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1 September 2013 Sudden Widespread Distribution of Frankliniella occidentalis (Thysanoptera: Thripidae) in Shandong Province, China
Hui-Sheng Duan, Yi Yu, An-Sheng Zhang, Dong Guo, Yu-Li Tao, Dong Chu
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In Shandong Province, China, the western flower thrips, Frankliniella occidentalis (Pergande) (Thysanoptera: Thripidae), was first detected in Qingdao in 2007. The pest is composed of 2 genetic strains or types based on analyses of the mitochondrial DNA gene, mtCOI. These are known as “the Greenhouse strain” and “the Lupin strain”, hereafter referred to as “WFTG” and “WFT-L”, respectively. To investigate the status and pathways of spread of this alien species in its new environment, we collected 78 samples of thrips from various plants in all of the 17 counties of Shandong Province during May–Jul, 2011. In total we made 16 collections of western flower thrips in 12 counties, and we analyzed the mtCOI gene of each of these samples. Most individuals (98.6%) in these 16 collections belonged to the WFT-G type and 3 (1.4%) belonged to WFT-L type. The results demonstrated that F. occidentalis has—without being noticed—become widespread in Shandong Province, and the main type is WFT-G. Field surveys coupled with genetic analyses proved to be helpful in revealing the invasion process including the invasion pathways or mechanisms, and such analyses may help in identifying approaches and options for prevention and management of the pest.

The western flower thrips, Frankliniella occidentalis (Pergande) (Thysanoptera: Thripidae), an important agricultural pest, severely damages ornamentals and vegetables directly by feeding and indirectly by transmitting viruses, and thus causes devastating losses of yield and/or market value (Jones et al. 2005). Frankliniella occidentalis is native to the western North America, where it has caused heavy damage to the ornamental industry as early as the 1940s (Bailey 1940). Since the late 1970s, international agricultural trade flows have increased very rapidly, and F. occidentalis has arrived and established in many countries to become a cosmopolitan pest. Presently, this thrips is established in more than 60 countries including the United States, Canada, Australia, United Kingdom, and Japan (Kirk & Terry 2003).

Recent research (Brunner & Frey 2010; Rugman-Jones et al. 2010) revealed that F. occidentalis could be divided into 2 genetic entities or strains based on phylogenetic analyses using mitochondrial cytochrome oxidase I (mtCOI) gene sequences. These 2 genetic entities (also known as “Greenhouse strain” and “Lupin strain”, thereafter referred to as “WFT-G” and “WFT-L” in this study, respectively) have been regarded as 2 ecotypes (Brunner et al. 2010) or cryptic species (Rugman-Jones et al. 2010). Prior studies showed that WFT-G or WFT-L type might differ in many biological traits including the fecundity, host adaptability, environmental adaptability, and insecticide resistance (de Kogel et al. 1997; Brødsgaard 1994; Brunner et al. 2010; Rugman-Jones et al. 2010). Unfortunately it seems that Rugman-Jones et al. (2010) gave the wrong primer sequences needed for the separation of the strains/haplotypes. Nevertheless many mitochondrial haplotypes of these 2 strains have been found in countries where the pest has become established (Brunner & Frey 2010; Rugman-Jones et al. 2010).

In China, F. occidentalis was first detected in Beijing in 2003 (Zhang et al. 2003) and in Shandong Province it was first detected in Qingdao in 2007 (Zheng et al. 2007). Indeed Rugman-Jones et al. (2010) showed that both the WFTG and the WFT-L type of F. occidentalis have been detected in China. However, the spread status of the pest in Shandong Province during the past several years was unknown (Yang et al. 2012). In addition, we still do not know the type composition (WFT-G and WFT-L) of the pest in the region, which is closely associated with the management measures of the pest because of possible differences in their biological traits (de Kogel et al. 1997; Brødsgaard 1994; Brunner & Frey 2010; Rugman-Jones et al. 2010). We hypothesize that F. occidentalis might spread to a few of the counties neighboring Qingdao, because this pest has been established only for a few years.

In this study, the geographical distribution of F. occidentalis in Shandong Province was systematically established for the first time since it was first detected in the Province in 2007. We first collected the samples of thrips from various host plants from a total of 17 counties in Shandong Province during May–Jul 2011. Then the mtCOI gene of each of the samples was sequenced and analyzed to determine the distribution of this thrips and the type composition of the samples. We posited that the field survey would not only be helpful in revealing the invasion process and the invasion mechanism of this adventive alien species, but also in the prevention and management of the pest.


Collection of Frankliniella occidentalis Samples

Seventy-eight thrips collections were sampled from various plant species in the field and greenhouse from the 17 counties of Shandong Province during May–Jul 2011. The adult thrips were collected in a tube with 95% ethanol and stored at -20 °C. The thrips specimens were first identified by dissecting microscope based on their morphological characteristics such as the number, size and location of the major setae on the head, prothorax and coloration characteristics (Funderburk et al. 2007). The information on sampling locations and sampling dates, and plants from which the thrips specimens were collected of each of the 16 populations are listed in Table 1.

DNA Extraction, PCR Amplification, and Sequencing

Genomic DNA was extracted from individual female adults as described in Frohlich et al. (1999) with a little modification. Essentially the procedure was as follows. One individual was put into a 0.2 mL centrifuge tube with 60 µL lysis buffer (50 mmol-L Tris-HCl (pH8.0), 20 mmol·L-1 NaCl, 1 mmol·L-1 EDTA, 1% SDS) and was ground thoroughly. This preparation was incubated at 65 °C for 15 min and then at 95 °C for 10 min. This lysis was used as the DNA template in PCR amplication. A fragment of the mtCOI gene was amplified via standard PCR using the primers C1-J-1751 (5′-GGATCACCTGATATAGCATTCCC-3′) and C1-N-2329 (5′-ACTGTAAATATATGATGAGCTCA-3′) under the PCR conditions described in Simon et al. (1994).

Haplotype Determination and Phylogenetic Analyses

Sequences were aligned with Clustal X (Thompson et al. 1997) and trimmed manually in MEGA5 (Tamura et al. 2011). All mtCOI sequences were checked for gaps, indels, numts, and pseudogenes by alignment using the multiple sequence editor Clustal X (Thompson et al. 1997). The mtCOI haplotypes were selected from all 225 mtCOI sequences in the present study and deposited in GenBank using DnaSP4.0 software (Librado et al. 2009). A phylogenetic tree was constructed using the neighbour-joining (NJ) or the minimum evolution (ME) method in MEGA5 with the Scirtothrips dorsalis (Hood) mtCOI sequence (GenBank No. GU570440) as an outgroup. The type of the haplotypes was determined based on the phylogenetic tree. The determination of the type (WFT-G or WFT-L) of each specimen was based on the diagnostic method of Rugman-Jones et al. (2010).





Geographical Distribution of Frankliniella occidentalis

The 78 thrips collections in the 17 counties of Shandong Province (Fig. 1), included 16 F. occidentalis collections in 12 counties (Qingdao, Weihai, Jinan, Dezhou, Zibo, Binzhou, Jining, Dongying, Taian, Heze, Weifang, and Yantai) (Table 1). Among these 16 F. occidentalis collections, 15 were from ornamental plants and only 1 was collected from a vegetable crop.

Haplotype Composition of the Adventive F. occidentalis Populations

A total of 303 mtCOI sequences were retrieved from GenBank that had been deposited before 9-20-2011, and the information is listed in Table 2. A total of 46 haplotypes have been determined through the world. Among them, 22 haplotypes (coded as Hap1–Hap22) are found in WFT-G type and 24 haplotypes (coded as Hap23–Hap46) are found in WFT-L type. In this study, we sequenced 225 mtCOI in the collections from Shandong Province and only 5 haplotypes were found. Among the 5 haplotypes, 4 haplotypes (Hapl-Hap4) belongs to the WFT-G type and 1 haplotype (Hap5) belongs to WFT-L type. Overall 98.9% of the 225 individuals were WFT-G type and others (1.1%) were WFT-L type. Most individuals (98.6%) in the collections from Shandong belonged to WFTG type and 3 individuals (1.4%), one each from Qingdao, Weihai, and Rongcheng belonged to the WFT-L type.

The most widespread haplotypes are Hap1, Hap2, and Hap3. Hap4 was found only in Dongying and Jining counties. Hap5 was found only in the coastal counties of Qingdao and Yantai.


Contrary to our expectation, our study revealed that F. occidentalis suddenly and unnoticed become widespread in many regions of Shandong Province. Currently, we are not sure whether this species was already widespread in 2007. Nevertheless it seems possible that this thrips did spread rapidly within Shandong Province during the past 4 yr, and such rapid spread had been observed in Shandong Province with another invasive species, Bemisia tabaci (Gennadius) biotype Q (Hemiptera: Aleyrodidae) (Chu et al. 2007, 2010). Frankliniella occidentalis was found not only in the counties neighboring Qingdao, but also in counties far from Qingdao, which indicates that this thrips is spread mainly through human activities rather than naturally. Currently, F. occidentalis mainly damages the ornamental plants in this Province. However, the infestation on the pepper crop in Weifang indicates that F. occidentalis may be gradually transferring to various vegetable crop species. Thus, it is essential to conduct additional field surveys of F. occidentalis on vegetable and fruit crops in the future.

Fig. 1.

Distribution of the western flower thrips in 12 of the 17 counties of Shandong Province, and the haplotvpe compositions of the 16 collections of this thrips in these counties. The sizes of the pie diagrams were chosen to fit into their respective counties, and they are not proportional to the number of samples taken.


In Shandong Province, both the WFT-G and WFT-L type of F. occidentalis have been detected in the field samples. However, the present study showed that the main type in this Province was the WFT-G type. There are 2 possibilities to explain the presence of both types or strains in the Province. The first possibility is that both types were represented in the first founder population to arrive. The haplotype composition among the collections indicated that there may have been multiple incursions into Shandong Province by F. occidentalis. Thus, if the initial founder population was mainly composed of WFT-G type, then the advantage of time may have enabled it spread widely and to become the most prevalent or dominant type. Another possibility is that WFT-G may be more invasive or more readily adapt to the environments of Shandong Province than WFT-L. Prior studies on their biological characteristics including fecundity (de Kogel et al. 1997), host adaptability (Rugman-Jones et al. 2010), environmental adaptability (Brunner et al. 2010) and insecticide resistance Brødsgaard 1994) suggested that WFT-G has the biological advantages over WFT-L. Shandong has a warm-temperate monsoonal climate, but its coastal and inland regions experience a sharp differences in weather ( WFT-L was only found in the eastern part of Shandong Province, which has cool-moist conditions. Thus, the WFT-G type might more readily adapt to the hoter and drier climatic conditions of most regions of Shandong Province. The distribution pattern of the 2 types of this thrips is consistent with the finding of Brunner et al. (2010) that WFT-G occurred mainly in the hot-dry conditions of its native range, while the WFT-L is better adapted to cool-moist conditions. The relationship between the geographic distribution pattern in this Province of the 2 types and temperature and humidity should also be explored in the future research.









This work was funded by the Special Fund for Agroscientific Research in the Public Interest (201303028; 200803025), the Science and Technology Development Planning Program of Qingdao (13-1-3-108-nsh), and the Taishan Scholarship Construction Engineering Special Fund. We are grateful to Prof. X. Y. Hong and Dr. X. M. Yang (Nanjing Agricultural University, Nanjing, China) for suggestions concerning a preliminary draft of this manuscript. RES 18



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Hui-Sheng Duan, Yi Yu, An-Sheng Zhang, Dong Guo, Yu-Li Tao, and Dong Chu "Sudden Widespread Distribution of Frankliniella occidentalis (Thysanoptera: Thripidae) in Shandong Province, China," Florida Entomologist 96(3), 933-940, (1 September 2013).
Published: 1 September 2013

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