Review Article |
Corresponding author: Yongyue Lu ( luyongyue@scau.edu.cn ) Academic editor: Jianghua Sun
© 2020 Lei Wang, Ling Zeng, Yijuan Xu, Yongyue Lu.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Wang L, Zeng L, Xu Y, Lu Y (2020) Prevalence and management of Solenopsis invicta in China. NeoBiota 54: 89-124. https://doi.org/10.3897/neobiota.54.38584
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Red imported fire ant, Solenopsis invicta, was first found in Taiwan province of China in 2003. To prevent transboundary expansion, the Chinese government has formulated various control strategies in the last 15 years to slow down the spread of S. invicta. Despite all efforts, S. invicta invasion has reached more than 390 counties of 13 provinces and two special administrative regions in China; at present, S. invicta remains at the stage of rapid expansion. The transnational entry of S. invicta is linked to imported logs and wastepaper coming mostly from the United States. In domestic settings, long-distance expansion of S. invicta relied on potted plant and turf transportation. Both monogyne and polygyne social forms of S. invicta were present in China with polygyne colonies as the dominant one. Data on population and breeding dynamics of S. invicta reveal the presence of two peaks annually with nuptial flights occurring throughout the year. Arthropods, plant seeds, and honeydew are important food sources of S. invicta, thereby causing negative impacts on the abundance, diversity, and richness of native arthropod communities. Fire ants are threats not only to agriculture and power facilities, but also to human health, with more than 30% of people having suffered from the sting and 10% having experienced an allergic reaction. To address the expansion of S. invicta, the National Fire Ant Detection and Management Union was established and the formulation and implementation of management policies were drawn. Plant quarantine becomes an essential step in fire ant management, whereas the two-step method of combing toxic baits and contact dust emerges as the forefront method crucial in managing S. invicta. The experience and lessons learned from fire ant management in China could benefit other countries when facing similar challenges.
Control, fire ant, invasive ant, management policies, quarantine
China suffers huge economic and biodiversity losses from biological invasions. The complex topography, diverse native ecosystems, and increasing international trade of China with other countries provide numerous opportunities for the entry and colonization of invasive species. In fact, more than 750 invasive species were confirmed in China (http://www.chinaias.cn, accessed on 2019-6-5). Among these pests, almost half of the 100 World’s Worst Invasive Alien Species were identified in China, including the notorious pest, the red imported fire ant, Solenopsis invicta. Solenopsis invicta is an ant species native to tropical regions of South America, and its original homeland was thought to be the Pantanal region of Brazil. The S. invicta invasion caused many problems with human health, public safety, agriculture, economy, and ecology around the world (
Solenopsis invicta was introduced to the United States in 1930s and infested more than 320 million acres of land in southern United States (
The emergency response and management against the invasive fire ants have been carried out since S. invicta were found in China. Technical officers from government agencies and entomologists from universities and research institutions were sent to the USA and Australia by the Ministry of Agriculture and Rural Affairs to learn how to deal with the S. invicta invasion. These activities helped Chinese experts realize that prevention and control of S. invicta is long-term work. After comparison and analysis of the situation of S. invicta at home and abroad, the aim of plant quarantine and management of S. invicta became clearer in China. It is impossible to eradicate S. invicta in most infested regions in some provinces and several isolated infested places in China where it has already become established. Here, we review the Chinese experiences in coping with the S. invicta invasion. We also put forward the challenges in managing S. invicta in China by offering suggestions to potentially solve the problem. Our focus is to discuss experiences and reflect on the lessons learned from S. invicta management in the context of potential fire ant invasion in tropical and subtropical countries.
The initial entry of S. invicta was firstly discovered in Taoyuan County and Chiayi County of Taiwan province between September to October 2003, where thorough investigation revealed that 4000 ha land were infested. A decade later, 10 counties with more than 60000 ha land were occupied by S. invicta in Taiwan province (http://www.fireant.tw, accessed on 2019-6-5). In mainland China, S. invicta was first found in Wuchuan, Guangdong province in September 2004, where, at the end of 2014, 12680 ha land were infested (
Distribution of Solenopsis invicta in China in May, 2019. The red areas represent fire ant infested territories at a national level.
Growth dynamics of S. invicta infected counties from 2003 to 2018. The data for infected counties in China quoted from
The origins of populations of S. invicta in China are important in the terms of tracing the source of the species and instigating future preventive measures. Several studies suggested that S. invicta populations in China may have originated from the USA (
The growth in global trade and travel accelerated the spread of S. invicta from one infected region to another (
Solenopsis invicta is a major threat to biodiversity, human health, and public safety in regions where it is introduced (
In China, fire ants invasion has caused a severe reduction of diversity and abundance of arthropods (
Investigation in China showed that S. invicta invasion presented a serious negative impact on the abundance, diversity, and richness of native ants in Litchi chinensis and Dimocarpus longan orchards, lawns, abandoned land, grassland, and residential areas. Ant species richness was reduced by more than 33% in several habitats (
Solenopsis invicta invasion has a negative impact on other arthropods. For example,
Plant seeds are important food sources of S. invicta.
Solenopsis invicta invasion also changes the physical and chemical properties of soil. The organic matter, alkalihydrolysable nitrogen, and available phosphorus decreased over time while the available potassium and soil acidity was raised after fire ant infestation in an orchard of L. chinensis (
Using the plant seeds preference test,
Although we did not get any authoritative data to show how much losses were attributed to S. invicta invasion in Chinese agriculture, a loss assessment in Fujian province showed that S. invicta has caused 744.70 Yuan/ha direct loss and 2756.48 Yuan/ha indirect loss in its agriculture sector (
Solenopsis invicta is an aggressive species that may attack people upon contact. Humans who suffer from the sting of S. invicta can experience itchiness and redness, and most of the time, a white pimple may appear several hours after the sting (Fig.
The typical symptom after Solenopsis invicta sting. A white pimple will appear in the place S. invicta sting several hours later (photo by Lei Wang).
In China, researchers found fire ant mounds in power facilities and transformer stations (
Dikes and dams are among the places with S. invicta mounds. An investigation in 2013 showed that 28 of 64 dikes and dams were infected by S. invicta in Guangdong province (
Solenopsis invicta workers attack a cable box (photo provided by Guangzhou Metro Group Co., Ltd).
The creation of a suitable strategy for management of S. invicta would depend on the deep understanding of its biology and ecology and must be tailored to the regions where the invasive species is newly introduced. In China, many research institutions have focused their work on fire ant biology and ecology since the first reports of the S. invicta invasion.
Solenopsis invicta has two social forms, monogyne (having a single queen within a colony) and polygyne (having multiple queens within a colony), which both possess several distinct differences in terms of biology and dispersal abilities (
Previous studies have shown that the population and breeding dynamics of S. invicta consist of two peaks in a year, i.e., spring and autumn (
Honeydew is an important food resource of S. invicta (
The main chemical components of S. invicta venom are 2-methyl-6-alkyl or alkenylpiperidines (
Aggressiveness is a very important weapon of fire ants in food competition and territory defense in the introduced regions. The aggressive activity of S. invicta can be affected by mound size, colony structure, habitat, temperature, humidity, degree of disturbance, and the use of pesticides (
Resistance to adversity is an important trait for successful adaption of the invasive species in a particular region.
Necrophoric behavior is an important behavior aspect of S. invicta to avoid horizontal transmission of pathogens in the colony.
Understanding the mechanisms of insecticide metabolism will provide a theoretical basis for the rational usage of insecticides in controlling S. invicta. Research has shown that larvae and pupae were less sensitive to insecticides than adults (
Strong leadership, good organization, and coordination skills provide a guarantee on preventing S. invicta invasion. Specific research institutions are needed for strong scientific and technological support in combatting the spread of this species. For example, the Animal and Plant Health Inspection Service (APHIS) of the United States Department of Agriculture (
Several attempts were also made in China to make further exploration in this field. In Taiwan province, the Fire Ant Control Organization was established through multi-agency cooperation involving universities and government agencies of agriculture, environmental protection, health, education, economy, and traffic. The functions of the organization included the collaborative work of various agencies, creation of control plans and strategies, funds allocation, research, fire ant management, and the holding of meetings. In mainland China, specific organizations and research institutions were also established for fire ant management. The provincial government of every infected province established a leading group for fire ant control. The Red Imported Fire Ant Research Center of South China Agricultural University was established to provide scientific and technological support and counseling and services on fire ant management for the government, enterprises, and the public. The National Fire Ant Detection and Management Union was founded by the Ministry of Agriculture and Rural Affairs in September 2006, and the union was comprised of provincial plant quarantine agencies of Guangdong, Guangxi, Hunan, Fujian, Hainan, and research institutions, including Institute of Zoology, Chinese Academy of Science, and South China Agricultural University, among others. The aim and missions of the union are to provide guidelines for fire ant management, control training, detection, specimen identification, etc. The National Fire Ant Detection and Management Union gives strong technical support to the government to cope with the fire ant invasion, holds management training meetings for the public which teach ways to appropriately deal with fire ants.
In countries infested with S. invicta, such as the United States and Australia, there are strict quarantine regulations drawn up for pest control and management (https://www.aphis.usda.gov/aphis/ourfocus/planthealth/plant-pest-and-disease-programs/pests-and-diseases/imported-fire-ants, accessed on 2019-6-5; https://www.daf.qld.gov.au/business-priorities/plants/weeds-pest-animals-ants/invasive-ants/fire-ants/general-information-about-fire-ants, accessed on 2018-8-28). With reference to the experience and lessons learned from the United States and Australia, S. invicta was put on the list of quarantine pests in China, and the strictest quarantine management was implemented immediately after the first report of S. invicta. In response to S. invicta invasion, many rules and plans were formulated by administration departments and enforcement agencies, including the Ministry of Agriculture and Rural Affairs, General Administration of Quality Supervision, Inspection and Quarantine, National Forestry and Grassland Administration, and General Administrative Office of National Health and Family Planning Commission (http://www.moa.gov.cn/xw/zwdt/200603/t20060306_563900.htm; http://www.moa.gov.cn/xw/zwdt/200412/t20041208_283440.htm; http://www.forestry.gov.cn/main/4818/content-797166.html). In addition, in provinces infected by S. invicta provincial governments issued a work program for red imported fire ant investigation, surveillance, and management, following the policies and rules of the Ministry of Agriculture and Rural Affairs. These policies and rules provided the basis and guarantee on red imported fire ant management.
In China, epidemics of S. invicta are ranked as Level 1, 2, 3, or 4 following the “Contingency plans for emergency response on red imported fire ant” (http://www.moa.gov.cn/nybgb/2005/derq/201806/t20180617_6152397.htm). Level 4 means that the invasive fire ant is in one county and that the county government or its agricultural agency must start a contingency plan to control its spread. Level 3 means that S. invicta is in two or more than two counties but these infected counties belong to the same prefecture; hence, the contingency plan for S. invicta control must start through the prefectural government or its agricultural agency. Level 2 means that S. invicta invasion is in different prefectures but in the same province, and thus the provincial government or its agricultural agency must start the contingency plan. Level 1 means S. invicta invasion is in different provinces, the Ministry of Agriculture and Rural Affairs starts the contingency plan. This emergency response system plays a key role in preventing the rapid expansion of S. invicta in China. This model could also become the blueprint in managing other new invasive pests in China.
Expansions of highly effective mechanisms and models designed for controlling the spread of S. invicta and preventing its entry to new regions are arduous tasks but need to be established urgently. In response to the invasion of S. invicta, China has dramatically launched several programs since 2004. There are three steps for the management of S. invicta, i.e., confirming the epidemic, formulating a scheme, and planning and organizing its implementation. In China, government agencies lead and are actively involved in all three management steps.
The current principle of routine fire ant management is dependent on the administration, i.e., fire ant management was launched by local county government where fire ant was invaded (Fig.
Financial support is one of the key factors on fire ant eradication and management. For example, New Zealand spent three years and ca 7.41 million USD to eradicate S. invicta successfully from a 12.56 km2 area of Whirinaki, which means that New Zealand spent 0.20 million USD per km2 in one year (http://www.scoop.co.nz/stories/PA0611/S00286.htm, accessed on 2019-6-5; http://b3.net.nz/gerda/refs/14.pdf, accessed on 2019-6-5). In China, Jiahe county of Hunan province spent three years and ca 82000 USD on an isolated infested area (ca 0.4511 km2) to successfully eradicate S. invicta, which translates to ca 0.06 million USD per km2 spent in a year just for eradicating an isolated infested area (data was collected from Bureau of Agriculture and Rural Affairs, Jiahe county). At present, Australia is planning to spend ca. 300 million USD over 10 years to eradicate red imported fire ants from a 7800 km2 region in south-east Queensland (https://www.daf.qld.gov.au/business-priorities/biosecurity/invasive-plants-animals/ants/fire-ants/eradication/10-year-plan, accessed on 2019-6-5) .
For many regions infested by fire ants, eradication is becoming impossible, and the local government instead runs a long-term management program that potentially consumes considerable financial resources. Shenzhen City is one of the best models in China. Shenzhen City spent ca 0.32 million USD to keep the fire ant under control in a 2000 km2 region in 2018, costing approximately 160 USD per km2 per year (data was collected from Shenzhen Agricultural Science and Technology Promotion Centre, http://www.szcast.com/index.html, accessed on 2019-6-5).
Although 40 products were registered for management of S. invicta in China, the main active ingredients were only 3 or 4 types, i.e. indoxacarb, fipronil, hydramethylnon, and beta cypermethrin. Among these four, the application of fipronil was forbidden in the agricultural system (http://www.icama.org.cn/hysj/index.jhtml, accessed on 2019-12-10). The selection of effective ingredients was done in China. Previous reports have suggested that other insecticides have great potential for the management of S. invicta, including sulfoxaflor, dinotefuran, clothianidin, nitenpyram, thiamethoxam, ethiprole, chlorfenapyr, cyantraniliprole (
Some research has also been done on repellence selection.
Studies on the biological control of S. invicta have been ongoing in China where entomopathogenic nematodes and fungi were evaluated.
Education is very important for invasive species management. After the pest was found in mainland China, the Ministry of Agriculture and Rural Affairs immediately announced the notice for the management of S. invicta. Then, several campaigns to inform the public about S. invicta were launched through various television commercials and leaflets. For example, several programs that introduce the biology and control methods of S. invicta were recorded and broadcast by China Central Television. These campaigns help the Chinese government to deliver messages to avoid panic by the public and to spread knowledge of the biology, behavior, and control of S. invicta. For instance, an intervention questionnaire (1715 valid questionnaires) in Shenzhen city showed that TV, internet, newspaper, and leaflets were the main ways residents received knowledge of S. invicta (
Meanwhile, fire ant management training activities were also lunched in infested regions, where entomologists who specifically study S. invicta were invited to give educational seminars and field training to residents, staff of agricultural agencies, and pest control companies. The national fire ant management training also held an anniversary for the staff of the agricultural agencies. The training normally has two parts where the attendees received educational presentations and fact sheets about fire ants and then field demonstrations of the methods for fire ant control.
In China, S. invicta can spread a long distance by the transportation of contaminated turf and nursery stock (
6.3.1 Plant quarantine
Surveillance at Chinese ports of logs, wastepaper, and wood packing materials from S. invicta-infected regions have shown that these objects were high-risk for the entry of S. invicta into China (
Domestically, transportation of infected garden plants and turf are considered the main vehicle the spread of fire ants (
6.3.2 Population assessment
Understanding the density, degree of damage, and boundary of occurrence is the first step for management of S. invicta. Populations can be estimated by scoring active S. invicta mounds, the number of workers per bait, and the percentage of bait with workers (
In China, “Solenopsis invicta Occurrence Notification System” was also applied. A total of 2488 surveillance sites were set up in more than 230 counties nationally where the area under surveillance reached more than 0.6 million hectares (
6.3.3 Chemicals application
Chemical application is the main method in managing the expansion of fire ants, especially in newly invaded regions. Many chemicals are effective for control, including bifenthrin, cyfluthrin, cypermethrin, deltamethrin, fenvalerate, fluvalinate, lambda-cyhalothrin, permethrin, s-bioallethrin, es-fenvalerate, tefluthrin, tralomethrin, carbaryl, and acephate (
In the first few years after S. invicta was found in mainland China, pesticides for S. invicta control were classified as special-need pesticides by the Ministry of Agriculture and Rural Affairs so that companies could put a certain number of specific pesticides on the market with a temporary registration certification (
Toxic bait and surface treatments, including liquid mound drench and application of granules or dusts, are the main methods for control of S. invicta (
The two-step method developed in the Unites States is one of the main and most effective methods for management of S. invicta. It involves a combination of contact dust and baits. i.e., “Step 1. broadcast a fire ant bait once or twice a year to reduce fire ant colonies by 80 to 90 percent. Step 2. Treat nuisance mounds or colonies that move into the bait-treated areas. Step 2 may not be needed.” (http://articles.extension.org/pages/14345/fire-ant-control:-the-two-step-method-and-other-approaches). Following the example used in the United States, a modified two-step method was developed in China. Step 1: whole area control. Broadcast a bait in areas with high densities of S. invicta or apply bait on individual mounds in areas with low densities. Meanwhile, contact dust is used to treat individual mounds that are easy to handle. Step 2: Key area control. After 4–6weeks, the population of S. invicta is assessed. Then, the remaining parts of the area with a high population of S. invicta is treated by bait and the individual mounds is treated by contact dust. After the two steps, fire ant colonies can be reduced by as much as 90%. The cycle of the two-step method can run again and again until S. invicta population is under control or eradicated in the treated area.
6.3.4 Model for fire ant management in China
The main system for managing S. invicta in China is hierarchical from top to down, i.e., the local government provides the financial support and the agricultural sectors (such as the Department of Plant Protection and Plant Quarantine, Agricultural Agency of county government), purchases the pesticides and management tools, and distributes these to the organizations of mass self-government (such as resident committees). However, this system is not very suitable for the management of S. invicta. Here are the main shortcomings: 1) basic-level agricultural agencies have a hard time comprehensively and effectively managing S. invicta because these agricultural agencies have limited human resources to oversee the huge and complicated job of managing all pests. This may result in a scenario where some staff may lack the professional ability to involve, guide, and supervise on management of S. invicta. 2) The field workers involved in the management of this species are always temporary employees in the basic-level government. Even with professional training, most workers still cannot fully master the technique and, as a result, pesticide use has always been a waste due to improper application. For instance, an investigation found that the control efficacy was only 20–65% when control was organized and operated by resident committees (personal communication).
Currently, professional pest control organizations are involved in the management of S. invicta in some provinces. In this system, the government agencies must create control plans and goals, review and approve the implementation plans that are provided by pest control organizations, inspect and supervise the implementation process, and check the control efficiency. The professional pest control organizations must make implementation plans, implement the management plans, and follow the goals of the government agencies. A third party, which is also the professional organization, was introduced by government agencies to inspect the implementation process and check the control efficiency. The professional pest control organizations have the professional skills to run an effective measure against S. invicta. This system does not only easily achieve the aim of managing S. invicta but also saves manpower, pesticides, and financial resources. The model is already running in several provinces and shows good effectiveness (http://www.hnjh.gov.cn/jhzf/2/3723/3757/3995/content_280184.html, http://www.ccgp.gov.cn/cggg/dfgg/jzxcs/201812/t20181213_11335311.htm; http://www.sx.gov.cn/art/2018/7/2/art_1463355_19027725.html, http://www.changsha.gov.cn/xxgk/szfxxgkml/ztbd/2014nddzldbzjxkhgzmbgs/zssnyj/201505/t20150518_722617.html, accessed on 2019-6-5) .
The model was also designed and implemented for area-wide suppression or eradication of fire ants in China. When the control strategies for S. invicta are formulated, several factors are taken into consideration, including the distribution pattern of the infestation (whether widely distributed or localized), the environmental characteristics of infested area (complexity of habitat), and the characteristics of the occurrence of S. invicta (mounds are easy or difficult to find). Inspections of the whole given area are conducted at the onset of the program to identify unreported infestations. Then, plant quarantine is strictly implemented to prevent dispersal of S. invicta in the given areas. Education of residents about the control measure follows. The new two-step method is then applied to the area of infestation. After one cycle of the new two-step method, the inspections of the whole given area are conducted again to evaluate the efficiency of the control and the situation of the infestations. These control steps can be applied in the infected area over and over until the aim is achieved. The model has been conducted in fire ant management programs and has been successful. For example, in the Tianhe District of Guangzhou after using the model for five months, from June to October 2013, the active mound of S. invicta reduced by 99.3% and the number of active fire ant workers reduced by 98.4% (unpublished data). In Hunan province, the agricultural agency of Jiahe county used the model and successfully eradicated S. invicta from a 45-ha region (http://www.hnjh.gov.cn/jhzf/2/3723/3757/3995/content_280184.html, access on 2019-6-5).
Since the discovery of S. invicta in China, great efforts have been made to control and prevent its invasion and expansion. To date, safe and effective technology systems designed for monitoring, quarantine, emergency response, and eradication has been developed. These technology systems give strong support to the management of S. invicta, although fire ants still expand their territory within China. Based on past experiences of fire ant management programs in China, the strategies below might help the country in better responding to the threat of invasion by S. invicta.
First, plant quarantine should be put in place. Poor fire ant management and lack of plant quarantine for seedlings remain one of the important reasons why S. invicta continues to quickly expand its territory in China. Long-distance domestic transportation of potted flowers, turf, nursery stock, and waste materials is the main means of dispersal for this species. Urbanization in China has increased the requirement for potted flowers, turf, and nursery stock and has accelerated the spread of fire ants. Meanwhile, more than 10 million landscaping seedlings are transferred from S. invicta-infested regions to uninfested regions every year in China, and many of these plants may not get the appropriate quarantine treatment because of lack of funds and a shortage of human resources. Also, interceptions of S. invicta in many Chinese ports has increased in cargo originating from other countries and regions. Therefore, the management of fire ant population in farms producing seedlings, effective quarantine technology system, and quarantine model should be strengthened and developed, as good management and quarantine can slow down the speed of S. invicta.
Second, the fire ant management system of government agencies should be updated. Various government agencies, for example agricultural and forestry, are involved in the management of S. invicta. However, cooperation among different local government agencies is not well executed, which has resulted in poor control of S. invicta in some regions. For fire ants to be eradicated at all points and in all regions, local government agencies should update the monitoring system, as well as its management, to avoid fire ants from reinfecting regions.
Third, developing more effective pesticides and applied methods is important to curb the spread of S. invicta. Traditional management methods are time consuming and laborious, especially in large areas with a high density of S. invicta. The development of rapid detection of nests is important for assessing control efforts and monitoring dispersal. Satellite aerial imagery could be used to assess the distribution of S. invicta mounds on a large scale (
Fourth,
We thank Dr Jian Chen,