Appl. Entomol. Zool. 45 (3): 387–393 (2010) http://odokon.org/
Temperature-dependent life history of the green plant bug, Apolygus lucorum (Meyer-Dür) (Hemiptera: Miridae)
Yanhui LU,1 Kongming WU,1,* Kris A. G. WYCKHUYS2 and Yuyuan GUO1 1 State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences; Beijing 100193, China 2 Horticulture Research Center, Universidad de Bogota Jorge Tadeo Lozano; Chia (Cundinamarca), Colombia (Received 2 November 2009; Accepted 7 April 2010)
Abstract Apolygus lucorum (Meyer-Dür) (Hemiptera: Miridae) is an important agricultural pest and may cause serious yield losses to numerous crops in eastern Asia, such as cotton (Gossypium hirsutum L.) production throughout northern China. In this paper, we determined the effect of six constant temperatures (10, 15, 20, 25, 30, and 35ºC) on A. luco- rum life history. Successful nymphal development and adult emergence were reported for all temperature regimes, whereas egg eclosion was not observed at 10ºC. Development time decreased with increasing temperature between 10 and 30ºC, slightly increasing at 35ºC. Lower development thresholds of egg and nymphal stages were estimated as 3.2 and 3.7ºC, and their thermal constants were 179.2 and 262.4 DD, respectively. Optimum and lethal temperatures for development were 33.8 and 42.5ºC for eggs, and 31.0 and 38.5ºC for nymphs, respectively. Adult longevity declined with increasing temperature. Fecundity greatly decreased at extreme temperatures (i.e., 10 and 35°C), with the highest value at 20ºC. Our findings could help predict A. lucorum population dynamics in different agro-production regions of eastern Asia and subsequently develop appropriate pest forecasting and management protocols.
Key words: Apolygus lucorum; temperature; life history
al., 1997; Lee et al., 2002; Wu et al., 2002; Lu and INTRODUCTION Wu, 2008; Lu et al., 2008a). The green plant bug, Apolygus lucorum (Meyer- In China, prior to commercial cultivation of Dür) (Hemiptera: Miridae) is a polyphagous insect transgenic Bt (Bacillus thuringiensis) cotton, A. lu- pest that affects multiple agricultural crops, vegeta- corum was kept at a low population level in cotton bles, stone fruits, ornamentals and pastures (Cao through frequent insecticide sprays for Helicoverpa and Wan, 1983; Lu and Wu, 2008). Both A. luco- armigera control; however, the commercial release rum nymphs and adults feed on a variety of plant of Bt cotton in 1997 meant a sharp drop in insecti- organs, causing plant stunting, abscission of cide use in this crop (Wu and Guo, 2005; Wu et al., squares and bolls (in cotton, Gossypium hirsutum 2008) and the subsequent appearance of A. luco- L.) and fruit malformation (Chu and Meng, 1958; rum and Adelphocoris spp. (Hemiptera: Miridae) Lu and Wu, 2008). At high population densities, A. as key pests (Wu et al., 2002; Lu et al., 2008a). The lucorum cause considerable yield and quality steady increase in A. lucorum population levels losses (Lu and Wu, 2008). This species is cosmo- since 1997 has resulted in this species presently politan, with a reported occurrence in Asia, Africa, causing yield losses in multiple other crops (Lu et Europe and North America (Zhang and Zhao, al., 2007a; Lu and Wu, 2008). Due to its long-dis- 1996). Especially in eastern Asia (inc. China, tance flight behaviour, an area-wide outbreak of A. Japan, Korea), A. lucorum is considered a key agri- lucorum is common in China (Lu and Wu, 2008). cultural pest (Cao and Wan, 1983; Miyata, 1993, During 2002–2009, many migratory individuals of 1994; Watanabe, 1995, 1996, 1999; Watanabe et A. lucorum were captured on Beihuang Island,
* To whom correspondence should be addressed at: E-mail: [email protected] DOI: 10.1303/aez.2010.387
387 388 Y. LU et al.
40–60 km from the Chinese mainland (Lu et al., Experiments were conducted at six constant 2007b; K. M. Wu, unpublished data). Hence, this temperatures (10, 15, 20, 25, 30, and 35ºC) in envi- pest also has the potential to disperse to other ronmental growth chambers (Ningbo Jiangnan In- countries, subsequently leading to population out- strument Factory, Ningbo, China) with a photope- breaks all over eastern Asia. riod of LD 14:10 h and 60 10% RH. Temperatures Amongst others, the actual acquisition of pest were maintained at 0.5ºC around the set point, and status in many major agricultural crops and the each temperature regime was considered a separate rapid geographic expansion of A. lucorum have treatment. been facilitated by a lack of appreciation of its phe- Immature development and survival. The nology (Lu et al., 2007a). Although A. lucorum methodology used was similar to Bommireddy et population dynamics have been extensively studied al. (2004) and Lu et al. (2009). Prior to the experi- in cotton fields (Ting, 1964; Wu et al., 2002; Guo ment, 4-cm-long green beans were placed for 24 h et al., 2005; Xu et al., 2007; Lu et al., 2008a; Fan et as oviposition substrate in adult rearing containers. al., 2009), only limited data are available on its life After the allotted time, bean sections were re- history traits (Ting, 1963; Men et al., 2008). Addi- moved, the number of deposited eggs was deter- tionally, distinct results had been described in two mined, and sections were subsequently placed in a previous studies (Ting, 1963; Men et al., 2008). container at a given temperature regime. Egg Therefore, a sound computation of the life history hatching was recorded daily for 25 d and newly- characteristics of A. lucorum is necessary and emerged nymphs were removed from containers. could allow an appropriate pest management re- Three batches of eggs (i.e., 30 to 80 eggs) were in- sponse for these emergent pests (Lu et al., 2009). cluded per temperature regime. In this paper, we describe the effect of constant Newly-emerged nymphs were placed singly into temperatures on A. lucorum development, survival 5 cm high, 1.5 cm diam. glass vials covered with a and fecundity. Our data should help develop pest nylon screen. Each glass vial contained a green forecasting programs and improve current manage- bean section as a food and water source, and a 1 5 ment strategies for one of the most important agri- cm paper strip. Nymphal development and mortal- cultural pests in eastern Asia. ity were recorded daily until adult molting or death occurred. Sixty to 90 nymphs were included per temperature treatment. MATERIALS AND METHODS Adult longevity and reproduction. Adults that Insect culture. A laboratory culture of A. luco- emerged under each temperature regime were rum was initiated with individuals collected from paired and placed into (3 cm high, 3 cm diameter) cotton fields at the Langfang Experimental Station glass vials with a nylon screen. Within each vial, (39.53ºN, 116.70ºE) of the Chinese Academy of we provided a 10% sucrose solution and included a Agricultural Sciences in Hebei Province (China) 4-cm-long green bean section as food and oviposi- from July to August 2005. The colony was kept in tion substrate. Bean sections were changed daily 20 10 6 cm rearing containers and maintained and inspected for presence of eggs. Adult mortality on green beans (Phaseolus vulgaris L.) and a 10% was recorded daily, and dead individuals were not sucrose solution (Lu et al., 2007b, 2008b). Green replaced. Per temperature regime, 20 to 40 mating beans also served as the oviposition substrate and pairs were included, and respective adult longevity were changed every other day. Beans containing and fecundity were recorded. eggs were subsequently placed in rearing contain- Data analysis and model development. Prior to ers lined with filter paper. At nymphal emergence, analysis, normality and homoscedasticity of data individuals were transferred to identical containers, were determined. Parametric statistics were used covered with nylon organdy mesh to allow air cir- for normally distributed data, while non-parametric culation, and provided with fresh food every two analyses were conducted on data sets that did not days until adult emergence. Each container housed comply with this assumption, even after transfor- about one hundred nymphs or sixty to eighty mation (Zar, 1999; Sokal and Rohlf, 2001). To de- adults. The colony was maintained at 29 1ºC, termine the effect of temperature on adult 60 5% RH and 14:10 (L:D). longevity, the pre-oviposition period and female fe- Temperature and Life History of A. lucorum 389 cundity, the Kruskal-Wallis test was used. When a RESULTS significant difference (p 0.05) was detected by the test, a comparison between temperatures was per- Immature development and survival formed using the Steel-Dwass test. Nymphs completed full development at all tem- Percentage data (i.e., nymphal survival, egg peratures, but no egg hatching was recorded after hatching rate) were arcsine transformed and com- 25 d incubation at 10ºC. Nymphal developmental pared between treatments using one-way ANOVA time gradually dropped with increasing tempera- followed by a Tukey’s honestly significant differ- ture until 30ºC, slightly increasing again at 35ºC ence (HSD) test (p 0.05). Nymphs that died prior (Table 1). The relationship between the develop- to adult eclosion and adults that produced no eggs ment rate (y) and temperature (x) were y 0.006x were excluded from the respective analyses. 0.018 (p 0.001) for eggs and y 0.004x 0.014 The effect of temperature on the development (p 0.001) for nymphs. Lower development thresh- rate of the various stages was characterized by lin- olds of eggs and nymphs were estimated at 3.2 and ear regression using the model y bx a, where y is 3.7ºC, respectively. Respective degree-day accumu- the development rate (1/development time), x is lations were 179.2 and 262.4 DD. The nonlinear temperature, and a and b are regression parame- Logan model VI gave a good fit to the data (p ters. The lower development threshold (To) and 0.004 for egg; p 0.008 for nymph) (Table 2; Fig. thermal constant requirement (DD) were estimated 1). Optimum temperatures were estimated at 34.0 using the parameters: To a/b and DD 1/b and 31.5ºC, and lethal temperatures at 43.4 and (Campbell et al., 1974). Estimation of the constants 39.7ºC for eggs and nymphs, respectively (Table To and DD was based on data obtained from the 2). The egg incubation rate and nymphal survival temperature range 10–30ºC. Also, the non-linear differed significantly between temperature regimes Logan VI model was used to describe the relation- (p 0.020 for egg; p 0.001 for nymph), with max- ship between temperature (10–35ºC) and the rate imum rates at 30ºC (Table 3). of development, principally because of the bio- logical significance of its parameters (Logan et Adult longevity and fecundity al., 1976). Y P1 {exp[P2 (X To)] exp[P2 Adult longevity significantly differed between (Tmax To) P3 (Tmax X)]} where X is tempera- temperature regimes (Kruskal-Wallis test; p 0.001 ture, To is the lower developmental threshold, Tmax for male and female), and declined with mounting is the upper (lethal) temperature developmental temperature. The length of the pre-oviposition pe- threshold, and P1, P2, and P3 are coefficients. The riod decreased significantly as temperature in- optimum temperature for development was calcu- creased, but increased again at 35ºC (Table 3). lated after setting the first derivative of the Logan Lower development thresholds and degree-day ac- equation equal to zero. Data fitting was done using cumulations during the pre-oviposition period were JMP IN software (SAS Institute, 2005). 0.8ºC and 191.7 DD, respectively. At a given tem- perature, longevity did not differ between gender
Table 1. Developmental time (days) of immature A. lucorum at different temperatures
Temperature (°C) Stage 10 15 20 25 30 35
Egg —a 14.9 0.3 11.0 0.2 8.2 0.1 6.7 0.1 6.3 0.1 First instar 7.3 0.4 5.6 0.2 3.6 0.1 3.0 0.1 2.0 0.1 2.6 0.2 Second instar 5.9 0.4 4.0 0.2 2.8 0.2 1.6 0.1 1.6 0.1 2.3 0.4 Third instar 5.6 0.5 4.4 0.2 2.4 0.1 2.2 0.1 1.5 0.1 1.7 0.3 Fourth instar 6.5 0.4 4.5 0.2 2.6 0.1 1.8 0.1 1.9 0.1 2.1 0.3 Fifth instar 12.9 0.7 7.7 0.2 4.1 0.1 3.2 0.1 3.0 0.1 2.4 0.3 Total nymph 38.2 0.8 26.2 0.2 15.5 0.2 11.8 0.2 10.2 0.2 11.1 0.6
a No eggs hatched after 25 d incubation. 390 Y. LU et al.
Table 2. Parameters of the Logan VI equation, upper temperature thresholds and optimum developmental temperatures for the immature stages of A. lucorum
Upper threshold Optimum Stage P P P p 1 2 3 (°C) temperature (°C)
Egg 0.034 0.085 0.130 0.007 43.4 34.0 Nymph 0.030 0.113 0.132 0.002 39.7 31.5
Fig. 1. Fitting the Logan VI model to development rate data of A. lucorum egg (A) and nymphal (B) stages at different temper- atures.
(p 0.05) (Table 3). Fecundity varied between tem- Most of our findings were similar to those of perature regimes (p 0.001), with the highest val- Ting (1963) but vastly different from those of Men ues at 20ºC and lowest at 35ºC (Table 3). et al. (2008) (Table 4). Distinct results may be re- lated to differences in the experimental temperature range, environmental humidity or geographic DISCUSSION strains, as observed in other insects (Trimble and Temperature is a key determining factor in the Lund, 1983; Stacey and Fellowes, 2002, Fantinou life history of various mirid species (Ting, 1963; et al., 2003). More specifically, Men et al. (2008) Wheeler, 2001; Bommireddy et al., 2004; Lu et al., conducted their research on an A. lucorum strain 2009). Similar to other studies on mirid ecology, from Shandong province over a temperature this paper shows that different temperatures greatly range of 17–29ºC and 80% RH; however, the aver- affected the development, fecundity and longevity age temperatures during February–March in key of A. lucorum. cotton growing regions of northern China range Temperature and Life History of A. lucorum 391
Table 3. Immature survival rate, adult longevity and fecundity of A. lucorum at different temperatures
Survival rate (%) Adult longevity (d) Fecundity Temperature Pre-oviposition (No. eggs per (°C) period (d) Egg Nymph Male Female female)
10 —a 38.7 4.8 bb 46.3 4.7 a 56.9 7.5 a 22.1 1.5 a 28.0 2.5 b 15 33.1 2.7 b 65.3 7.4 ab 40.7 4.6 ab 47.7 5.4 ab 14.1 0.8 b 56.7 7.7 ab 20 43.1 8.4 ab 74.7 3.5 a 34.8 3.6 ab 40.2 4.5 abc 9.8 0.4 c 84.4 14.9 a 25 64.6 5.0 a 54.7 5.8 ab 31.3 3.1 bc 34.1 2.0 bcd 8.4 0.3 c 81.3 12.7 a 30 67.0 7.4 a 77.3 7.4 a 21.9 1.7 c 25.6 1.6 cd 6.7 0.5 c 73.9 11.9 a 35 53.5 7.3 ab 9.3 1.3 c 18.1 1.7 c 19.9 1.6 d 6.9 0.9 c 21.9 3.8 b
a No eggs incubated. b Means ( SE) within a column followed by different letters are significantly different (Tukey’s HSD, p 0.05 for survival rate; Steel-Dwass test, p 0.05 for other variables).
Table 4. Lower development threshold (To, ºC) and thermal constant (DD) of A. lucorum compared with other three common mirid species in China
Egg Nymph Species Host plant Reference To (°C) DD To (°C) DD
A. lucorum Green beans 3.2 179.2 3.7 262.4 Present study Cotton 3.0 188 4.6 340 Ting, 1963a Green beans 6.3 160.1 9.5 210.3 Men et al., 2008 Adelphocoris suturalis Cotton 5.4 214 9.0 329 Ting, 1963 Green beans 5.6 189.9 5.0 308.8 Lu et al., 2009 Adelphocoris fasciaticollis Cotton 7.8 186 7.0 373 Ting, 1963 Green beans 6.7 188.8 3.0 366.7 Lu et al., 2009 Adelphocoris lineolatus Cotton 5.2 213 6.7 409 Ting, 1963 Green beans 5.6 231.7 6.2 291.6 Lu et al., 2009
a In Ting (1963), To was accurate to the first decimal point and DD was kept as an integer. between 0–7ºC. Based upon the lower developmen- Certain temperature extremes may prove detri- tal threshold for eggs (i.e., 6.2°C) calculated by mental to insect development (Andrewartha and Men et al. (2008), overwintering eggs of A. luco- Birch 1954; Wang et al. 1982; Briere et al., 1999). rum may not hatch in early April; however, as sub- In our study, nymphal development was slow at the stantial A. lucorum egg hatching is recorded during highest temperatures. Maximum temperatures were this time period in northern China (Cao and Wan, reported as 43.4ºC for egg development and 39.7ºC 1983; Lu and Wu, 2008), computed threshold lev- for nymphs, with optimal temperatures of 34.0ºC els very likely were overestimated. Also, the lower and 31.5ºC, respectively. To avoid negative effects developmental threshold of A. lucorum was lower of elevated temperatures in their natural habitats, than for other mirid pests, such as Adelphocoris su- A. lucorum nymphs and adults tend to take shelter turalis, Adelphocoris fasciaticollis and Adelpho- under leaf surfaces or flowers (Chu and Meng, coris lineolatus (Ting, 1963; Lu et al., 2009) (Table 1958). Similarly, A. lucorum eggs are inserted into 4). These dissimilarities are consistent with their plant tissues, and hence likely benefit from the rel- phenology. In northern China, A. lucorum usually atively stable conditions in the plant interior (Chu has five generations per year, while Adelphocoris and Meng, 1958). spp. only have three or four generations, and A. lu- The response of an insect species or strain to a corum overwintering eggs hatch earlier than eggs given temperature regime is inherently linked to its of Adelphocoris spp. (Lu and Wu, 2008). geographic distribution (Keena, 2006). The favor- 392 Y. LU et al. able development and high survival across a broad Briere, J. F., P. Pracros, A. P. Roux and J. S. Pierre (1999) A temperature range of A. lucorum is in agreement novel model of temperature-dependent development for with its geographic distribution throughout China arthropods. Environ. Entomol. 28: 22–29. Campbell, A., B. D. Frazer, N. Gilbert, A. P. Gutierrez and M. (Lu and Wu, 2008; Lu et al., 2008a). Aside from its Mackauer (1974) Temperature requirements of some effect on development time, temperature also influ- aphids and their parasites. J. Appl. Ecol. 11: 431–438. ences a multitude of fitness parameters, such as Cao, C. Y. and C. S. Wan (1983) Management of Cotton adult longevity and fecundity. Our research showed Mirids. Shanghai Science and Technology Press, that A. lucorum fecundity is greatest at 20ºC, and Shanghai. 60 pp. (in Chinese). adult longevity gradually drops with increasing Chu, H. F. and H. L. Meng (1958) Studies on three species of cotton plant bugs, Adelphocoris taeniophorus Reuter, temperature. Higher temperatures increase metabo- A. lineolatus (Goeze), and Lygus lucorum Meyer-Dür lism and consequently reduce life span proportion- (Hemiptera: Miridae). Acta Entomol. Sin. 8: 97–118 (in ally (Slansky and Scriber, 1985). Considering the Chinese with English summary). temperature effects on A. lucorum development Fan, G. H., D. G. Li, Z. S. Li and F. J. Gao (2009) Influence and fitness, we designated 25–28ºC as an optimal of ecological habitat on the occurrence and dynamics of Lygus lucorum Mayer and its natural predator. Chinese temperature range for rearing this species in the J. Eco-Agri. 17: 728–733 (in Chinese with English sum- laboratory (Lu et al., 2008b). mary). In addition to temperature, rainfall and other abi- Fantinou, A. A., D. C. Perdikis and C. S. Chatzoglou (2003) otic factors are likely to affect the A. lucorum life Development of immature stages of Sesamia nonagioides history, and indirectly its distribution and phenol- (Lepidoptera: Noctuidae) under alternating and constant ogy. Rainfall can lead to substantial increases in A. temperatures. Environ. Entomol. 32: 1337–1342. Guo, J. Y., H. X. Zhou, F. H. Wan, X. J. Liu and Z. J. Han lucorum population numbers (Ting, 1964; Wu et (2005) Population dynamics and damage of Lygus luco- al., 2002), and rainfall patterns may therefore also rum in Bt cotton fields under two control measures. have an effect in determining geographic distribu- Chinese Bull. Entomol. 42: 424–428 (in Chinese with tion and phenology; however, much remains to be English summary). investigated on the effect of rainfall and relative Keena, M. A. (2006) Effects of temperature on Anoplophora glabripennis (Coleoptera: Cerambycidae) adult survival, humidity on A. lucorum development, survival, fe- reproduction, and egg hatch. Environ. Entomol. 35: cundity, and population dynamics. 912–921. Although insects are naturally not subject to Lee, S., G. S. Lee and H. G. Goh (2002) Mirid bugs (Het- constant temperature regimes, such as those em- eroptera: Miridae) on grapevine: their damages and host ployed in our assays (Summers et al., 1984), our plants. Korean J. Appl. Entomol. 41: 33–41 (in Korean work does provide valuable information on A. luco- with English summary). Logan, J. A., D. J. Wollkind, S. C. Hoyt and L. K. Tanigoshi rum life history. Some of our findings could be (1976) An analytic model for description of tempera- used to predict population dynamics, and help im- ture dependent rate phenomena in arthropods. Environ. prove current pest management practices for A. lu- Entomol. 5: 1133–1140. corum in several agro-production environments of Lu, Y. H. and K. M. Wu (2008) Biology and Control of the eastern Asia. Mirids. Golden Shield Press, Beijing. 151 pp. (in Chi- nese). ACKNOWLEDGMENTS Lu, Y. H., G. M. Liang and K. M. Wu (2007a) Advances in integrated management of cotton mirids. Plant Prot. 33: This research was supported by the Chinese Ministry of Sci- 10–15 (in Chinese with English summary). ence and Technology (973 Projects Grant, 2006CB102004), Lu, Y. H., K. M. Wu and Y. Y. Guo (2007b) Flight potential National Key Project of Scientific and Technical Supporting of Lygus lucorum Meyer-Dür (Heteroptera: Miridae). Programs (2006BAD08A07) and Commonwealth Agricultural Environ. Entomol. 36: 1007–1013. Scientific Research Project (200803011). Lu, Y. H., F. Qiu, H. Q. Feng, H. B. Li, Z. C. Yang, K. A. G. REFERENCES Wyckhuys and K. M. Wu (2008a) Species composition and seasonal abundance of pestiferous plant bugs Andrewartha, H. C. and L. C. Birch (1954) The Distribution (Hemiptera: Miridae) on Bt cotton in China. Crop Prot. and Abundance of Animals. University of Chicago 27: 465–472. Press, Chicago, IL. 782 pp. Lu, Y. H., K. M. Wu, X. M. Cai and Y. Q. Liu (2008b) A Bommireddy, P. L., M. N. Parajulee and D. O. Porter (2004) rearing method for mirids using the green bean, Phaseo- Influence of constant temperatures on life history on im- lus vulgaris in the laboratory. Acta Phytophylacica Sin. mature Lygus elisus (Hemiptera: Miridae). Environ. En- 35: 215–219 (in Chinese with English summary). tomol. 33: 1549–1553. Lu, Y. H., K. M. Wu, K. A. G. Wyckhuys and Y. Y. Guo Temperature and Life History of A. lucorum 393
(2009) Comparative study of temperature-dependent Wang, R. S., Z. X. Lan and Y. C. Ting (1982) Studies on life histories of three economically important Adelpho- mathematical models of the relationships between insect coris spp. Physiol. Entomol. 34: 318–324. development and temperature. Acta Ecol. Sin. 2: 47–57 Men, X. Y., Y. Yu, A. S. Zhang, L. L. Li, J. T. Zhang and F. Ge (in Chinese with English summary). (2008) Life table of the laboratory population of Lygus Watanabe, K. (1995) Occurrence of Lygocoris (Apolygus) lu- lucorum Meyer-Dür (Hemiptera: Miridae) at different corum (Meyer-Dür) (Heteroptera: Miridae) and damage temperatures. Acta Entomol. Sin. 51: 1216–1219 (in on cherry. Ann. Rept. Plant Prot. North Japan 46: Chinese with English summary). 161–163 (in Japanese with English summary). Miyata, M. (1993) Damage to chrysanthemum by sucking of Watanabe, K. (1996) Characteristic of damages of Lygocoris plant bugs, Lygocoris lucorum Meyer-Dür. Ann. Rept. (Apolygus) lucorum (Meyer-Dür) (Heteroptera: Miridae) Plant Prot. North Japan 44: 172–174 (in Japanese with and Halyomorpha halys (Stal) (Heteroptera: Pentatomi- English summary). dae) on cherry. Ann. Rept. Plant Prot. North Japan 47: Miyata, M. (1994) Damage to chrysanthemum by sucking of 143–144 (in Japanese with English summary). a plant bug, Lygocoris lucorum (Meyer-Dür) (Hemiptera: Watanabe, K. (1999) Damages and control of Lygocoris Miridae). Ann. Rept. Plant Prot. North Japan 45: (Apolygus) lucorum (Meyer-Dür) (Heteroptera: Miridae) 181–183 (in Japanese with English summary). on Cherry. Plant Prot. 43: 56–59 (in Japanese with SAS Institute (2005) SAS/STAT User’s Guide. SAS Insti- English summary). tute, Cary, NC. Watanabe, K., S. Kikuchi and T. Tanaka (1997) Seasonal oc- Slansky, F. and J. M. Scriber (1985) Food consumption and currence of Lygocoris (Apolygus) lucorum (Meyer-Dür) utilization. In Comprehensive Insect Physiology, Bio- (Heteroptera: Miridae) on Artemisia spp. Ann. Rept. chemistry, and Pharmacology (G. A. Kerkut and L. I. Plant Prot. North Japan 48: 181–183 (in Japanese with Gilbert, eds.). Pergamon Press, Oxford, pp. 87–163. English summary). Sokal, R. R. and F. J. Rohlf (2001) Biometry. 3rd edition. Wheeler, A. G. Jr. (2001) Biology of the Plant Bugs Freeman, New York, NY. 887 pp. (Hemiptera: Miridae): Pests, Predators, Opportunists. Stacey, D. A. and D. E. Fellowes (2002) Temperature and the Cornell University Press, Ithaca, NY. 528 pp. development rates of thrips: evidence for a constraint on Wu, K. M. and Y. Y. Guo (2005) The evolution of cotton local adaptation. Eur. J. Entomol. 99: 399–404. pest management practices in China. Annu. Rev. Ento- Summers, C. G., R. L. Coviello and A. P. Gutierrez (1984) mol. 50: 31–52. Influence of constant temperatures on the development Wu, K., W. Li, H. Feng and Y. Guo (2002) Seasonal abun- and reproduction of Acyrthosiphum kondoi (Homoptera: dance of the mirids, Lygus lucorum and Adelphocoris Aphididae). Enviorn. Entomol. 13: 236–242. spp. (Hemiptera: Miridae) on Bt cotton in northern Ting, Y. Q. (1963) Studies on the ecological characteristics China. Crop Prot. 21: 997–1002. of cotton mirids I. effect of temperature and humidity on Wu, K. M., Y. H. Lu, H. Q. Feng, Y. Y. Jiang and J. Z. Zhao the development and distribution of the pests. Acta Phy- (2008) Suppression of cotton bollworm in multiple tophylacica Sin. 2: 285–296 (in Chinese with English crops in China in areas with Bt toxin-containing cotton. summary). Science 321: 1676–1678. Ting, Y. Q. (1964) Studies on the population fluctuations Xu, W. H., T. Y. Bian, B. Liu, R. M. Wang and Y. P. Zhen of cotton mirids in the cotton cultivation region of (2007) Population dynamics of dominant mirid species Kwanchung, Shensi, China. Acta Entomol. Sin. 13: in transgenic Bt cotton field. Acta Agri. Jiangxi 19: 298–310 (in Chinese with English summary). 53–58 (in Chinese). Trimble, R. M. and C. T. Lund (1983) Intra- and interpopu- Zar, J. H. (1999) Biostatistical Analysis. 4th edition. Pren- lation variation in the thermal characteristics of preadult tice-Hall, Upper Saddle River, NJ. 718 pp. development of two latitudinally diverse populations of Zhang, S. M. and Y. X. Zhao (1996) The Geographical Dis- Toxorhynchites rutilus septentrionalis (Diptera: Culici- tribution of Agricultural and Forest Insects in China. dae). Can. Entomol. 115: 659–662. China Agriculture Press, Beijing. 400 pp. (in Chinese).