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International Journal of Zoology and Animal Biology Research Article 32 min read

A Review on the Biological Control of Common Ragweed, Ambrosia artemisiifolia (Asteraceae)

Chao MA, Hong Song CH, Chen Chen Z, Yan Z, Zhen Ya T, Guang Mei C, Fang Hao W# and Zhong Shi Z*
* Corresponding author
ISSN: 2639-216X  10.23880/izab-16000498  Received: August 01, 2023  Published: August 14, 2023
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Keywords
Common Ragweed Ambrosia Artemisiifolia Biological Control Zygogramma Suturalis Epiblema Strenuana Ophraella Communa
Abstract

Common ragweed (Ambrosia artemisiifolia) is an annual in the Asteraceae that is broadly distributed in most temperate regions of the world. Since it is both extremely competitive and has allergenic pollens, common ragweed presents problems to agricultural production and public health. Currently, over 450 species of natural enemies of ragweed have been discovered, among which the leaf beetle Zygogramma suturalis (Chrysomelidae) and the moth Epiblema strenuana (Tortricidae)have been the two most effective species for ragweed suppression. In addition, in China outstanding control has been provided by the leaf beetle Ophraella communa. The complementary use of O. communa and E. strenuana has also been tested in southern China to good effect on A. artemisiifolia. In addition, several pathogens have been considered as potential biological control agents of common ragweed. This paper mainly introduces common ragweed, considers its negative effects, and reviews the history and current achievements of common ragweed biological control.

Introduction

Common ragweed (Ambrosia artemisiifolia) is an invasive North American plant that has spread across most temperate regions of the world since the mid-19th century, especially in recent decades when it was facilitated by socio-economic factors. Currently, common ragweed can been found in Europe, Asia, Africa, South America and Oceania. In the 1930s, ragweed spread to the southeast coast of China, and the earliest ragweed specimens were collected in Hangzhou (Zhejiang, Province) in 1935 [1]. Since common ragweed has escaped from biotic factors (e.g., natural enemies) in its new range, its population has expanded rapidly and it has caused significant damage in China. In 1997, ragweed was classified in China as one of three most dangerous weeds, at which time it was widely distributed in 21 provinces in China [2].

Common ragweed is an annual herbaceous member of the Asteraceae that is extremely competitive and can quickly invade both agricultural and urban areas. In recent decades, more attention has been given to common ragweed in China because it can lower crop yields, and its pollen is a potent human allergen. While a range of physical and chemical controls have been employed against common ragweed, biological control provides a new approach for the control of common ragweed, and biological control has been found to be among the most effective and sustainable methods [3]. Biological control of common ragweed began in the 1960s [4], and in the ensuing decades many natural enemies have been discovered [5, 6] and biological control of common ragweed has entered a new stage. Here, we review the biology of common ragweed, its effects on agricultural production and public health, and management tactics for control of common ragweed, especially biological control in worldwide.

Biology and Negative Impacts of Common Ragweed

Common ragweed seeds germinate in spring, grow from May to August, and flower from August to October [7, 8]. Common ragweed produces thousands of seeds per plant, and these seeds can remain dormant in the soil for long periods. One common ragweed plant can produce 3,000-62,000 seeds, and some seeds (4%) can remain viable underground for 39 years [9, 10]. Consequently, common ragweed can produce a large seed bank in the soil. Fumanal, et al. [11] reported that the total soil seed bank (to a depth of 20 cm) ranged from 250 to 5,000 seeds/m2 while the top 5 cm of soil held 200-2,800 seeds/m2 seeds.

In central and eastern Europe, common ragweed is a dominant weed in cultivated fields [12]. Common ragweed at densities of 5 and 10 plants m-2 reduced sunflower yields 21% and 30%, respectively, and that of maize by almost 30% at both densities [13]. Compared to a weed-free condition, common ragweed caused losses of 50-70% of sugar yield in sugar beet [14]. When the ragweed population is high, yield loss in soybean can reach 75% [12], and 80% in maize [15]. Common ragweed is also a serious risk to human health, whose pollen is one of the most potent human allergens in the world [16]. Its pollen is responsible for hay fever, asthma and hypersensitivity dermatitis. Whether in its native or introduced range, common ragweed pollen poses a threat to human health. In most areas of the USA and Canada, common ragweed pollen has become the second most common cause of asthma and rhinitis [17, 18]. In Europe, the proportion of people sensitive to common ragweed pollen is 10% generally [19], and 60% in Hungary in particular [20].

Biological Control of Common Ragweed

Classical biological control is considered to be an effective method to control invasive plants by introducing phytophagous natural enemies from their native region. According to the Enemy Escape Release Hypothesis [21], introduced plants become invasive because of escape from their usual herbivores or pathogens in newly invaded areas.

Attempts to achieve biological control of common ragweed began in the 1960s, when many invaded countries began to search for effective common ragweed natural enemies in North America. In its original range, common ragweed is attacked by various invertebrate herbivores, such as Zygogramma suturalis F. and some polyphagous consumers including beetles, moths and bugs [22]. While most of these insects feed on common ragweed leaves, the plant is also attacked by stem-galling moths in the genus Epiblemaand seed predators such as ground beetles (Harpalus spp: Carabidae) and snails (Trichia striolata: Hygromiidae) [23]. The eriophyid gall mite Aceria artemisiifoliae sp.nov. (Acari: Eriophyoidea) is a potential biological control candidate of common ragweed in Serbia, due to its narrow host range and ability to prevent male flower development, thereby reducing pollen production [24]. Farr, et al. found more than 25 fungal pathogens with impacts on common ragweed [25]. While some 450 species of insects, mites, or fungi are known from species of plants in the genus Ambrosia [26], most are polyphagous species that cause little impact on common ragweed. For use as biocontrol agents, specialized agents are required, such as Z. suturalis and E. strenuana, and it is such specialized agents that are most likely to be successful.

Zygogramma Suturalis

The leaf beetle Z. suturalis (Coleoptera: Chrysomelidae) is a monophagous natural enemy native to North America. This leaf beetle is known only to feed on common ragweed and perennial ragweed (Ambrosia psilostachya Decandolle) [27]. Wan, et al. [28] conducted a host selection test in the laboratory, and found that among 72 plants species including major cash crops, grain crops, ornamental plant and species closely related to ragweed, Z. suturalis only fed on common ragweed. In no-choice feeding tests, both adults and larvae fed exclusively on common ragweed among 126 species [29]. Under laboratory conditions, females, males live on average 82.5 and 67.8 days, respectively, at 26℃. Female Z. suturalis beetles have a lifetime fecundity of 394.5 eggs, and eggs can hatch from 28 to 32℃. The optimum temperature for development of Z. suturalis immature stagesis 24-28℃ [30]. In Ohio, Z. suturalis underwent two generations each year and 2-3 generations in the Soviet Union [27]. In China, the beetle undergoes three generations in Beijing and Dandong, but only two generations a year in Hunan province [4]. In addition, Z. suturalis adults has a strong tolerance for starvation and low temperatures. Females of Z. suturalis feed on undamaged ragweed plants but lay their eggs on other nearby ragweed plants [31]. Under natural conditions, ovipositing females tend to leave damaged common ragweed plants for less damaged plants [31]. If the common ragweed population suffered at an extremely high level, female Z. suturalis are unable to find intact common ragweed plants on which to oviposit, resulting in the females entering reproductive diapause during the summer [31].

The former Soviet Union imported Z. suturalis from North America in 1978 and the species was established successfully in the northern Caucasus Mountains [32]. In the Caucasus Mountains, Z. suturalis suppressed common ragweed populations at release sites and nearby locations between 1983 and 1985 [33]. The density of the beetle Z. suturalis in the Caucasus Mts. at the height of its abundance in this region reached 5,000 individuals per m2 in farmland in south USSR and destroying all ragweed completely, resulting in a two to three fold increase in crop production [26]. In addition, Z. suturalis also significantly reduced the density of common ragweed seeds in the soil surface, from 24,000/ m2 in 1980 to 35/m2 in 1985 [34]. Further investigation has shown that Z. suturalis population density remains at a low level in fields after this wave of near complete defoliation of the host plant. In 2005 and 2006, found to be 0.001 adults of Z. suturalis per m2 in fields of rotated crops and 0.1 adult per m2 in more stable habitats; consequently the impact on common ragweed was considered negligible [33]. Overall, the introduction of Z. suturalis was considered as a moderate success. The former USSR republics of Kazakhstan, Georgia, and Ukraine also released Z. suturalis in 1978, but Z. suturalis only established in Kazakhstan [32]. In the early 1980s, Croatia (then part of the former Yugoslavia) introduced Z. suturalisfrom the USA and released it near Bjelovar, Zagreb, et al. [29]. In 1988, establishment was confirmed in Zagreb and Zadar and the common ragweed population was suppressed to a certain extent. However, in autumn of 1991, the beetle population decreased drastically and lost its control of common ragweed [29]. Over the same period, Australia and Hungary also introduced this beetle but it failed to establish [32, 35].

In view of the success of Z. suturalis in Russia, China introduced this leaf beetle from Canada and former Soviet Union in 1987 [28]. After a series of biology, ecology and host specificity studies of Z. suturalis, 30,000 individuals were released in Beijing and three cities in Liaoning province (Shenyang, Tieling, Dandong) from 1988 to 1991. As in Russia, the Z. suturalis population initially developed quickly, established, and partly suppressed the pest [36]. However, the leaf beetle proved unable to adapt to the climatic conditions in this part of China and its population disappeared [36]. The major reason for the failure of application of Z. suturalis may be related to its oviposition strategy, which causes Z. suturalis to remain at a low density in field [31, 37]. In addition, its weak searching and spreading ability limits Z.

suturalis population reproduction and its control effect [38].

Epiblema Strenuana Walker

Epiblema strenuana (Lepidoptera: Tortricidae) is an effective biological control agent against common ragweed and Parthenium hysterophorus [39]. Females scatter eggs host plant foliage and, larvae emerge in 3-5 days and feed on leaves [40]. After a few days, larvae bore into the stem at a growing point, typically at the axil and top buds. As the larvae continue to feed, forming a stem gall [40]. Larvae pupate inside the gall and then emerge through a portion of the stem that has been eaten to a thin-walled emergence window before pupation. Newly emerged adults can mate immediately [40]. E. strenuana adults have high dispersal ability and can fly over 20 kilometers with the wind, giving them an annual dispersal rate of as much as 160 kilometers [41]. E. strenuana developmental periods are egg (4 days), larvae + pupa (28-30 days), and adult (7-11 days) at 22-30℃ [41]. There are six generations per year in Australia [41] and 2-3 generations in Mexico [42]. In China, 2-3 generations occurred in Beijing, two generations occurred in Dandong (Liaoning procinve) and 4-5 generations were found in Hunan province [30]. Mature larvae overwinter in the stem of the host plant in diapause. Five plant species are most commonly used by E. strenuana: common ragweed, Ambrosia trifida, Ambrosia psilostachya, Parthenium hysterophorus, and Xanthium sp. In addition, E. strenuana occasionally feeds on Siegesbeckia orientalis and Artemisia annua. However, in the presence of common ragweed and P. hysterophorus, S. orientalis and A. annua are generally free from damage [39]. Under no- choice conditions, E. strenuana can feed and develop on Bidens pilosa, Rsdbeckia hirta, Tagetes erecta, Tagetes patula and Parthenium confertum, and can also oviposit and feed on Guizotia abyssinica [43]. In Mexico, 14 economically important species of composite plants, including species of Helianthus, were examined in host range tests. Among these plants, E. strenuana was only able to complete its development on P. hysterophorus. Only one adult was discovered on B. pilosaand R. hirta, and its developmental stages were prolonged significantly on these plants. But in the field, there has been no observation of E. strenuana feeding on B. pilosa [42]. Multiple-choice tests were conducted in Queensland [44], which found E. strenuanaonly fed on common ragweed, P. hysterophorus and Xanthium strumarium, consistent with results by Wan FH [45]. Since first being released in sunflower growing regions of Queensland, there has been no records of E. strenuana damaging sunflower, demonstrating the limited host-range of this moth. However, E. strenuana was rejected for release in India for completely developing on Guizotia abyssinica in laboratory testing [43]. Russia and Africa also have noted potential risks with releases of E. strenuana [46].

Because larvae of E. strenuana bore into and gall plant stems, they change the physiological status of host plant [47]. Fusiform stem galls such as those of E. strenuana, cause plants to change their metabolism and disrupt the tissue regeneration process, stopping the further growth and development of host plants [42]. E. strenuana was introduced from Mexico into Australia in 1979 as a biological control agent of Parthenium hysterophorus (Asteraceae) [48]. After the first release of the moth in Queensland, E. strenuana established and spread rapidly to most P. hysterophorus- infested areas within two years [49]. In 1984, field surveys found 500-800 galls per square meter and E. strenuana spread to an area of 120 thousand square kilometers, at least 25% of the invaded area. Observed that heavily attacked host plants were severely stunted, bearing 30 to 100 stem galls [50]. The stem-galling moth scan kill seedlings and significantly reduce plant height and flowering production, thereby reducing the production of pollen and seeds. However, being attacked by E. strenuana has no effect on seed fresh weight, the percentage of seeds filled or seed vitality [42]. Presently, common ragweed is under good biological control in Queensland, and New South Wales [50] as a result ragweed is no longer a serious weed in eastern Australia. China introduced E. strenuana from Australia and released the moth in Beijing in 1990 and in Yue yang, Hunan province in 1993 [51], where it established and spread across Hunan province, eventually covering more than 2000 hectares.

Ophraella Communa

Ophraella communa (Coleoptera: Chrysomelidae, Galercinae), originating from North America, is an oligophagous insect feeding on various species of Asteraceae, including common ragweed. The leaf beetle is multivoltine and all stages occur on ragweed. Currently, O. communa populations are present in the USA, Canada, Mexico, Japan, South Korea, and China. In Japan, the beetle was discovered in Chiba Prefecture in 1996, from where it quickly spread across eastern Japan within two years [52]. In 2001, O. communa was occasionally found in China in Nanjing in Jiangsu province, and by now is widely distributed across southern China [53]. This beetle has also been found recently attacking common ragweed in northwestern Italy [54], which is the first report of O. communa in Europe, presumable from natural or accidental spread. Ophraella communa undergoes at least three generations each year in southern California [55], four or five generations in Japan [56], and at least four generations in Nanjing, China [57]. Female beetles lay eggs on the front or back of common ragweed leaves, which turn quickly from yellow to orange. Eggs hatch in four or five days and there are three larval instars. Mature larvae spin loosely woven cocoons and pupate on common ragweed leaves or stems. Usually, O. communa takes one month to finish its life cycle in summer. On perennial ragweed, Goeden and Ricker found a female can oviposit 667 eggs, with an oviposition period of 66 days and a total developmental period of 25 to 29 days [58]. Welch reared the beetle on common ragweed at 26℃ and a 16:8 h L:D photoperiod, and found developmental times for eggs, larvae, pupae and pre-adults to be 5.1, 8.9- 11.4, 3.7-4.4 and 21.8 days, respectively [59]. Adults can also display mixed sex aggregations in the field. Mate location and recognition depend on olfactory and tactile cues, but sex pheromones absent [60]. A study showed that O. communa could survive and reproduce successfully at different photoperiods, which may expand its distribution to regions [61]. Subsequently, they also reported frequent mating can significantly increase male and female adult longevity, fecundity, and the hatch rates of eggs [62]. Interestingly, studies have reported that large males of O. communa facilitate population expansion [63].

Generally, in the presence of ragweed in the field, O. communa only feeds on common ragweed, but it can also foraging some other species of Asteraceae such as A. psilostachya, Iva axillaris, and X. strumarum. Palmer and Goedenstudied the leaf beetle host selection using small scale, no-choice tests, and found that both larvae and adults feed on A. psilostachya, X. strumarum, Parthenium and H. Annuus [55]. In addition, eggs were also laid on H. annuus, leading to the rejection of the use of O. communa as a natural enemy even though there is no record of O. communa as a pest of H. annuus in its native range in North America [55]. Yamazaki, et al. [56] studied the feeding behavior of O. communa and found that it preferred common ragweed and that sunflower was free of damage in the presence of O. communa. Dernovici, et al. [64] used both choice and no- choice tests to demonstrate that common ragweed is the main host plant of the leaf beetle. Even though sunflowers suffered some damage in the no-choice test, the beetle cannot complete its life cycle on sunflowers and beetle populations decrease on sunflowers. Hu, et al. [65] found O. communa feeding on H. annuus, X. strumarum, Helianthus tuberosus, Eupatorium adenophorum, Centipeda minima and Carpesium abrotanoides among a total of 52 plant species tested. However, except for common ragweed, feeding by O. communa on other plants was insufficient to support the development of its offspring, and reproduction was reduced on these plants.

Because both larvae and adults feed extensively, have short developmental periods, high fertility, and high longevity, O. communa populations can completely defoliate a common ragweed stand within a few insect generations [52]. At high densities, O. communa can prevent flowering and seed set. In addition, O. communa has a strong host discrimination ability and spreads rapidly [56]. Moriya, et al. [66] reported that the average rate of beetle expansion was 100 km/year, making the leaf beetle a promising biological control agent of common ragweed in China. In Canada, O. communa has been widely applied augmentatively against common ragweed in various vegetable crops and organic soybean fields, achieving good control and demonstrating the potential for using O. communa to suppress ragweed in this way [67, 68]. In addition, the leaf beetle has been successfully used to control common ragweed in the USA and Mexico [68]. Teshler, et al. [69] designed a device especially for collecting and transporting the leaf beetle for long distance use, making its augmentative use practical. In Europe interest in this species is developing. Kiss found O. communa to be the most suitable biological control agent of common ragweed in Europe [68]. In Japan, the leaf beetle was first discovered in Chiba-ken in 1996, from where it spread quickly and could be found in 39 ragweed infested areas in 2001, causing significant control on common ragweed [56, 70]. O. communa has also been found in many regions of South Korea including Inchon and Busan, where it can completely kill common ragweed plants, reducing pollen and seed production. In Italy, common ragweed populations were completely defoliated by O. communa feeding, stopping growth, causing the plant to dessicate, and preventing flowering and pollen production [54]. Since O. communa was first discovered in Nanjing in 2001, it has spread across southern China [53]. In areas where this leaf beetle is present, common ragweed has been significantly suppressed. In a field-release experiment, with increasing initial release density of O. communa adults, plant height and number of branches was reduced and the leaf control index increased [71]. In the early stage of ragweed growth, even at a release density as low as 1adult per plant, the beetle significantly suppressed plant height and number of branches and a higher leaf control index compared with the herbicide treatment.

Pathogens

In common ragweed’s native range, it is infected by many pathogens. Among these, Puccinia xanthii is the most promising species for biological control. Puccinnia xanthii is a microcyclic autoecious rust that has been reported to infect common ragweed in some regions of North America [25, 72]. This rust as a species is comprised of several different formae speciales that have a high degree of host specialization and can complete their life cycles on just one plant species performae speciales.

Another fungal pathogen of common ragweed, Protomyces gravidus causes a stem gall disease on A. trifida in the USA, and has been evaluated as a mycoherbicide against both giant and common ragweed [73]. While the fungus causes stem gall disease and ragweed mortality if hosts are infected systemically, mycoherbicide production has a low infection rate and a general lack of virulence, limiting its control ability of common ragweed.

A third fungal pathogen, as species in the genus Phoma performed well in inundative experiments where it was tested as a potential mycoherbicide. When combined with the leaf beetle O. communa, Phoma and the beetle synergistically increased common ragweed mortality [74].

Another mycoherbicide under development is a strain of Sclerotinia sclerotiorum, which was evaluated as a potential biocontrol agent of common ragweed in Hungary [75]. In the same study, two fungal pathogens, Phyllachora ambrosiae and Plasmopara halstedii, were found to significantly suppress common ragweed and its pollen production in 1999 and 2002, but no infection of ragweed was discovered in other years [76, 77].

In glasshouse trials, the bacterium Pseudomonas syringae pv. tagetis was found to infect a related species, Ambrosia Grayi, causing systemic chlorosis. This bacterium was found to kill the weed at low concentrations under field conditions in Texas [78]. However, none of these pathogens can be cultured in vitro, making them as of yet unsuitable for mass production and application as a mycoherbicide.

Joint control with Two Biological Control Agents

According to the ecological niche theory, two or more phytophagous insects that do not directly compete for resources will synergistically combine to produce greater damage to their host plant. Ostrinia orientalis, a local herbivore associated with X. sibiricum in Hunan, China, attacks ragweed. Ma, et al. [79] found that the selection and use of host resources differed significantly between E. strenuanaand O. orientalis and competition between them was rare in the field. Similarly, the spatial niche resources needed by O. communa and E. strenuanaare different because all developmental stages of O. communa occur on common ragweed leaves and both E. strenuana larvae and pupae live in ragweed stems. This means O. communa and E. strenuana can survive together on the same common ragweed plant and there control effects should be synergistic. Zhou, et al. [80] demonstrated that a combination of O. communa and E. strenuana killed all common ragweed plants before seed production, while all or some plants could survive or bear seeds in the other, single species treatments and control plots. A joint biological control strategy using both O. communa and E. strenuana has been proposed in China, and it has been widely adopted in Hunan, Jiangxi, and Guangxi provinces, markedly inhibiting the development and diffusion of common ragweed [2].

Discussion

As global trade and travel increase every year, common ragweed has more opportunities to be accidentally spread as a crop or birdseed contaminant, in ballast soil or in other cargo. Climate changes may further cause this species to spread in to currently unsuitable areas of the world. To date, various control methods have been used in different regions of the world. In Europe (except eastern Europe), the main methods to control common ragweed are artificial extraction, physical machinery and herbicide control or combined measures. However, these methods require extensive manpower and material resources. In addition, the movement of people or machines may unintentionally spread common ragweed to new locations. Sometimes the actual terrain of ragweed habitat will limit the control implementation for mowers. Control of common ragweed with herbicides is very difficult in crops like sugar beet or soybean, and is nearly impossible in sunflowers because both common ragweed and sunflower belong to the same botanical family. Furthermore, the continuous application of herbicides results in herbicide resistant common ragweed biotypes and loss of biodiversity, which carries a risk to human health. More problematic, short-term abandonment, inadequate chemical control and mowing may stimulate the development of persistent soil seed banks and allow common ragweed to sprout quickly from the bases of stems. Some countries have passed legislation on the control of ragweed and launched large-scale ragweed eradication campaigns [81]. On the other hand, many countries have a long history of the biological control of common ragweed, including Russia, the former Yugoslavia, Georgia, Ukraine, Australia, China and Kazakhastan. Especially in Australia and China, the biological control of common ragweed is considered an outstanding success [82, 83]. Significantly, in china, one study found that O. communa can follow host plants by adapting to new temperature environments via rapidgenetic evolution [84]. Although there is no single agent that is and effective biological control agent for common ragweed in Europe, more and more scientists are shifting their focus to biological control and many previously studied species have been reconsidered.

Unfortunately, there are several introduced enemies that have failed after release in the field. For example, Tarachidia candefacta was the first intentional introduction of a natural enemy for biological control of common ragweed in Europe and released in 1969 [85]. While the noctuid moth cannot play an effective role under harsh environmental conditions [86], Euaresta bella, Trigonorhinus tomentosus (Say), and Zygogramma disrupta Rogers have all been shown to have strict host specificity, although all failed to establish after release in Russia [32]. Wan and Dingintroduced Z. suturalis, E. strenuana, Liothips sp., Euaresta spp., and T. candefacta into China during 1990s, but only E. strenuana established successfully [45]. With more than 450 species that attack ragweed in North America, the selection of specific and effective natural enemies is still the most critical work for the biological control of common ragweed. When an organism is selected as biological control agent, its biology, ecology, and host-specificity should be studied before release. In addition, a prediction of suitable habitat and proper domestication for introduced natural enemies is also needed [87].

Compared with other methods, biological control for alien plants is safe, practical and economically feasible [87]. More and more countries are adopting this approach, even as outstanding successes in Australia and China have demonstrated that biological control is a promising method in such situations. In the future, relevant laws are needed to strengthen the control of common ragweed, and the public is still to be encouraged to increase their awareness over common ragweed control and engage more in management programs.

Acknowledgements

This work was supported by the Youth National Natural Science Foundation of China (No. 32102292) and China Postdoctoral Science Foundation (2021M693461).

Statements and Declarations

  • Funding: The authors declare that no funds, grant or other support were received during the preparation of this manuscript.
  • Conflicts of interests: The authors have no relevant financial or non-financial interests to disclose.
  • Ethics Approval: Not applicable.
  • Consent to Participate: Not applicable.
  • Consent for Publication: Not applicable.
  • Code Availability: Not applicable.

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@article{chao2023,
  title   = {A Review on the Biological Control of Common Ragweed,
Ambrosia artemisiifolia (Asteraceae)},
  author  = {Chao MA, Hong Song CH, Chen Chen Z, Yan Z, Zhen Ya T, Guang Mei C, Fang Hao W# and Zhong Shi Z},
  journal = {International Journal of Zoology and Animal Biology},
  year    = {2023},
  volume  = {6},
  number  = {4},
  doi     = {10.23880/izab-16000498}
}
Chao MA, Hong Song CH, Chen Chen Z, Yan Z, Zhen Ya T, Guang Mei C, Fang Hao W# and Zhong Shi Z (2023). A Review on the Biological Control of Common Ragweed,
Ambrosia artemisiifolia (Asteraceae). International Journal of Zoology and Animal Biology, 6(4). https://doi.org/10.23880/izab-16000498
TY  - JOUR
TI  - A Review on the Biological Control of Common Ragweed,
Ambrosia artemisiifolia (Asteraceae)
AU  - Chao MA, Hong Song CH, Chen Chen Z, Yan Z, Zhen Ya T, Guang Mei C, Fang Hao W# and Zhong Shi Z
JO  - International Journal of Zoology and Animal Biology
PY  - 2023
VL  - 6
IS  - 4
DO  - 10.23880/izab-16000498
ER  -