Control of the invasive weed Ambrosia artemisiifolia with Ophraella communa and Epiblema strenuana

Ambrosia artemisiifolia L. is native to North America, and was unintentionally introduced into China in the 1930s, where it has become invasive. The two insect species Epiblema strenuana and Ophraella communa have been considered as biological control agents of A. artemisiifolia in China. The purpose of this study was to examine the control effect of O. communa + E. strenuana on A. artemisiifolia in the field. The mortality of A. artemisiifolia plants increased with time and increasing initial release densities of O. communa and/or E. strenuana in 2008 and 2009. The treatments of 0.53 O. communa + 0.53 E. strenuana per plant and 12 O. communa + 16 E. strenuana per plant at early (60–70 cm tall) and later (90–100 cm tall) growth stages could subsequently kill all plants prior to seed production in both 2008 and 2009. Thus, the two initial densities of the two insect species may be recommended when they are jointly used for biological control of A. artemisiifolia at the two growth stages. However, all or some plants could survive and bear seeds in any other treatment and in the non-treated control plots. This implies that biological control of A. artemisiifolia with the two biological control agents will be recommended in the areas invaded by A. artemisiifolia in China.     

Review of the biology and ecology of a ragweed leaf beetle,Ophraella communa (Coleoptera: Chrysomelidae), which is a biological control agent of an invasive common ragweed,Ambrosia artemisiifolia (Asterales: Asteraceae)

A ragweed leaf beetle, Ophraella communa (Coleoptera: Chrysomelidae), has been highlighted as a potential biological control agent of Ambrosia artemisiifolia. O. communa and A. artemisiifolia are native in North America and alien species in East Asia and Europe. As an invasive weed, A. artemisiifolia causes severe economic losses as reducing agricultural production as well as producing severe allergenic pollen. As an herbivore insect, O. communa has strong host preference on A. artemisiifolia. All the developmental stages of O. communa can be found on A. artemisiifolia and it attacks a single plant in repeated and extended manners. With few individuals on A. artemisiifolia, O. communa can completely defoliate before pollen production. Therefore, O. communa had been focused as a biological control of this invasive weed, but its introduction was denied because of possible damage on an important crop, Helianthus annuus. O. communa was accidentally introduced in East Asia and Europe in 1990s and 2010s, respectively. Fortunately, O. communa population was well established to suppress A. artemisiifolia in the introduced areas. Following detailed field surveys and host specificity tests of O. communa were conducted and proved a strong potential of O. communa as a biological control agent of A. artemisiifolia. Moreover, O. communa has been investigated in physiological and evolutionary studies. In this study, the potential of O. communa as a biological control agent and a study organism are reviewed.     

永州广聚萤叶甲和豚草卷蛾的种群动态及对豚草的控制效果

【目的】豚草是一种重要的入侵杂草,严重危害农业生产和人类健康。广聚萤叶甲和豚草卷蛾是豚草的专一性天敌。研究这2种天敌在永州的种群动态及其对豚草的控制效果,可以为永州豚草的防控及这2种天敌的有效利用提供依据。【方法】在湖南省永州市江永县豚草大面积发生区域,人工释放广聚萤叶甲和豚草卷蛾,调查这2种天敌在释放区和扩散区的种群动态和对豚草的防治效果,以及这2种天敌在扩散区的越冬情况。【结果】广聚萤叶甲和豚草卷蛾的扩散能力强。释放1个月后,在释放区,广聚萤叶甲各虫态及豚草卷蛾虫瘿均被发现。整体上,随时间延长,广聚萤叶甲各虫态虫口密度先增后减,而豚草卷蛾虫瘿密度呈逐渐降低趋势。释放2个月后,在距释放区边缘10 km的豚草发生区,发现了广聚萤叶甲和豚草卷蛾,且成功建立了种群并顺利越冬。释放区豚草株高几乎没有增加,且叶片最终被取食精光,几乎全部死亡;扩散区豚草株高略有增加,最终近75%叶片被取食。【结论】广聚萤叶甲和豚草卷蛾可在永州成功建立种群并安全越冬,还能自行扩散,可持续控制野外豚草的发生。     

Reevaluation of biosecurity of Ophraella communa against sunflower (Helianthus annuus)

Ophraella communa (Coleoptera: Chrysomelidae), originally from North America, has been used for biological control of common ragweed, Ambrosia artemisiifolia, in China since 2007. However, there is still a debate on whether O. communa can attack sunflowers under field conditions. To re-evaluate the biosecurity of O. communa against sunflower (Helianthus annuus), we investigated the population density of O. communa on three sunflower varieties that were intercropped with or planted in circumambience of A. artemisiifolia under field conditions. Our results showed that only very few O. communa eggs (<0.5 eggs/plant) were found on sunflower plants at the last two surveys when sunflowers were planted in circumambience of common ragweed. O. communa eggs were not found on sunflower plants at each survey when sunflowers were intercropped with common ragweed. The first–second instar larvae, third instar larvae, pupae and adults of O. communa were occasionally found on sunflower plants, but their densities were very low under either case of planting patterns. Based on these results, we conclude that sunflower is not a potential host plant for O. communa and the beetle is an effective host-specific biological control agent of common ragweed.     

Rapid cold-hardening response in Ophraella communa LeSage (Coleoptera: Chrysomelidae), a biological control agent of Ambrosia artemisiifolia L.

In China, an unintentionally introduced beetle Ophraella communa shows good control efficiency against invasive common ragweed, Ambrosia artemisiifolia. With the aim of understanding the capacity of O. communa to overcome sub-zero low temperature rapidly, the longevity, survival and fecundity of the beetle adults were studied at conditions of different rapid cold-hardening in the laboratory. The results showed that approximately 20% female or male individuals still survive at ?12°C for 2 h, thus the discriminating temperature for rapid cold-hardening of both female and male beetles is ?12°C. The survival, longevity and fecundity of adult beetles were significantly affected by rapid cold-hardening treatments. Compared to the control, the survival rates of adult beetles experiencing 2 h of rapid cold-hardening at 2, 5 and 8°C prior to exposure to its discriminating temperature (?12°C) were significantly increased. Adult longevity and fecundity were significantly higher after pre-treatment at 2, 5 and 8°C for 2 h than those of the control. Both longest longevity and maximum fecundity of adult beetles were observed at the rapid cold-hardening of 2°C. Our experiment implies that the cold-tolerance ability of O. communa can be rapidly increased after rapid cold-hardening treatments, which reveals an important ecological significance for population establishment and expansion of O. communa in the invaded areas of common ragweed.     

Food deprivation-dependent development and fecundity in Ophraella communa

Ophraella communa LeSage is native to North America and a biological control agent of the invasive weed Ambrosia artemisiifolia L. Since A. artemisiifolia plants grow old and die after September annually, O. communa suffers from food shortage. To understand the effect of food shortage or deprivation on population fitness of O. communa, the development and fecundity and hatchability of its progeny eggs were observed when larvae were offered A. artemisiifolia plants for either 3, 6, 12 or 24 hours daily. The results showed that larval food deprivation significantly influenced survival and developmental durations of larvae and pupae. Survival rates and developmental durations of larvae and pupae decreased and were prolonged significantly with decreasing time of larval daily food intake. Longevity and fecundity of adults shortened and decreased significantly with decreasing time of larval daily food intake. In addition, the hatch rates of progeny eggs decreased significantly with decreasing time of larval daily food intake. The present study suggests that food shortage is one of the most critical factors that suppresses O. communa populations. This can explain why field populations of the beetle decrease significantly with ageing and death of A. artemisiifolia plants after late September.     

Contemporary evolution of host plant range expansion in an introduced herbivorous beetle Ophraella communa

Host range expansion of herbivorous insects is a key event in ecological speciation and insect pest management. However, the mechanistic processes are relatively unknown because it is difficult to observe the ongoing host range expansion in natural population. In this study, we focused on the ongoing host range expansion in introduced populations of the ragweed leaf beetle, Ophraella communa, to estimate the evolutionary process of host plant range expansion of a herbivorous insect. In the native range of North America, O. communa does not utilize Ambrosia trifida, as a host plant, but this plant is extensively utilized in the beetle's introduced range. Larval performance and adult preference experiments demonstrated that native O. communa beetles show better survival on host plant individuals from introduced plant populations than those from native plant populations and they also oviposit on the introduced plant, but not on the native plant. Introduced O. communa beetles showed significantly higher performance on and preference for both introduced and native A. trifida plants, when compared with native O. communa. These results indicate the contemporary evolution of host plant range expansion of introduced O. communa and suggest that the evolutionary change of both the host plant and the herbivorous insect involved in the host range expansion.     

Geographical dispersion of ragweed leaf beetle (Ophraella communa) based on climatic and biological characters in the Palearctic habitats

1. The accidentally introduced ragweed leaf beetle (Ophraella communa) is a most promising biological control agent for common ragweed (Ambrosia artemisiifolia), which herbivore has already emerged in several areas of the Palearctic region.
2. The aim of our study was to model the expansion of O. communa and the number of generations in the various Palearctic regions. Furthermore, our objective was to determine the effect of the prevailing wind on the direction of its spread and to ascertain the relationship between the green biomass production of ragweed and individual numbers of this leaf beetle.
3. According to our meta-analytical findings, the advancement of O. communa is continuous in the Palearctic areas. This phytophagous insect invades new habitats, which are occupied by A. artemisiifolia, and spreads quickly. The stable populations of O. communa seem to be strictly linked to the presence of its primary host, A. artemisiifolia.
4. We show that the rapid spread of this insect is due to the combination of wind direction and topography features, which was reinforced by our analysis. O. communa possesses uniformly multivoltine populations in its Palearctic habitats. So, insects possessing facultative diapause are able to colonize northern areas depending on the presence of their host, which statement is based on the processing of 143 East- and 68 West-Palearctic records
5. According to our investigations, the mass appearance of this phytophagous insect coincided with the assimilation peak of its main host, common ragweed.

     

Population abundance and host use pattern of Ophraella communa (Coleoptera: Chrysomelidae) in its native and introduced range

We found that the abundance of Ophraella communa, a specialist herbivore of the invasive weeds Ambrosia artemisiifolia and A. trifida, is higher in the introduced range than in its native range. We also found that the native O. communa does not feed on A. trifida, but introduced O. communa does so extensively.     

Seasonal changes in cold hardiness of Ophraella communa

Insects can prepare themselves to tolerate subzero temperatures through various physiological changes, such as the alteration in body water or glycerol content. Indeed, it has been hypothesized that increasing glycerol body content has the benefit of decreasing the temperature necessary to freeze their body water and therefore increasing the supercooling point (SCP) and the cold hardiness. We here studied physiological plasticity in cold tolerance in Ophraella communa LeSage (Coleoptera: Chrysomelidae), a potential biological control agent of an invasive plant, the common ragweed, Ambrosia artemisiifolia L. (Asteraceae). Pupae of O. communa were collected from June to October, and the water and glycerol contents and the SCP of emerging adults were assessed. We found that SCP, water, and glycerol contents of beetles fluctuated significantly with season. Glycerol content of males and females increased with decreasing temperature between July and October, and glycerol content reached a maximum in October in the field. The lowest SCP was observed in adults in October prior to overwintering, and the highest SCP was evident in the summer population in July. Thus, cold hardiness of the beetles in the autumn population was significantly higher than in the summer population. We therefore conclude that cold tolerance, via changes in the relative composition of their body fluids and fats, is a plastic trait that can be influenced by fluctuations in abiotic factors (e.g., temperature) throughout the breeding season of the insect.     

Effect of humidity on the development and fecundity of <Emphasis Type="Italic">Ophraella communa</Emphasis> (Coleoptera: Chrysomelidae)

Ophraella communa, an unintentionally introduced leaf beetle in China, has good control efficiency on ragweed, Ambrosia artemisiifolia. Aspects of the climatic requirements for development, survival, longevity and fecundity of O. communa were studied under the conditions of constant temperature (25 ± 1°C), photoperiod of 14 L:10 D and three relative humidities (60%, 75% and 90% RHs). The results showed that the developmental periods of O. communa at different stages shortened along with the increasing relative humidity, except that of the pupal stage. Although no differences were observed in the pupal survival rate, ovipositional period, fecundity, longevity and adult female age-specific survivorship of O. communa under the three humidity conditions, the survival rates during the egg, larva and entire immature stage were significantly higher at 75% RH and 90% RH than at 60% RH. The innate rate of increase (r _m), net reproductive rate (R ₀), finite rate of increase (λ) reached the maximum at 75% RH, with values of 0.181, 1116.4 and 1.198, respectively. These results indicated that the optimum relative humidity for the development of O. communa ranged from 75% RH to 90% RH. Thus O. communa prefers moist microclimate habitats. Its population may expand rapidly during mid-May to late August in south, east and central China, when the humidity is relatively high.     

广聚萤叶甲成虫产卵行为及其产卵部位的选择性

【目的】明确广聚萤叶甲成虫产卵行为及其产卵部位的选择性。【方法】在室内条件下,对广聚萤叶甲成虫交配及产卵的系列行为、产卵场所选择、不同部位豚草植株叶片叶绿素b的含量进行了观察和测定:(1)将1对成虫放到养虫笼内的一株豚草上,观察交配时间,记录产卵数量、前后2粒卵之间的产卵时间间隔;(2)在均匀分为5部分(0～10、11～20、21～30、31～40和41～50 cm)的豚草植株上,随机放置10对成虫,观察雌虫对于产卵场所的选择。(3)将上述5个部位的豚草叶片通过丙酮匀浆法处理,用紫外分光光度计测定其在645和663 nm的吸光值,计算叶绿素b含量。【结果】广聚萤叶甲成虫完成一次成功交配平均需96.09 min。雌虫一般需45 min的时间来寻找其适应的产卵场所,在产卵过程中,成虫习惯将卵产于叶片背面,雌虫喜欢用口器来清理刚产下的卵粒。在一株50 cm高的豚草植株上,雌虫喜欢将卵产在植株中部21～30 cm和中上部31～40cm的叶片上(从下往上划分)。卵块数量和豚草不同部位叶片叶绿素b含量呈显著的正相关性。【结论】广聚萤叶甲成虫喜欢产卵在叶绿素b含量较高的叶片背面,可能以视觉识别叶片颜色来选择和定位产卵场所。     

An Experimental Test of Trade-Offs Associated with the Adaptation to Alternate Host Plants in the Introduced Herbivorous Beetle, <Emphasis Type="Italic">Ophraella communa</Emphasis>

The adaptation to alternate host plants of introduced herbivorous insects can be vital to agriculture due to the emergence of crop pests. Historically, it is assumed that there are trade-offs associated with the adaptation to new host plants; a generalist genotype that adapts to an alternate host is expected to have a relatively lower fitness on the ancestral host than a specialist genotype (physiological cost) or a relatively lower host-searching ability for the ancestral host plant (behavioral cost). In this study, we tested the costs of adaptation to a new host plant in the introduced herbivorous insect, Ophraella communa LeSage (Coleoptera: Chrysomelidae). In its native range (United States), O. communa feeds mostly on Ambrosia artemisiifolia L. (Asterales: Asteraceae) and cannot utilize the related species, Ambrosia trifida L. (Asterales: Asteraceae), as a host plant. On the other hand, the introduced O. communa population in Japan utilizes A. trifida extensively, and is adapting to it, both physiologically and behaviorally. We compared larval performance on the ancestral and alternate plants and adult host-searching ability between the native and introduced beetle populations. The introduced O. communa showed higher larval survival and adult feeding preference for the alternate host plant A. trifida than did the native O. communa, indicating that the introduced O. communa has rapidly adapted to the alternate host plant. However, there are no differences in either larval performance on the ancestral host A. artemisiifolia or host-searching accuracy between the native and introduced O. communa.     

Mating frequency positively associates with fitness in Ophraella communa

1. Why animals mate multiple times, owing to the lack of immediate fitness benefits, presents an intriguing problem for evolutionary biologists. Yet, the profusion of this behaviour suggests it must be maintained by natural selection via increased performance. 2. The possible benefits of multiple mating using the leaf beetles Ophraella communa LeSage, the biological control agent of the invasive common ragweed Ambrosia artemisiifolia L., were studied and the fitness consequences of single, twice, three, four, and unrestricted mating events were assessed. 3. Overall, it was observed that the number of copulation events was positively associated with fitness parameters of the insects. Insects performed the best under unrestricted mating regimes, with average increases of 48% in longevity, 75% in fecundity, and 55% in egg hatch rate. In addition, females that experienced unrestricted access to mates maintained very high viability over their entire reproductive lives. Nevertheless, insects also performed better when allowed to mate four times compared with once or twice. 4. The present findings thus support the hypothesis that multiple‐mating behaviour is maintained owing to increased fitness benefits in the current and the next generation. Selection for re‐mating is, therefore, expected in field populations, which is likely to happen naturally owing to the aggregate lifestyle of O. communa.     

Risk to nontarget plants from <Emphasis Type="Italic">Ophraella communa</Emphasis> (Coleoptera: Chrysomelidae), a potential biological control agent of alien invasive weed <Emphasis Type="Italic">Ambrosia artemisiifolia</Emphasis> (Asteraceae) in China

Ophraella communa LeSage is an oligophagous insect that shows promise for controlling the alien invasive weed Ambrosia artemisiifolia L. in China. This study was performed to evaluate the risk of O. communa on the basis of host-specificity testing of larval development under no-choice conditions and of oviposition preferences under choice conditions in greenhouses and in the open field. Under no-choice conditions, O. communa larvae experienced much higher mortality rates on the nontarget plants than on the target weed, but a small proportion of larvae completed development on the nontarget plants examined, including Xanthium sibiricum Patrin ex Widder, Helianthus tuberosus L., and H. annuus L. Multiple-choice tests indicated that O. communa showed a strong oviposition preference for the target weed over the nontarget plants and laid few eggs on the economically important Helianthus crops tested. In paired-choice trials, O. communa adults showed an obvious preference for the target weed over X. sibiricum but preferred X. sibiricum to H. annuus. The results suggest that X. sibiricum might be used as a lower-ranked host plant next to the target weed by O. communa, and that Helianthus crops would not be at risk of being used for oviposition in the field.     

Effect of short-term high temperature stress on the development and fecundity of Ophraella communa (Coleoptera: Chrysomelidae)

Since insects are ectothermic, they are highly vulnerable to the sudden increase of temperature. Indeed, it has been hypothesized that the survival, development, fecundity, and even population expansion of insects are all affected significantly by extremely high temperature. We studied the effect of short-term high temperature stress on the survival and development of different stages, adult longevity and fecundity of Ophraella communa (Coleoptera: Chrysomelidae), a biological control agent of the invasive plant, the common ragweed, Ambrosia artemisiifolia (Asterales: Asteraceae) in the laboratory. The results showed that egg, larval, pupal and adult survival rates were significantly affected after 2 hour-short-stress at high temperatures (35 to 47°C) when compared to the 28°C control. With the exceptions of the control and 35°C stress, survival rate of females was significantly higher than that of males after short-stress at any high temperature. Short-term high temperature stress also significantly impacted longevity and fecundity of adult beetles. Except for control, female longevity was significantly longer than male's after short-stress at any high temperature. The survival rates of different stages, and adult longevity and fecundity of the beetle decreased significantly with the increase of short-term stress temperature. Based on the results of the present study, we conclude that the development and population expansion of O. communa may be significantly affected when they are exposed to a high temperature stage in a summer day in the areas invaded by common ragweed, in southern China.     

Effects of high temperature on body size and weight of Ophraella communa

Ophraella communa LeSage (Coleoptera: Chrysomelidae) is an effective biological control agent of the invasive common ragweed, Ambrosia artemisiifolia L. Body size, one of the most important life-history characters for many insects, affects O. communa mating choice. Temperature is one of the most important factors on body size, especially high temperatures. Adult body lengths were significantly inhibited after eggs, larvae and pupae of O. communa experienced high temperature stresses. With exception of subsequent female body after exposure of larvae to high temperatures, the body weights of females and males were not affected by temperatures. Since adult insect fecundities are often in proportion to their body sizes, we concluded that high temperatures may influence the population expansion of O. communa in the field.     

Defoliation of common ragweed by Ophraella communa beetle does not affect pollen allergenicity in controlled conditions

Ragweed allergy is one of the primary causes of seasonal allergies in Europe and its prevalence is expected to rise. The leaf beetle Ophraella communa, recently and accidentally established in N-Italy and S-Switzerland, represents a promising approach to control ragweed, but negative side effects should be excluded before its use. Since biotic and abiotic stresses are known to influence the allergenicity of pollen, we set out to assess the effect of sub-lethal defoliation by O. communa on the quantity and quality of ragweed pollen. Seventeen sister pairs (including six clones) of ragweed plants were grown in controlled conditions. One of each pair was exposed to O. communa as soon as the plant started to produce reproductive structures. After 10 weeks of exposure, plant traits were measured as a proxy for pollen quantity. Pollen quality was assessed by measuring its viability and allergenicity. Generally, plants produced very few male flowers and little amount of pollen. Damage by the beetle was severe with most of the leaf tissue removed, but no treatment effect was found on any of the quantitative and qualitative traits assessed. In conclusion, O. communa did not increase the amount or allergenicity of ragweed pollen grains in our experimental conditions.     

Effects of morphological traits,age and copulation experience on mate choice in Ophraella communa

Ophraella communa is a biological control agent of invasive common ragweed, Ambrosia artemisiifolia. To understand the mate choice tactic of the beetle and improve mass-rearing of high-quality populations, the effects of morphological traits, age and copulation experience on mate choice in this beetle were studied in the laboratory. The results showed thatmate choice of male or female was related to certain adult morphological traits. Wing length, black streak width of frons and metaleg femur length of males were central to female mate choice. Females with longer wing length, black streak width of frons, pronotum width and foreleg tibia length were more attractive to males than those with the smaller ones. The chosen rate of older males was significantly higher than those of younger ones, and the chosen rate of females reached a maximum value on the 8th day after eclosion. The newly copulated females were less attractive to males than virgins, but females that have copulated in the distant past were more attractive than or were similar to virgins. The chosen rates of virgin males were significantly higher than those of newly copulated and 8 days past copulated ones, but no difference between virgin males and 3, 5 or 12 days past copulated ones in O. communa. The results of our study have added much needed empirical data regarding the significance of morphological traits, age and copulation experience as a source of variation in insect copulation signals. In addition, the results provide valuable information for mass-rearing of high-quality populations of O. communa.     

Changes in Defense of an Alien Plant Ambrosia artemisiifolia before and after the Invasion of a Native Specialist Enemy Ophraella communa

The evolution of increased competitive ability hypothesis (EICA) predicts that when alien plants are free from their natural enemies they evolve lower allocation to defense in order to achieve a higher growth rate. If this hypothesis is true, the converse implication would be that the defense against herbivory could be restored if a natural enemy also becomes present in the introduced range. We tested this scenario in the case of Ambrosia artemisiifolia (common ragweed) – a species that invaded Japan from North America. We collected seeds from five North American populations, three populations in enemy free areas of Japan and four populations in Japan where the specialist herbivore Ophraella communa naturalized recently. Using plants grown in a common garden in Japan, we compared performance of O. communa with a bioassay experiment. Consistent with the EICA hypothesis, invasive Japanese populations of A. artemisiifolia exhibited a weakened defense against the specialist herbivores and higher growth rate than native populations. Conversely, in locations where the herbivore O. communa appeared during the past decade, populations of A. artemisiifolia exhibited stronger defensive capabilities. These results strengthen the case for EICA and suggest that defense levels of alien populations can be recuperated rapidly after the native specialist becomes present in the introduced range. Our study implies that the plant defense is evolutionary labile depending on plant-herbivore interactions.