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Range expansion of the invasive cotton mealybug, Phenacoccus solenopsis Tinsley: An increasing threat to agricultural and horticultural crops in China
Journal of Integrative Agriculture 2020, 19(3): 881–885 Available online at www.sciencedirect.com
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Range expansion of the invasive cotton mealybug, Phenacoccus solenopsis Tinsley: An increasing threat to agricultural and horticultural crops in China WANG Yu-sheng1, DAI Tian-mei2, TIAN Hu3, WAN Fang-hao1, 4, ZHANG Gui-fen1, 4 1
State Key Laboratory for Biology of Plant Diseases and Insect Pests/Key Laboratory of Integrated Pest Management of Crop, Ministry of Agriculture and Rural Affairs/Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing 100193, P.R.China 2 Hunan Provincial Key Laboratory for Control of Forest Diseases and Pests, College of Forestry, Central South University of Forestry and Technology, Changsha 410004, P.R.China 3 Caofeidian Customs House, Tangshan 063210, P.R.China 4 Center for Management of Invasive Alien Species, Ministry of Agriculture and Rural Affairs, Beijing 100193, P.R.China
Abstract The globally invasive cotton mealybug Phenacoccus solenopsis Tinsley, has recently invaded several Chinese regions, and continues to expand its range. This mealybug is a polyphagous insect pest, with at least 200 host plants from 63 families, including cotton, food crops, fruits, ornamental plants, tobacco, and vegetables. Here, we describe the first finding of P. solenopsis in Shandong Province, and investigate the abundances of its natural enemies (predator Coccinella septempunctata L. and parasitoid Aenasius bambawalei Hayat). All three species were detected from ornamental and weed species in Linyi, Shandong, in September 2018, and were positively identified using DNA barcoding. BLAST analysis revealed significant identity (99.38–100%) between sequences of P. solenopsis obtained in this study and those published in the past. This invasive pest represents a major potential threat to agri-horticulture in Shandong, which is a key province of China for production and export of many vegetables, flowers, fruits, and other crops. This mealybug species has a wide range of potential distribution in Shandong and is easily dispersed with agricultural and horticultural transport products. Further monitoring and management strategies are required to limit the spread of this pest species. Keywords: Aenasius bambawalei, Coccinella septempunctata, field investigation, invasive insect pest, molecular identification, Phenacoccus solenopsis, rapid spreading
1. Introduction Received 22 April, 2019 Accepted 17 June, 2019 WANG Yu-sheng, E-mail: [email protected]; Correspondence ZHANG Gui-fen, Tel: +86-10-82109572, E-mail: [email protected] © 2020 CAAS. Published by Elsevier Ltd. This is an open access article under the CC BY-NC-ND license (http:// creativecommons.org/licenses/by-nc-nd/4.0/). doi: 10.1016/S2095-3119(19)62765-6
The cotton mealybug, Phenacoccus solenopsis Tinsley (Hemiptera: Pseudococcidae), is a cosmopolitan insect pest that damages over 200 host plant species from 63 families (ScaleNet 2016), and inflicts significant damage on coffee, cotton, food crops, fruits, medicinal plants, oil crops, ornamental plants, tobacco, and vegetables (Fand and
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Suroshe 2015; ScaleNet 2016; Tong et al. 2019a). It can feed on any aboveground part of the hosts and may cause damage to the hosts ranging from wilting to death (Hodgson et al. 2008). The concealed manner and strong resistance to adverse environmental conditions of P. solenopsis allow it to survive on harvested host plants (CABI 2018) and spread worldwide via intra- and inter-national transportation of agri-horticultural products. Moreover, this mealybug species has a high reproductive capacity (Tong et al. 2019b), and thus could easily cause an outbreak after invading new areas. Phenacoccus solenopsis is native to North America, and has spread to more than 46 countries/ regions worldwide (ScaleNet 2016), causing serious economic losses and ecological damage (Hodgson et al. 2008; Fand and Suroshe 2015). Phenacoccus solenopsis was first detected in the Chinese Mainland in 2008 in Guangdong (Ma et al. 2009) and has since invaded areas of the other 15 provinces (MOA 2017; MOARA 2018). It is included in the list of imported plant quarantine pests in China (MOA and GAQSIQ 2009) and the national quarantine pests of agricultural and forestry plants (MOA and SFA 2010), and is one of the 52 key invasive species to be managed with priority in China. Moreover, this mealybug has spread northward to eastern China in recent years. Shandong Province, a major producer of vegetables, ornamentals, cotton, peanut, and tobacco, was assessed to be a suitable region for cotton mealybug colonization (Fan 2018). Although this mealybug had not been detected previously in Shandong, its neighboring provinces, including Hebei (the most northern area in the geographic range of the mealybug so far reported in eastern China), Anhui, and Jiangsu, have been invaded. Because of this, it is essential to monitor this mealybug in Shandong Province. This study investigated the occurrence of P. solenopsis and its damage on roadside ornamental and weed plants in Linyi, Shandong, China, during a field survey in September 2018. The mealybug was identified based on morphological keys (Hodgson et al. 2008) and a DNA barcoding technique.
The natural enemy species coexisting with the cotton mealybug were also investigated.
2. Materials and methods During field investigation (including agricultural fields, garden fields, and green spaces) in September 2018, P. solenopsis was detected on roadside ornamental and weed plants in Linyi, Shandong, and located within an area of ca. 1.5 km (Table 1). We also investigated the presence of natural enemies, including the predatory ladybird beetle (Coccinella septempunctata L.; larval stage) and a parasitoid wasp (Aenasius bambawalei Hayat (synonymized with Aenasius arizonensis (Girault)). To calculate the percent of infested plants and population density of P. solenopsis and its natural enemies, we examined three sample points (about 1 m2 per sample point) randomly in the field planted with ornamental (about 20 plants m–2) and weed (about 1–3 plants m–2) plants (Table 1, site 1), and all plants in pots (about 30 plants) (Table 1, site 2) and beds (Table 1, site 3) with flowers. The following formulas were then used: Infested plants (%)=(No. of infested plants/Total no. of examined plants)×100 Population density=Sum (No. of cotton mealybugs or ladybird beetles/Plant)/Total no. of examined plants Parasitized cotton mealybugs (%)=(No. of parasitized mealybug individuals/Total no. of examined mealybug individuals)×100 IBM SPSS Statistics version 19.0.0 (SPSS Inc, Chicago, IL, USA) was used to calculate the mean percentage or population density in each site. Species were identified based on morphological characteristics (Tian et al. 1982; Hodgson et al. 2008; Chen et al. 2010) and a DNA barcoding technique. Two P. solenopsis nymphs and three female adults from each of six host plants (Table 1) were extracted individually for genomic DNA with DNeasy Blood & Tissue Kit (Qiagen,
Table 1 Location, percentage of infestation and population density of Phenacoccus solenopsis per sampled host plant in the present study Site 1
2 3
Infested plants by No. of P. solenopsis P. solenopsis (%) per plant (mean±SE) (mean±SE) Feicheng Town, Feixian, Linyi Portulaca grandiflora Hook. Ornamental plant 80.0±5.8 15.2±2.1 (35°16´10.29´´N, 117°58´19.14´´E) Euonymus japonicus Thunb. Ornamental plant 25.0±7.6 6.2±0.7 Achyranthes aspera L. Weed 40.0±20.0 15.0±7.6 Kochia scoparia (L.) Schrad. Weed 26.7±6.7 7.7±1.5 Feicheng Street Office, Feixian, Linyi Portulaca pilosa L. Ornamental plant 100 8.9±2.3 (35°16´39.72´´N, 117°58´27.08´´E) Feicheng Town, Feixian, Linyi Dahlia pinnata Cav. Ornamental plant 100 15.7±5.2 (35°16´13.14´´N, 117°58´43.64´´E) Location
Host plant
Plant classification
WANG Yu-sheng et al. Journal of Integrative Agriculture 2020, 19(3): 881–885
Duesseldorf, Germany). The mtDNA COI gene was amplified and sequenced (Park et al. 2011). Sequence alignment and haplotype analyses were conducted using MEGA5.22 (Tamura et al. 2011) and DnaSP5.10.01 (Librado and Rozas 2009), respectively. A BLAST search was performed to confirm species identity.
3. Results 3.1. Phenacoccus solenopsis occurrence, density, and damage This study revealed the occurrence of P. solenopsis in three roadside green spaces (about 0.01 ha in total) in Linyi. The host plants of this mealybug were ornamental plants, including Portulaca grandiflora Hook., Portulaca pilosa L., Dahlia pinnata Cav., and Euonymus japonicus Thunb.; and weeds, including Achyranthes aspera L. and Kochia scoparia (L.) Schrad. This mealybug caused serious damage to the ornamental plants, especially to P. grandiflora, P. pilosa, and D. pinnata. All plants of P. pilosa and D. pinnata and about 80% of P. grandiflora plants were infested by P. solenopsis. The population density of this mealybug in those ornamental plants varied between 8.9 mealybugs per plant in P. pilosa to 15.7 in D. pinnata (Table 1). Phenacoccus solenopsis preferentially fed on young tissues, especially tender leaves, petioles, flower buds, and stems of the host plants.
3.2. Natural enemy species We found two natural enemy species of P. solenopsis, including the predatory ladybird beetle C. septempunctata and the parasitoid wasp A. bambawalei in the field. Both species were verified using DNA barcoding. The ladybird beetle preyed on the P. solenopsis collected from the host plant P. grandiflora and achieved population densities of 2.3 individuals m–2. Aenasius bambawalei parasitized P. solenopsis on P. pilosa, with a natural parasitism rate of about 4.4%.
3.3. Molecular identification of Phenacoccus solenopsis The P. solenopsis sequences from the six host plants resulted in a 649-bp fragment that was analyzed for identification. Only one haplotype (accession MK164397) was found in all of the tested samples. The BLAST analysis revealed significant identity (99.38–100%) between the sequences generated from samples in Shandong and those of P. solenopsis in GenBank, and <95.22% identity with other mealybug species.
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4. Discussion Phenacoccus solenopsis is one of the most pernicious invaders in China. We reported the occurrence of P. solenopsis for the first time in Shandong, a major source and exporter of vegetables, flowers, fruits, and other crops (Yao 2018). This mealybug can rapidly disperse to new areas due to its capacity of using a wide range of host plants (ScaleNet 2016) and high reproduction (Tong et al. 2019b). Shandong is particularly susceptible due to the presence of developed agricultural facilities that could facilitate the epidemic and further spreading of P. solenopsis (Fan 2018). In this study, P. solenopsis was detected on ornamental plants and weeds in a small section of roadside green space, not in agricultural fields or the other areas investigated. However, the occurrence site is located in a main transportation route, near the train station, expressway, and a shopping center, which make dispersal to other areas easier and faster. Additionally, the site is approximately 10 km from farmland and a vegetable-planting base, including greenhouses and open fields, and 35 km from a flower wholesale market. These nearby resources all but ensure that this population would have adequate host plants and suitable places to survive in adverse environmental conditions, such as the cold winter, although further investigation should be conducted. Moreover, Linyi is the freight transportation center of China. This could facilitate incidental transport of the mealybug over long distances via the import-and-export of plant materials, with the potential to affect agricultural, forestry, and horticultural production across multiple provinces of China. Phenacoccus solenopsis has been reported from many host plants of economic importance. In India, this mealybug caused 30–60% cotton yield losses (Nagrare et al. 2009). Additionally, heavy infestation of P. solenopsis on okra Abelmoschus esculentus (L.) Moench in India resulted in a 90% loss of seeds (Sharma 2007). Shandong is the major producing region for cotton and vegetables in China with 465 200 ha cotton (second to Xinjiang) and 1 888 600 ha of vegetable crops (Gao et al. 2017; Xiao and Yu 2018). Vegetables, exported to other Chinese regions and globally (more than 170 countries and regions), contributed US$ 30.9 billion annually which accounts for 43.45% of the total agricultural output value of Shandong Province (Gao et al. 2017). Furthermore, Shandong is a hub for planting, sale, and distribution of flowers in China (Gao et al. 2016). In China, ornamental plants are the major hosts of P. solenopsis, constituting 34.5% (57 vs. 166 species) of its total host species (Tong et al. 2019a) and infested severely and continuously year round (Vennila et al. 2014). The occurrence of an established population of P. solenopsis in
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Shandong requires ongoing monitoring and management to mitigate the potential diffusion into these industries. Biological control with natural enemies is essential for suppressing P. solenopsis and reducing damage to crops (Ahmad et al. 2011). So far, there are 53 known natural enemies of P. solenopsis (Tong et al. 2019a). In this study, a predatory ladybird beetle C. septempunctata and a parasitoid wasp A. bambawalei were detected and confirmed with DNA barcoding. Aenasius bambawalei, a solitary endoparasitoid, shows a 30–60% natural parasitism rate against P. solenopsis in fields (Tanwar et al. 2008); this parasitoid should be especially effective because of its simultaneous movement with P. solenopsis (Ahmed et al. 2015). Moreover, C. septempunctata, a cosmopolitan species, could be another effective natural control agent against P. solenopsis (Shera et al. 2010). Although the densities of natural enemies at the initial invasion front are relatively low, they are likely to increase over time. Implementation of biological control for management of P. solenopsis in newly invaded areas deserves further investigation.
5. Conclusion This study described the first recorded observation of the invasive cotton mealybug P. solenopsis and its parasitoid and predatory natural enemies in Shandong, China. This invasive insect has the potential to invade large areas of Shandong and can be easily transported with agrihorticultural products. Thus, its establishment and spread could represent a severe threat to agri-horticultural industries nationwide. Further monitoring (exact spatiotemporal distribution, population dynamics, and host plants) and effective management (especially using biocontrol agents) are required to limit the spread of this pest species.
Acknowledgements This work was supported by the National Key Research and Development Program of China (2017YFC1200600 and 2016YFC1201200) and the Science and Technology Innovation Program of the Chinese Academy of Agricultural Sciences (caascx-2017-2022-IAS).
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using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution, 28, 2731–2739. Tanwar R K, Bhamare V K, Ramamurthy V V, Hayat M, Jeyakumar P, Singh A, Bambawale O M. 2008. Record of new parasitoid on mealy bug, Phenacoccus solenopsis. Indian Journal of Entomology, 70, 404–405. Tian L X, Qi L Z, Qiu H, Shao Z R. 1982. A preliminary study on the common Coccinellid larvae of Jiangsu Province. Journal of Nanjing Agricultural College, 3, 39–55. (in Chinese) Tong H J, Ao Y, Li Z H, Wang Y, Jiang M X. 2019a. Invasion biology of the cotton mealybug, Phenacoccus solenopsis Tinsley: Current knowledge and future directions. Journal of Integrative Agriculture, 18, 758–770. Tong H J, Li Z H, Ye W Y, Wang Y, Omar M A A, Ao Y, Li F, Jiang M X. 2019b. Male mating and female post mating performances in cotton mealybug (Hemiptera: Pseudococcidae): Effects of female density. Journal of Economic Entomology, 112, 1145–1150. Vennila S, Agarwal M, Nagrare V S, Prasad Y G, Prabhakar M. 2014. Ornamental hosts of cotton mealybug (Phenacoccus solenopsis). Indian Journal of Agricultural Sciences, 84, 161–163. Xiao H F, Yu Y X. 2018. Layout of cotton production and its comparative advantage in China. Agricultural Economics and Management, 50, 38–47. (in Chinese) Yao Y. 2018. An Empirical Study on the Influencing Factors of Agricultural Export in Shandong Province. MSc thesis, Shandong University, Jinan, China. (in Chinese)
Executive Editor-in-Chief WAN Fang-hao Managing editor SUN Lu-juan
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Range expansion of the invasive cotton mealybug, Phenacoccus solenopsis Tinsley: An increasing threat to agricultural and horticultural crops in China WANG Yu-sheng1, DAI Tian-mei2, TIAN Hu3, WAN Fang-hao1, 4, ZHANG Gui-fen1, 4 1
State Key Laboratory for Biology of Plant Diseases and Insect Pests/Key Laboratory of Integrated Pest Management of Crop, Ministry of Agriculture and Rural Affairs/Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing 100193, P.R.China 2 Hunan Provincial Key Laboratory for Control of Forest Diseases and Pests, College of Forestry, Central South University of Forestry and Technology, Changsha 410004, P.R.China 3 Caofeidian Customs House, Tangshan 063210, P.R.China 4 Center for Management of Invasive Alien Species, Ministry of Agriculture and Rural Affairs, Beijing 100193, P.R.China
Abstract The globally invasive cotton mealybug Phenacoccus solenopsis Tinsley, has recently invaded several Chinese regions, and continues to expand its range. This mealybug is a polyphagous insect pest, with at least 200 host plants from 63 families, including cotton, food crops, fruits, ornamental plants, tobacco, and vegetables. Here, we describe the first finding of P. solenopsis in Shandong Province, and investigate the abundances of its natural enemies (predator Coccinella septempunctata L. and parasitoid Aenasius bambawalei Hayat). All three species were detected from ornamental and weed species in Linyi, Shandong, in September 2018, and were positively identified using DNA barcoding. BLAST analysis revealed significant identity (99.38–100%) between sequences of P. solenopsis obtained in this study and those published in the past. This invasive pest represents a major potential threat to agri-horticulture in Shandong, which is a key province of China for production and export of many vegetables, flowers, fruits, and other crops. This mealybug species has a wide range of potential distribution in Shandong and is easily dispersed with agricultural and horticultural transport products. Further monitoring and management strategies are required to limit the spread of this pest species. Keywords: Aenasius bambawalei, Coccinella septempunctata, field investigation, invasive insect pest, molecular identification, Phenacoccus solenopsis, rapid spreading
1. Introduction Received 22 April, 2019 Accepted 17 June, 2019 WANG Yu-sheng, E-mail: [email protected]; Correspondence ZHANG Gui-fen, Tel: +86-10-82109572, E-mail: [email protected] © 2020 CAAS. Published by Elsevier Ltd. This is an open access article under the CC BY-NC-ND license (http:// creativecommons.org/licenses/by-nc-nd/4.0/). doi: 10.1016/S2095-3119(19)62765-6
The cotton mealybug, Phenacoccus solenopsis Tinsley (Hemiptera: Pseudococcidae), is a cosmopolitan insect pest that damages over 200 host plant species from 63 families (ScaleNet 2016), and inflicts significant damage on coffee, cotton, food crops, fruits, medicinal plants, oil crops, ornamental plants, tobacco, and vegetables (Fand and
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Suroshe 2015; ScaleNet 2016; Tong et al. 2019a). It can feed on any aboveground part of the hosts and may cause damage to the hosts ranging from wilting to death (Hodgson et al. 2008). The concealed manner and strong resistance to adverse environmental conditions of P. solenopsis allow it to survive on harvested host plants (CABI 2018) and spread worldwide via intra- and inter-national transportation of agri-horticultural products. Moreover, this mealybug species has a high reproductive capacity (Tong et al. 2019b), and thus could easily cause an outbreak after invading new areas. Phenacoccus solenopsis is native to North America, and has spread to more than 46 countries/ regions worldwide (ScaleNet 2016), causing serious economic losses and ecological damage (Hodgson et al. 2008; Fand and Suroshe 2015). Phenacoccus solenopsis was first detected in the Chinese Mainland in 2008 in Guangdong (Ma et al. 2009) and has since invaded areas of the other 15 provinces (MOA 2017; MOARA 2018). It is included in the list of imported plant quarantine pests in China (MOA and GAQSIQ 2009) and the national quarantine pests of agricultural and forestry plants (MOA and SFA 2010), and is one of the 52 key invasive species to be managed with priority in China. Moreover, this mealybug has spread northward to eastern China in recent years. Shandong Province, a major producer of vegetables, ornamentals, cotton, peanut, and tobacco, was assessed to be a suitable region for cotton mealybug colonization (Fan 2018). Although this mealybug had not been detected previously in Shandong, its neighboring provinces, including Hebei (the most northern area in the geographic range of the mealybug so far reported in eastern China), Anhui, and Jiangsu, have been invaded. Because of this, it is essential to monitor this mealybug in Shandong Province. This study investigated the occurrence of P. solenopsis and its damage on roadside ornamental and weed plants in Linyi, Shandong, China, during a field survey in September 2018. The mealybug was identified based on morphological keys (Hodgson et al. 2008) and a DNA barcoding technique.
The natural enemy species coexisting with the cotton mealybug were also investigated.
2. Materials and methods During field investigation (including agricultural fields, garden fields, and green spaces) in September 2018, P. solenopsis was detected on roadside ornamental and weed plants in Linyi, Shandong, and located within an area of ca. 1.5 km (Table 1). We also investigated the presence of natural enemies, including the predatory ladybird beetle (Coccinella septempunctata L.; larval stage) and a parasitoid wasp (Aenasius bambawalei Hayat (synonymized with Aenasius arizonensis (Girault)). To calculate the percent of infested plants and population density of P. solenopsis and its natural enemies, we examined three sample points (about 1 m2 per sample point) randomly in the field planted with ornamental (about 20 plants m–2) and weed (about 1–3 plants m–2) plants (Table 1, site 1), and all plants in pots (about 30 plants) (Table 1, site 2) and beds (Table 1, site 3) with flowers. The following formulas were then used: Infested plants (%)=(No. of infested plants/Total no. of examined plants)×100 Population density=Sum (No. of cotton mealybugs or ladybird beetles/Plant)/Total no. of examined plants Parasitized cotton mealybugs (%)=(No. of parasitized mealybug individuals/Total no. of examined mealybug individuals)×100 IBM SPSS Statistics version 19.0.0 (SPSS Inc, Chicago, IL, USA) was used to calculate the mean percentage or population density in each site. Species were identified based on morphological characteristics (Tian et al. 1982; Hodgson et al. 2008; Chen et al. 2010) and a DNA barcoding technique. Two P. solenopsis nymphs and three female adults from each of six host plants (Table 1) were extracted individually for genomic DNA with DNeasy Blood & Tissue Kit (Qiagen,
Table 1 Location, percentage of infestation and population density of Phenacoccus solenopsis per sampled host plant in the present study Site 1
2 3
Infested plants by No. of P. solenopsis P. solenopsis (%) per plant (mean±SE) (mean±SE) Feicheng Town, Feixian, Linyi Portulaca grandiflora Hook. Ornamental plant 80.0±5.8 15.2±2.1 (35°16´10.29´´N, 117°58´19.14´´E) Euonymus japonicus Thunb. Ornamental plant 25.0±7.6 6.2±0.7 Achyranthes aspera L. Weed 40.0±20.0 15.0±7.6 Kochia scoparia (L.) Schrad. Weed 26.7±6.7 7.7±1.5 Feicheng Street Office, Feixian, Linyi Portulaca pilosa L. Ornamental plant 100 8.9±2.3 (35°16´39.72´´N, 117°58´27.08´´E) Feicheng Town, Feixian, Linyi Dahlia pinnata Cav. Ornamental plant 100 15.7±5.2 (35°16´13.14´´N, 117°58´43.64´´E) Location
Host plant
Plant classification
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Duesseldorf, Germany). The mtDNA COI gene was amplified and sequenced (Park et al. 2011). Sequence alignment and haplotype analyses were conducted using MEGA5.22 (Tamura et al. 2011) and DnaSP5.10.01 (Librado and Rozas 2009), respectively. A BLAST search was performed to confirm species identity.
3. Results 3.1. Phenacoccus solenopsis occurrence, density, and damage This study revealed the occurrence of P. solenopsis in three roadside green spaces (about 0.01 ha in total) in Linyi. The host plants of this mealybug were ornamental plants, including Portulaca grandiflora Hook., Portulaca pilosa L., Dahlia pinnata Cav., and Euonymus japonicus Thunb.; and weeds, including Achyranthes aspera L. and Kochia scoparia (L.) Schrad. This mealybug caused serious damage to the ornamental plants, especially to P. grandiflora, P. pilosa, and D. pinnata. All plants of P. pilosa and D. pinnata and about 80% of P. grandiflora plants were infested by P. solenopsis. The population density of this mealybug in those ornamental plants varied between 8.9 mealybugs per plant in P. pilosa to 15.7 in D. pinnata (Table 1). Phenacoccus solenopsis preferentially fed on young tissues, especially tender leaves, petioles, flower buds, and stems of the host plants.
3.2. Natural enemy species We found two natural enemy species of P. solenopsis, including the predatory ladybird beetle C. septempunctata and the parasitoid wasp A. bambawalei in the field. Both species were verified using DNA barcoding. The ladybird beetle preyed on the P. solenopsis collected from the host plant P. grandiflora and achieved population densities of 2.3 individuals m–2. Aenasius bambawalei parasitized P. solenopsis on P. pilosa, with a natural parasitism rate of about 4.4%.
3.3. Molecular identification of Phenacoccus solenopsis The P. solenopsis sequences from the six host plants resulted in a 649-bp fragment that was analyzed for identification. Only one haplotype (accession MK164397) was found in all of the tested samples. The BLAST analysis revealed significant identity (99.38–100%) between the sequences generated from samples in Shandong and those of P. solenopsis in GenBank, and <95.22% identity with other mealybug species.
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4. Discussion Phenacoccus solenopsis is one of the most pernicious invaders in China. We reported the occurrence of P. solenopsis for the first time in Shandong, a major source and exporter of vegetables, flowers, fruits, and other crops (Yao 2018). This mealybug can rapidly disperse to new areas due to its capacity of using a wide range of host plants (ScaleNet 2016) and high reproduction (Tong et al. 2019b). Shandong is particularly susceptible due to the presence of developed agricultural facilities that could facilitate the epidemic and further spreading of P. solenopsis (Fan 2018). In this study, P. solenopsis was detected on ornamental plants and weeds in a small section of roadside green space, not in agricultural fields or the other areas investigated. However, the occurrence site is located in a main transportation route, near the train station, expressway, and a shopping center, which make dispersal to other areas easier and faster. Additionally, the site is approximately 10 km from farmland and a vegetable-planting base, including greenhouses and open fields, and 35 km from a flower wholesale market. These nearby resources all but ensure that this population would have adequate host plants and suitable places to survive in adverse environmental conditions, such as the cold winter, although further investigation should be conducted. Moreover, Linyi is the freight transportation center of China. This could facilitate incidental transport of the mealybug over long distances via the import-and-export of plant materials, with the potential to affect agricultural, forestry, and horticultural production across multiple provinces of China. Phenacoccus solenopsis has been reported from many host plants of economic importance. In India, this mealybug caused 30–60% cotton yield losses (Nagrare et al. 2009). Additionally, heavy infestation of P. solenopsis on okra Abelmoschus esculentus (L.) Moench in India resulted in a 90% loss of seeds (Sharma 2007). Shandong is the major producing region for cotton and vegetables in China with 465 200 ha cotton (second to Xinjiang) and 1 888 600 ha of vegetable crops (Gao et al. 2017; Xiao and Yu 2018). Vegetables, exported to other Chinese regions and globally (more than 170 countries and regions), contributed US$ 30.9 billion annually which accounts for 43.45% of the total agricultural output value of Shandong Province (Gao et al. 2017). Furthermore, Shandong is a hub for planting, sale, and distribution of flowers in China (Gao et al. 2016). In China, ornamental plants are the major hosts of P. solenopsis, constituting 34.5% (57 vs. 166 species) of its total host species (Tong et al. 2019a) and infested severely and continuously year round (Vennila et al. 2014). The occurrence of an established population of P. solenopsis in
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Shandong requires ongoing monitoring and management to mitigate the potential diffusion into these industries. Biological control with natural enemies is essential for suppressing P. solenopsis and reducing damage to crops (Ahmad et al. 2011). So far, there are 53 known natural enemies of P. solenopsis (Tong et al. 2019a). In this study, a predatory ladybird beetle C. septempunctata and a parasitoid wasp A. bambawalei were detected and confirmed with DNA barcoding. Aenasius bambawalei, a solitary endoparasitoid, shows a 30–60% natural parasitism rate against P. solenopsis in fields (Tanwar et al. 2008); this parasitoid should be especially effective because of its simultaneous movement with P. solenopsis (Ahmed et al. 2015). Moreover, C. septempunctata, a cosmopolitan species, could be another effective natural control agent against P. solenopsis (Shera et al. 2010). Although the densities of natural enemies at the initial invasion front are relatively low, they are likely to increase over time. Implementation of biological control for management of P. solenopsis in newly invaded areas deserves further investigation.
5. Conclusion This study described the first recorded observation of the invasive cotton mealybug P. solenopsis and its parasitoid and predatory natural enemies in Shandong, China. This invasive insect has the potential to invade large areas of Shandong and can be easily transported with agrihorticultural products. Thus, its establishment and spread could represent a severe threat to agri-horticultural industries nationwide. Further monitoring (exact spatiotemporal distribution, population dynamics, and host plants) and effective management (especially using biocontrol agents) are required to limit the spread of this pest species.
Acknowledgements This work was supported by the National Key Research and Development Program of China (2017YFC1200600 and 2016YFC1201200) and the Science and Technology Innovation Program of the Chinese Academy of Agricultural Sciences (caascx-2017-2022-IAS).
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