.95×10 11.30 0.0008 1.75×10 ±1.73×10 1.02 0.3127 6.16×10 ±2.06×10 8.96 0.0028

-5 -5 -5 -5 -5 -5 P3 -5×10 ±1.710 7.93 0.0049 -1×10 ±1.5×10 0.54 0.4632 -5×10 ±1.8×10 6.67 0.0098

Larva P0 4.7270±1.2036 15.43 <0.0001 3.0955±0.6524 22.51 <0.0001 6.4069±1.6550 14.99 0.0001

P1 -0.1381±0.1009 1.87 0.1710 -0.2285±0.0621 13.54 0.0002 -0.2420±0.1337 3.28 0.0702

-4 -4 -3 -3 -3 -3 P2 3.97×10 ±2.66×10 0.02 0.8811 4.85×10 ±1.78×10 7.40 0.0065 3.32×10 ±3.42×10 0.94 0.3313

-5 -5 -5 -5 -5 -5 P3 1.1×10 ±2.2×10 0.27 0.6057 -3×10 ±1.6×10 4.71 0.0300 -1×10 ±2.8×10 0.25 0.6140

Proton P0 3.0638±0.9860 9.65 0.0019 2.4304±0.6830 12.66 0.0004 2.6105±0.8103 10.38 0.0013 ymph P1 -0.0664±0.1372 0.23 0.6281 -0.2579±0.1025 6.33 0.0119 -0.1431±0.1187 1.45 0.2279

-3 -3 -3 -3 P2 -3.81×10 ±5.83×10 0.43 0.5129 0.0107±0.00460 5.45 0.0196 3.64×10 ±5.24×10 0.48 0.4872

-5 -5 -4 -5 -5 -5 P3 8.7×10 ±7.6×10 1.31 0.2516 -1.5×10 ±6.2×10 5.58 0.0181 -3×10 ±7×10 0.20 0.6546

Deuton P0 3.3311±0.6908 23.25 <0.0001 5.0016±0.7964 39.44 <0.0001 2.4997±0.7127 12.30 0.0005 ymph P1 -0.4531±0.1035 19.15 <0.0001 -0.7108±0.1165 37.24 <0.0001 -0.2146±0.1056 4.13 0.0422

-3 -3 P2 0.0174±0.00463 14.03 0.0002 0.0280±0.00510 30.05 <0.0001 6.73×10 ±4.70×10 2.05 0.1521

-4 -5 -4 -5 -5 -5 P3 -2.1×10 ±6.3×10 11.34 0.0008 -3.4×10 ±6.8×10 25.06 <0.0001 -7×10 ±6.3×10 1.22 0.2703

The estimated attack rate coefficients (α) of N. californicus to each stage of T. urticae were greater than those of N. cucumeris (Tables 2 and 3). However, the handling times (Th) of N. californicus feeding on T. urticae were overall longer than those of N. cucumeris, except for the larvae of T. urticae. The maximum attack rates (T/Th, expressed as prey items killed per day) of N. cucumeris on eggs (43.92), protonymphs (34.51) and deutonymphs (73.53) were much higher than the values calculated for N. californicus (eggs: 12.58; protonymphs: 21.30; and deutonymphs: 33.60), whereas the maximum attack rate of N. californicus on larvae (44.66) was higher than that for N. cucumeris (40.45) (Tables 2 and 3). N. cucumeris consumed more eggs than N. californicus per day, and significantly so at densities 50 and 60 prey individuals per arena (Table 5). N. californicus consumed significantly more larvae

1062 SYSTEMATIC & APPLIED ACAROLOGY VOL. 22 than N. cucumeris at each density (Table 6). There was no significant difference between the predation of nymphs by N. californicus and N. cucumeris (Table 7 and 8).

α TABLE 2. Estimates (±SE) of instantaneous attack rate ( ) and handling time (Th) of Neoseiulus californicus on different stages of Tetranychus urticae.

α -1 2 Prey stage (h ) Th (h) T/Th r Egg 0.1840.112 (-0.040–0.407) 1.9070.153 (1.600–2.214) 12.58 0.903 Larva 0.1190.030 (0.060–0.179)0.5370.072 (0.394–0.681) 44.66 0.964 Protonymph 0.1480.034 (0.081–0.216)1.1270.089 (0.949–1.305) 21.30 0.967 Deutonymph 0.0330.005 (0.024–0.043)0.7140.185 (0.345–1.083) 33.60 0.952

The values in parentheses represent 95% confidence intervals. T/Th, maximum attack rate.

 α TABLE 3. Estimates ( SE) of instantaneous attack rate ( ) and handling time (Th) of Neoseiulus cucumeris on different stages of Tetranychus urticae.

α -1 2 Prey stage (h ) Th(h) T/Th r Egg 0.0510.012 (0.027–0.075)0.5460.134 (0.279–0.814) 43.92 0.935 Larva 0.0400.007 (0.027–0.053)0.5930.117 (0.359–0.827) 40.45 0.961 Protonymph 0.0620.013 (0.037–0.087)0.6960.155 (0.385–1.006) 34.51 0.940 Deutonymph 0.0250.008 (0.009–0.042)0.3260.510 (-0.694–1.347) 73.53 0.780

The values in parentheses represent 95% confidence intervals. T/Th, maximum attack rate.

α TABLE 4. Estimates (±SE) of instantaneous attack rate ( ) and handling time (Th) of two Neoseiulus species combined on different stages of Tetranychus urticae.

α -1 2 Prey stage (h ) Th(h) T/Th r Egg 0.0560.012 (0.032–0.079)0.2160.122 (-0.028–0.461) 110.90 0.952 Larva 0.1230.036 (0.050–0.195)0.3660.088 (0.191–0.541) 65.67 0.957 Protonymph 0.0680.015 (0.038–0.099)0.3140.166 (-0.019–0.647) 76.51 0.946 Deutonymph 0.0490.010 (0.029–0.069)0.3650.191 (-0.018–0.748) 65.72 0.934

The values in parentheses represent 95% confidence intervals. T/Th, maximum attack rate.

TABLE 5. Mean (±SE) daily consumption by female adults of single and combined Neoseiulus species at different densities of eggs of Tetranychus urticae.

N. californicus+N. cucumeris Prey density N. californicus N. cucumeris Combined (Theoretical Value) 10 8.40±0.62 bc 7.00±0.58 c 15.40±0.69 a 9.60±0.31 b 20 10.20±0.88 b 13.30±1.21 b 23.50±1.57 a 13.80±1.03 b 30 10.50±1.06 c 14.90±1.21 bc 25.40±1.31 a 19.80±1.68 b 40 11.80±1.25 c 18.80±1.88 bc 30.60±2.42 a 24.60±2.67 ab 50 12.10±1.45 c 23.20±2.34 b 35.30±2.16 a 30.60±2.34 ab 60 12.20±1.60 c 25.10±1.49 b 37.30±1.93 a 36.40±1.55 a

The means followed by different letters within one row (the same density) are significantly different (P<0.05, Tukey’s test).

2017 ZHENG ET AL.: FUNCTIONAL RESPONSE OF NEOSEIULUS ON TETRANYCHUS URTICAE 1063 TABLE 6. Mean (±SE) daily consumption by female adults of single and combined Neoseiulus species at different densities of larvae of Tetranychus urticae.

N. californicus+N. cucumeris Prey density N. californicus N. cucumeris Combined (Theoretical Value) 10 9.50±0.31 b 7.50±0.40 c 17.00±0.52 a 9.90±0.10 b 20 18.40±0.50 b 11.90±0.57 c 30.30±0.87 a 18.80±0.53 b 30 23.60±1.42 b 11.90±1.79 c 35.50±1.36 a 25.40±1.53 b 40 24.20±2.14 b 15.20±1.02 c 39.40±2.33 a 30.80±1.55 b 50 29.10±1.64 b 20.10±1.32 c 49.20±2.58 a 34.80±3.19 b 60 34.50±1.82 b 22.40±1.14 c 56.90±2.11 a 41.80±2.95 b

The means followed by different letters within one row (the same density) are significantly different (P<0.05, Tukey’s test).

TABLE 7. Mean (±SE) daily consumption by female adults of single and combined Neoseiulus species at different densities of protonymphs of Tetranychus urticae.

N. californicus+N. cucumeris Prey density N. californicus N. cucumeris Combined (Theoretical Value) 5 4.60±0.22 b 4.10±0.31 b 8.70±0.42 a 4.40±0.27 b 10 8.90±0.50 b 6.60±0.60 b 15.50±0.73 a 8.20±0.88 b 15 12.80±0.44 b 9.40±0.75 c 22.20±0.71 a 11.40±1.03 bc 20 13.60±0.95 b 12.00±0.87 b 25.60±1.35 a 14.50±0.82 b 30 15.20±0.47 c 17.70±1.19 bc 32.90±1.32 a 20.30±1.61 b 40 18.80±1.38 b 18.60±1.78 b 30.40±2.35 a 26.70±2.12 ab

The means followed by different letters within one row (the same density) are significantly different (P<0.05, Tukey’s test).

TABLE 8. Mean (±SE) daily consumption by female adults of single and combined Neoseiulus species at different densities of deutonymphs of Tetranychus urticae.

N. californicus+N. cucumeris Prey density N. californicus N. cucumeris Combined (Theoretical Value) 5 4.20±0.33 b 4.90±0.10 b 9.10±0.31 a 4.00±0.21 b 10 5.70±0.60 b 4.90±0.77 b 10.60±0.88 a 7.60±0.58 b 15 5.90±0.48 b 5.60±1.12 b 11.50±1.14 a 9.40±0.62 a 20 8.50±0.50 b 7.40±1.24 b 15.90±1.40 a 11.50±1.10 b 30 12.10±0.77 b 11.90±1.66 b 24.00±2.02 a 16.90±1.38 b 40 14.80±0.92 c 15.60±2.98 c 37.40±1.67 a 22.10±2.06 b

The means followed by different letters within one row (the same density) are significantly different (P<0.05, Tukey’s test).

The theoretical values of the predation by N. californicus and N. cucumeris combined were calculated by adding up the observed predation values of N. californicus and N. cucumeris when tested separately. Whereas for the predation of eggs at high densities (40, 50 and 60) by the combined N. californicus and N. cucumeris no significant deviations from the theoretical predation rates were found, the observed predation of eggs at lower densities, and of larvae and nymphs at all densities by the combined N. californicus and N. cucumeris were significantly lower than the theoretical predation rates (Table 5 to 8).

1064 SYSTEMATIC & APPLIED ACAROLOGY VOL. 22 The searching efficiency (E) of single and combined Neoseiulus species when offered different stages of T. urticae at different densities is presented in Figure 1. The searching efficiency of the Neoseiulus species decreased with increasing prey densities, and for all stages of T. urticae, the searching efficiency in the treatments with single females of each species was lower than in the combined treatments.

FIGURE 1. Searching efficiency of single and combined Neoseiulus species when offered different stages of Tetranychus urticae at different densities.

Discussion

In this study, the handling time of N. californicus feeding on T. urticae was longer than that of N. cucumeris except for the larvae of T. urticae, and the daily consumption by the Neoseiulus species at different densities of eggs and larvae showed that overall N. californicus consumed more larvae, whereas N. cucumeris consumed more eggs. Likewise, Li & Zhang (2016) reported that N. cucumeris showed high predation ability on T. urticae eggs. On the other hand, the consumption of protonymphs or deutonymphs by both Neoseiulus species was similar. Thus, under conditions where there is little or no webbing on the leaf surface, like in our laboratory study, N. cucumeris showed the same ability as N. californicus to prey on T. urticae. This can explain why the preventive release of N. cucumeris was shown to be effective against spider mites in China (Li & Zhang 2016).

2017 ZHENG ET AL.: FUNCTIONAL RESPONSE OF NEOSEIULUS ON TETRANYCHUS URTICAE 1065 The actual values of predation by the combined Neoseiulus species on eggs offered at lower densities, and on larvae and nymphs at all densities were significantly lower than the calculated theoretical values. This indicates that both N. californicus and N. cucumeris may have interfered with one and other when foraging for prey, particularly at low prey densities. Indeed, the difference in predator densities among the treatments may have affected the outcome of our experiments: whereas in the single treatments only one female was present per experimental unit, the combined treatment had two females per arena. To fully understand the interference between N. californicus and N. cucumeris, it would be advisable to use the same initial predator density in the functional response experiments. For instance, Farazmand et al. (2012) showed that the per capita searching efficiencies of both N. californicus and Typhlodromus bagdasarjani Wainstein & Arutunjan decreased significantly with increasing predator densities, indicating mutual interference among the phytoseiids. Several semi-field and greenhouse experiments have been conducted to evaluate the effectiveness of releasing multiple species of natural enemies to that of using single species for the control of single or multiple prey species, and they have indicated that in a number of cases different species may facilitate each other and have a synergistic effect on pest control. Releasing P. persimilis together with N. californicus could achieve better control of spider mite infestations (Schausberger & Walzer 2001; Rhodes et al. 2006; Cakmak et al. 2009). Further, Messelink et al. (2008) reported that when offered a mixed diet, the phytoseiids Amblyseius swirskii (Athias-Henriot) and Euseius ovalis (Evans) were better at suppressing thrips and whiteflies. Our laboratory study suggests that the combined release of N. californicus and N. cucumeris has potential for the control of two-spotted spider mite populations. However, it deserves emphasis that the parameters estimated in simple laboratory units cannot be easily extrapolated to field conditions (De Clercq et al. 2000). Further studies should focus on the interference effect between these two species under more realistic conditions and how to effectively combine releases of N. californicus and N. cucumeris in the field.

Acknowledgements

This study was supported by the Science and Technology Planning Project of Guangdong Province, China (2015A020209071) and a Grant-in-aid from the National Key Research & Development (R&D) Plan (2016YFD0200900). We acknowledge the Grant for Overseas Training Projects from the Guangdong Academy of Agricultural Sciences for supporting the international cooperation. We thank two anonymous reviewers for their constructive comments.

References

Ali, M., Naif, A.A. & Huang, D. (2011) Prey consumption and functional response of a phytoseiid predator, Neoseiulus womersleyi, feeding on spider mite, Tetranychus macfarlanei. Journal of Insect Science, 11, 167. Amoah, B., Anderson, J., Erram, D., Gomez, J., Harris, A., Kivett, J., Ruang-Rit, K., Wang, Y., Murray, L. & Nechols, J. (2016) Plant spatial distribution and predator-prey ratio affect biological control of the twospotted spider mite Tetranychus urticae (Acari: Tetranychidae) by the predatory mite Phytoseiulus persimilis (Acari: ). Biocontrol Science and Technology, 26, 548−561. https://doi.org/10.1080/09583157.2015.1133807 Barbosa, M.F.C. & de Moraes, G.J. (2015) Evaluation of astigmatid mites as factitious food for rearing four predaceous phytoseiid mites (Acari: Astigmatina; Phytoseiidae). Biological Control, 91, 22–26.

1066 SYSTEMATIC & APPLIED ACAROLOGY VOL. 22 https://doi.org/10.1016/j.biocontrol.2015.06.010 Beddington, J.R. (1975) Mutual interference between parasites or predators and its effect on searching effi- ciency. Journal of Ecology, 44, 331−340. https://doi.org/10.2307/3866 Blackwood, J.S., Schausberger, P. & Croft, B.A. (2001) Prey-stage preferences in generalist and specialist phy- toseiid mites (Acari: Phytoseiidae) when offered Tetranychus urticae (Acari: Tetranychidae) eggs and lar- vae. Environmental Entomology, 30, 1103−1111. https://doi.org/10.1603/0046-225x-30.6.1103 Cakmak, I., Janssen, A., Sabelis, M.W. & Baspinar, H. (2009) Biological control of an acarine pest by single and multiple natural enemies. Biological Control, 50, 60−65. https://doi.org/10.1016/j.biocontrol.2009.02.006 Canlas, L.J., Amano, H., Ochiai, N. & Takeda, M. (2006) Biology and predation of the Japanese strain of Neo- seiulus californicus (McGregor) (Acari: Phytoseiidae). Systematic & Applied Acarology, 11, 141−157. https://doi.org/10.11158/saa.11.2.2 De Clercq, P., Mohaghegh, J. & Tirry, L. (2000) Effect of host plant on the functional response of the predator Podisus nigrispinus (Heteroptera: Pentatomidae). Biological Control, 18, 65−70. https://doi.org/10.1006/bcon.1999.0808 Denoth, M., Frid, L. & Myers, J.H. (2002) Multiple agents in biological control: improving the odds? Biologi- cal Control, 24, 20−30. https://doi.org/10.1016/S1049-9644(02)00002-6 Gigon, V., Camps, C., & Le Corff, J. (2016) Biological control of Tetranychus urticae by Phytoseiulus macro- pilis and Macrolophus pygmaeus in tomato greenhouses. Experimental & Applied Acarology, 68, 55–70. https://doi.org/10.1007/s10493-015-9976-2 Farazmand, A., Fathipour, Y. & Kamali, K. (2012) Functional response and mutual interference of Neoseiulus californicus and Typhlodromus bagdasarjani (Acari: Phytoseiidae) on Tetranychus urticae (Acari: Tet- ranychidae). International Journal of Acarology, 38, 369−376. https://doi.org/10.1080/01647954.2012.655310 Juliano, S.A (2001) Non-linear curve fitting: predation and functional response curves. In: Schneider, S.M. & Gurevitch, J. (eds.) Design and analysis of ecological experiments. Oxford University Press, New York, pp. 178–196. Li, G.Y. & Zhang, Z.Q. (2016) Some factors affecting the development, survival and prey consumption of Neo- seiulus cucumeris (Acari: Phytoseiidae) feeding on Tetranychus urticae eggs (Acari: Tetranychidae). Sys- tematic & Applied Acarology, 21, 555−566. https://doi.org/10.11158/saa.21.5.1 Liu, R., Nyoike, T.W. & Liburd, O.E. (2016) Evaluation of site-specific tactics using bifenazate and Neoseiulus californicus for management of Tetranychus urticae (Acari: Tetranychidae) in strawberries. Experimental & Applied Acarology, 70, 189−204. https://doi.org/10.1007/s10493-016-0073-y McMurtry, J.A., De Moraes, G.J. & Sourassou, N.F. (2013) Revision of the lifestyles of phytoseiid mites (Acari: Phytoseiidae) and implications for biological control strategies. Systematic & Applied Acarology, 18, 297−320. https://doi.org/10.11158/saa.18.4.1 Mendel, D. & Schausberger, P. (2011) Diet-dependent intraguild predation between the predatory mites Neo- seiulus californicus and Neoseiulus cucumeris. Journal of Applied Entomology, 135, 311−319. https://doi.org/10.1111/j.1439-0418.2010.01548.x Messelink, G.J., van Maanen, R., van Steenpaal, S.E.F. & Janssen, A. (2008) Biological control of thrips and whiteflies by a shared predator: Two pests are better than one. Biological Control, 44, 372−379. https://doi.org/10.1016/j.biocontrol.2007.10.017 Pavela, R. (2017) Extract from the roots of Saponaria officinalis as a potential acaricide against Tetranychus urticae. Journal of Pest Science, 90, 683−692. https://doi.org/10.1007/s10340-016-0828-6 Rhodes, E.M., Liburd, O.E., Kelts, C., Rondon, S.I. & Francis, R.R. (2006) Comparison of single and combi- nation treatments of Phytoseiulus persimilis, Neoseiulus californicus, and Acramite (bifenazate) for con- trol of twospotted spider mites in strawberries. Experimental & Applied Acarology, 39, 213−225. https://doi.org/10.1007/s10493-006-9005-6

2017 ZHENG ET AL.: FUNCTIONAL RESPONSE OF NEOSEIULUS ON TETRANYCHUS URTICAE 1067 SAS (2007) SAS/Stat. Software. Hangen and Enhanced, USA, SAS, Institute Incorporation. Schausberger, P. & Walzer, A. (2001) Combined versus single species release of predaceous mites: predator– predator interactions and pest suppression. Biological Control, 20, 269−278. https://doi.org/10.1006/bcon.2000.0908 Seiedy, M., Soleymani, S. & Hakimitabar, M. (2017) Development and reproduction of the predatory mite Amblyseius swirskii Athias-Henriot (Acari: Phytoseiidae) on Tetranychus urticae Koch (Acari: Tetranych- idae) and Bemisia tabaci Gennadius (Heteroptera: Aleyrodidae). International Journal of Acarology, 43, 160–164. https://doi.org/10.1080/01647954.2016.1248486 Song, Z.W., Zheng, Y., Zhang, B.X. & Li, D.S. (2016) Prey consumption and functional response of Neosei- ulus californicus and Neoseiulus longispinosus (Acari: Phytoseiidae) on Tetranychus urticae and Tetrany- chus kanzawai (Acari: Tetranychidae). Systematic & Applied Acarology, 21, 936−946. https://doi.org/10.11158/saa.21.7.7 Toldi, M., Reichert, M.B., Rode, P.A., Johann, L. & Ferta, N.J. (2016) Influence of various preys in soybean and the biological performance of the predatory mite Neoseiulus californicus (Phytoseiidae). Systematic & Applied Acarology, 21, 1662−1669. https://doi.org/10.11158/saa.21.12.7 Uddin, M.N., Alam, M.Z., Miah, M.R.U., Mian, M.I.H. & Mustarin, K.E. (2017) Life table parameters of an indigenous strain of Neoseiulus californicus McGregor (Acari: Phytoseiidae) when fed Tetranychus urti- cae Koch (Acari: Tetranychidae). Entomological Research, 47, 84−93. https://doi.org/10.1111/1748-5967.12202 Wu, S.Y., Xie, H.C., Li, M.Y., Xu, X.N. & Lei, Z.R. (2016) Highly virulent Beauveria bassiana strains against the two-spotted spider mite, Tetranychus urticae, show no pathogenicity against five phytoseiid mite spe- cies. Experimental & Applied Acarology, 70, 421–435. https://doi.org/10.1007/s10493-016-0090-x Xu, X.N., Borgemeister, C. & Poehling, H.M. (2011) Interactions of , two-spotted spider mites and the predatory mite Amblyseius cucumeris (Oudemans) on beans. Chinese Journal of Applied Entomology, 48, 579−587. Zhang, Y.X., Lin, G.Y., Wei, H., Lin, J.Z., Tian, R.D., Chen, X., Sun, L. & Zeng, Y. (2016) Evaluation of Neo- seiulus cucumeris (Oudemans) as a biological control for Oliganychus ununguis (Jacobi) (Acari: Tetrany- chidae). Chinese Journal of Applied Entomology, 53, 55−63.

Submitted: 5 May 2017; accepted by Zhi-Qiang Zhang: 29 Jun. 2017; published: 17 Jul. 2017

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