Effects of Transgenic Cry1ab Rice Pollen on Fitness of Propylea Japonica
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J Pest Sci (2005) 78: 123–128 DOI 10.1007/s10340-004-0078-x ORIGINAL ARTICLE Y. Y. Bai Æ M. X. Jiang Æ J. A. Cheng Effects of transgenic cry1Ab rice pollen on fitness of Propylea japonica (Thunberg) Received: 17 September 2004 / Published online: 8 February 2005 Ó Springer-Verlag 2005 Abstract The transgenic rice lines Kemingdao 1 (KMD1) Keywords Cry1Ab toxin Æ Ecological and Kemingdao 2 (KMD2) contain a synthetic cry1Ab risk Æ Pollen Æ Propylea japonica Æ Transgenic rice gene derived from Bacillus thuringiensis Berliner and are highly resistant to rice stem borers and foliage-feeding lepidopterans. Propylea japonica (Coleoptera: Coccinel- lidae) is an important predator of rice insect pests; it also Introduction uses rice pollen as a food source under natural condi- tions. In the present study, the effects of KMD1 and The striped stem borer (SSB), Chilo suppressalis KMD2 pollen expressing Cry1Ab protein on the fitness (Walker) (Lepidoptera: Pyralidae), and the yellow stem of P. japonica were assessed in the laboratory. P. borer (YSB), Scirpophaga incertulas (Walker), are two of japonica larvae and adults were provided with the fol- the most serious pests of rice in temperate and sub- lowing four diets: KMD1 pollen with the aphid Myzus tropical Asia (Dale 1994). Over the past decade, several persicae, KMD2 pollen with M. persicae, nontransgenic synthetic genes including cry1Ab, cry1Ac and cry1B Xiushui 11 (parent variety of KMD1 and KMD2) pollen derived from Bacillus thuringiensis Berliner (Bt) have with M. persicae, and M. persicae only (KMD1–pollen, been transferred into indica or japonica rice to confer KMD2–pollen, XS11–pollen, and aphid treatments, resistance to SSB and YSB (Fujimoto et al. 1993;Wu¨ nn respectively). The results showed that the longevity of et al. 1996; Ghareyazie et al. 1997; Nayak et al. 1997; female adults in the KMD1–pollen treatment was sig- Wu et al. 1997; Cheng et al. 1998; Datta et al. 1998; nificantly lower than that in the XS11–pollen treatment, Alam et al. 1999; Breitler et al. 2000; Khanna and Raina but was not significantly different from that in the 2002). In China, the obtained transgenic Bt rice lines KMD2–pollen and aphid treatments. Newly emerged have been proven to be highly resistant to rice stem males in the KMD2–pollen treatment were evidently less borers (including SSB and YSB) and foliage-feeding le- vital than those in the XS11–pollen treatment, but not pidopterans under field conditions (Shu et al. 2000;Ye significantly different from those in the KMD1–pollen et al. 2001). and aphid treatments. The development, survival and Adverse effects of Cry1Ab-expressing Bt plants on reproduction indices for the three pollen treatments did arthropod predators may arise as a result of several not differ significantly from one another. In short, Bt factors, including high concentration of Bt protein in toxin expressed in Bt rice pollen had no evident negative pollen (a food source for predators), modifications of the impacts on P. japonica fitness when the pollen was used introduced cry1Ab gene, and expression of Bt protein as a food by this beetle. throughout the plant (Jepson et al. 1994; Pilcher et al. 1997). Thus, potential risk exists for Bt plants to ad- versely affect the fitness of predators. In the case of Bt rice, Bernal et al. (2002) reported that both the mirid Y. Y. Bai Æ M. X. Jiang Æ J. A. Cheng (&) predator Cyrtorhinus lividipennis Reuter and its prey, the Institute of Applied Entomology, Zhejiang University, brown planthopper Nilaparvata lugens Sta˚ l, could be 310029 Hangzhou, P.R. China exposed to Bt toxins from Bt rice, but this exposure E-mail: [email protected] Tel.: +86-571-86971212 might not affect the fitness of C. lividipennis. Laboratory Fax: +86-571-86971212 observation has indicated that Bt rice has no marked effect on the predation capacity of the wolf spider Pirata Y. Y. Bai Plant Protection College, Southwest Agricultural University, subpiraticus (Liu et al. 2003a). In rice fields, Bt rice also 400716 Chongqing, P.R. China has no significant effect on the population dynamics of 124 dominant spider species, or the community of arthropod (KMD2), and from plants of the nontransgenic line, predators (Liu et al. 2002, 2003b). According to Scho- japonica rice cv. Xiushui 11 (XS11, parent variety of enly et al. (2003), however, planting Bt rice appeared to KMD1 and KMD2). Both KMD1 and KMD2 were alter the species richness of predators. homozygous containing a synthetic cry1Ab gene derived Predaceous coccinellids play important roles in nat- from B. thuringiensis. They were transformed by Agro- ural control of pest insects (Obrycki and Kring 1998). bacterium infection (Cheng et al. 1998; Shu et al. 1998). Previous studies demonstrated that Bt crop pollen Expression of the cry1Ab gene is driven by maize expressing Bt proteins, such as Cry1Ab, Cry3A and ubiquitin promoter (Cheng et al. 1998). Cry3Bb1, poses little risk to this group of predators One day before anthesis, inflorescences were cut from (Pilcher et al. 1997; Riddick and Barbosa 1998; Duan plants. In the laboratory, anthers enclosed within glume et al. 2002). However, to clarify conclusively the impact were collected, lyophilized, ground, and sifted through a of Bt plant pollen on predaceous coccinellids, more 1-mm sieve. The obtained anther powder (containing extensive experiments are needed (Schoenly et al. 2003). pollens) was placed in sealed plastic vials and kept at Propylea japonica (Thunberg) (Coleoptera: Coccinel- À20°C until use. The concentration of Cry1Ab toxin in lidae) is a very common and abundant predator in many anther powder was determined using a commercially crop systems throughout China including rice (Yang available enzyme-linked immunosorbent assay (ELISA) 1983; Ma and Liu 1985; Zou et al. 1986; Zhou and Xiang kit (Envirologix). 1987; Cheng 1996). Both larval and adult P. japonica are predaceous, feeding predominantly on aphids (Song et al. 1988). When insect prey is scarce, they also use Effects of Bt rice pollen on preimaginal fitness of P. plant pollen as a supplemental food source (Li et al. japonica 1992). In rice fields, P. japonica preys on the aphid Macrosiphum avenae (F.), young larvae of the rice leaf- Propylea japonica could not complete larval develop- folder Cnaphalocrocis medinalis Guene´e, young nymphs ment solely on rice pollen (personal observation). Thus of N. lugens, and others (Song et al. 1988); it can also feed M. persicae, an optimal food source of P. japonica (Guo on rice pollen during both larval and adult stages (per- and Wan 2001), was supplemented in the three pollen sonal observation). In this study, development, survival, treatments. The experimental treatments were KMD1 and reproduction of P. japonica feeding on Bt rice pollen pollen with aphid, KMD2 pollen with aphid, and XS11 were observed. The objectives were to determine effects pollen with aphid (described hereafter as KMD1–pollen, of Bt rice pollen on the fitness of this beetle, and subse- KMD2–pollen, and XS11–pollen treatments, respec- quently to broaden our knowledge about the ecological tively). A control diet of only M. persicae (described risk of transgenic Bt plants pending commercial release. hereafter as aphid treatment) was used to verify that experimental conditions used in this study were suitable for P. japonica. A total of 200 newly hatched P. japonica Materials and methods larvae from 20 female sources were used, with 50 larvae being subjected to each treatment. In addition, to Propylea japonica determine average percentage of larvae that pupated and percentage of pupae that eclosed, the larvae in each Propylea japonica adults were collected from rice plants treatment were divided into three subgroups. during the flowering stage on the experimental farm of Larvae were reared individually in glass tubes (1.4 cm Zhejiang University during August 2003. Pairs were diameter, 10 cm long). In the aphid treatment, 10, 20, 40 placed in glass tubes (1.4 cm diameter, 10 cm long) and 60 M. persicae adults per day were provided to each containing the green peach aphid, Myzus persicae (Sul- larva during the first, second, third and fourth instars, zer), and maintained in a climatically controlled cham- respectively. In the pollen treatments, each larva was ber with photoperiod 16:8 h (L:D), 28±1 C, and 60– ° given 20 anthers together with 5, 10, 20 and 30 M. 80% RH. M. persicae was supplied daily to the tubes. As persicae adults per day during the first, second, third and egg deposition occurred, adults were transferred to other fourth instars, respectively. To increase the probability clear glass tubes, and the tubes bearing eggs were that P. japonica would feed on pollen, aphids were not maintained until egg hatch. The newly hatched larvae supplied during the first 12 h of each instar. were subjected to experiments. A water-saturated cotton The experiment was conducted in the climatically ball was placed in each glass tube to maintain moisture. controlled chamber described earlier. Water was pro- The M. persicae had been raised on Brassica oleracea vided to larvae by placing a water-saturated cotton ball var. capitata L. in the climatically controlled chamber. in each tube. Anthers in tubes were refreshed twice daily. Larvae were checked every 3 h for ecdysis and mortality; Rice pollen development time and survival rate of each preimaginal stage were determined. Weight of pupae and adults was Pollen was obtained from field-grown plants of the Bt measured approximately 12 h after pupation and within rice lines Kemingdao 1 (KMD1) and Kemingdao 2 6 h after emergence, respectively. 125 Effects of Bt rice pollen on adult fitness of P. japonica were compared among treatments using the Tukey HSD test at the level P=0.05.