Mass rearing and augmentative releases of the native parasitoid Chouioia cunea for biological control of the introduced fall webworm Hyphantria cunea in China

The fall webworm, Hyphantria cunea Drury, is an economically important introduced pest in China. A native pupal endoparasitoid, Chouioia cunea Yang (Hymenoptera: Eulophidae, Tetrastichinae) causes considerable mortality of H. cunea pupae in some areas of China. Alternative hosts of C. cunea were tested to find potential substitute hosts for mass rearing the parasitoid. Antheraea pernyi Guerin-Meneville (Lepidoptera: Saturniidae) was chosen as a surrogate host as a single pupa produced an average of 6552 wasps and a maximum of 11,256 per pupa. A mass-rearing technique and successful release program of this parasitoid is described. Parasitism by C. cunea in the areas where it was released averaged 67.74% and was usually over 80%. Other native parasitoids, such as Coccygomimus disparis (Viereck), C. parnasae (Viereck) (Hymenoptera: Ichneumonidae) and Exorita japonica Townes (Diptera: Tachnidae), caused the total average parasitism to exceed 90% on average, reaching a maximum of 96.28% in the release areas. These successful releases indicate that an introduced pest species can also be controlled by the mass-rearing and release of native parasitoids in the country of introduction.     

重大外来入侵害虫——美国白蛾生物防治技术研究

美国白蛾Hyphantria cunea(Drury)是重大外来入侵害虫,对我国林业和园林绿化造成重大危害,尤其是近年来美国白蛾传入北京,严重威胁着我国“绿色奥运”的顺利举办和首都园林绿化及生态环境安全。根据美国白蛾多发生在居民区、乡镇和城市的特点,作者开展对环境安全的生物防治技术研究。汲取前苏联等国家从美国白蛾的原产地引进天敌进行生物防治没有成功的经验和教训,立足调查和寻找我国本土天敌。经过21年的努力,发现和筛选出白蛾周氏啮小蜂Chouioia cunea Yang(新属新种)这种寄生美国白蛾的特优天敌;研究这种小蜂的行为学、生态学、生物学、解剖学及人工大量繁殖、放蜂防治技术;筛选出人工大量繁殖小蜂的替代寄主,解决小蜂的大量繁殖的瓶颈问题;通过放蜂防治试验,取得良好的防治效果。同时,筛选出防治美国白蛾的高毒力HcNPV病毒毒株,研制出美国白蛾人工饲料,利用人工饲料大量饲养美国白蛾幼虫,然后接种扩增病毒,成功解决HcNPV病毒大量扩增生产和常年生产的技术难题,做到病毒的规模化生产和常年生产,保证大面积生产防治的需要和病毒质量。研究出利用天敌昆虫和病原微生物综合应用的防治模式:在美国白蛾幼虫期喷洒HcNPV病毒,蛹期释放白蛾周氏啮小蜂,达到既控制当代美国白蛾的危害,又有效抑制其下代的种群数量,取得长期的持续控制美国白蛾的防治效果。上海市、大连市、烟台市和青岛市利用该项技术已经完全控制美国白蛾,特别是上海市利用本项生物防治技术防治后,已经连续6年没有再发现美国白蛾。由于该项生物防治技术利用的是自然界原有的控制害虫的生态因子,因而对环境安全,做到既消灭害虫,又保证生态环境和人畜的安全,也保护生物多样性。该项研究成果也为北京采用“绿色”防治技术有效控制美国白蛾提供重要的科技支撑和技术保障。     

Mitochondrial DNA analysis of the introduced fall webworm, showing its shift in life cycle in Japan

The fall webworm, Hyphantria cunea (Drury) (Lepidoptera: Arctiidae), was introduced from North America into Japan in 1945. For the first three decades after its introduction, its life cycle was bivoltine. Thereafter, its life cycle shifted to trivoltine in south‐western areas of Japan. Two hypotheses have been proposed for the process that led to the shift in voltinism: one based on a single and the other on multiple independent colonizations. To test these hypotheses, mitochondrial (mt)DNA sequences were analyzed in the black‐headed type of 14 Japanese, one Korean and two North American populations of H. cunea. In addition, the same regions of mtDNA were compared with the red‐headed type of two North American populations. In the black‐headed type, mtDNA sequences were the same in all Japanese populations and in the Korean population, but sequences of the North American populations differed from each other and from those of the other populations. These results suggest that the process of the shift in voltinism occurred originally in Japan, and that the Japanese and the Korean population of H. cunea originated from a relatively small area in North America.     

Seasonal adaptations of the fall webworm <Emphasis Type="Italic">Hyphantria cunea</Emphasis> (Drury) (Lepidoptera: Arctiidae) following its invasion of Japan

The fall webworm, Hyphantria cunea (Drury) (Lepidoptera: Arctiidae), invaded Japan from North America about 60 years ago. Immediately after its invasion – and for the first three decades – its life cycle was bivoltine, two generations per year throughout its entire distribution in Japan. Thereafter, its life cycle shifted to trivoltine in the southwestern areas of Japan. In the present study we examined the life-history traits proposed to be implicated in this event with the aim of clarifying the mechanism of this life-cycle shift. The critical photoperiod for diapause induction, as defined by the photoperiod at which 50% of individuals enter diapause, was shorter in the trivoltine populations than in their bivoltine counterparts. The temperature sensitivity of the photoperiodic response, as defined by the difference in the critical photoperiod between 20 and 25°C, was greater in the trivoltine populations than in the bivoltine ones. The geographic variation in larval and pupal periods was positively correlated to the latitude of the original localities of the populations. The change in the number of larval instars would be one of the main factors accounting for the regional differences in the developmental period. These results suggest that some life-history traits of H. cunea have changed following its invasion of Japan as an adaptive response to local climates.     

Recent advances in biological control of important native and invasive forest pests in China

In recent decades, China has suffered severe attacks by both native and invasive forest pests. We have carried out a series of research projects on biological control of these pests. The fall webworm, Hyphantria cunea (Drury) (Lepidoptera: Arctiidae) has been sustainably controlled by an effective gregarious pupal endoparasitoid, Chouioia cunea Yang (Chalcidoidea: Eulophidae), which is native to China, and spraying HcNPV virus against the pest’s larval stage. Pine wilt disease, caused by the pine wood nematode (Bursaphelenchus xylophilus (Steiner et Buhrer) Nickle) (Aphelenchida: Aphelenchidae), is currently the number one pest in China. The strategy for controlling the disease is to manipulate the nematode’s vector, Monochamus alternatus Hope (Coleoptera: Cerambycidae). We discovered that Dastarcus helophoroides (Fairmaire) (Coleoptera: Bothrideridae) is the most important natural enemy in China pine forests. Mass rearing and release techniques were studied and developed. By releasing the parasitoid, 92.6% of the M. alternatus were parasitized in the first year. Meanwhile, three elaterid beetle species were found to prey on the larva of M. alternatus. The red turpentine beetle, Dendroctonus valens (LeConte) (Coleoptera:Scolytidae) was suppressed by a predator, Rhizophagus grandis Gyllenhal (Coleoptera: Rhizophagidae) introduced from Belgium and a total 3334 ha. of pine forests were protected. The oak longhorned beetle, Massicus raddei (Blessig) (Coleoptera: Cerambycidae) is the number one pest in the northeast forests of China, where it damages trunk of oaks, mainly Quercus liaotungensis and Q. mongolicus. An integrated management technique was developed for controlling the longhorned beetle: a special black light was invented for trapping the adults; the parasitoid Sclerodermus pupariae Yang et Yao (Hymenoptera: Bethylidae) was released against young larvae; and the parasitoid Dastarcus helophoroides eggs and/or adults were released when the hosts were mature larvae and/or pupae. By applying the technique for five years in northeastern China oak forests, the oak longhorned beetle has been controlled to a large extent. The emerald ash borer, Agrilus planipennis Fairmaire (Coleoptera: Buprestidae), is native to eastern Asia, including China, and feeding by larvae damages ash trees. Natural enemies of the emerald ash borer were investigated and seven species were found in China, of which Spathius agrili Yang (Hymenoptera: Braconidae), Tetrastichus planipennisi Yang (Hymenoptera: Eulophiae), Sclerodermus pupariae Yang et Yao and Oobius agrili Zhang et Huang (Hymenoptera: Encyrtidae) are predominant and have high potential for biocontrol of the pest. The biology, behavior, ecology and mass rearing techniques of the parasitoids were studied.     

Laboratory rearing and biological parameters of the eulophid Pnigalio agraules,a parasitoid of Cameraria ohridella

Predators as well as parasitoids native to Europe accept the exotic horse chestnut leafminer, Cameraria ohridella Deschka and Dimi? 1986 (Lepidoptera: Gracillariidae), either as prey or as host. However, the influence of these antagonists on the populations of the pest insect is so far very low. Therefore, efforts to develop an integrated pest management system against C. ohridella should include methods which foster the natural enemy complex. In the present study we developed a laboratory rearing method and investigated several biological parameters of Pnigalio agraules (Walker 1839) (Hymenoptera: Eulophidae), a dominant species in the horse chestnut leafminer’s parasitoid complex in many European regions. This native parasitoid satisfies three basic requirements for successful use as a biocontrol agent with regard to C. ohridella. The parasitoid’s fecundity, longevity and the speed of juvenile development by far exceeds that of the leafminer, enabling the parasitoid population to increase faster than that of the host. Furthermore, our results show that the impact of this species on C. ohridella populations has been previously underestimated, because non‐reproductive killing (i.e. host‐feeding and host‐stinging) of the hosts, resulting in considerable larval mortality of the leafminer, has not been quantitatively assessed. However, naturally occurring parasitoid populations have negligible impact on C. ohridella populations. Further studies, including experimental releases of P. agraules, are necessary to understand the constraints limiting the parasitoid’s performance in the field and to assess the potential benefits of releases for the control of C. ohridella.     

Geographic variation in critical photoperiod for diapause induction and its temperature dependence in Hyphantria cunea Drury (Lepidoptera: Arctiidae)

The fall webworm, Hyphantria cunea Drury (Lepidoptera: Arctiidae), was introduced from North America to Japan half a century ago. The critical photoperiod for diapause induction and its temperature dependence, as defined by the difference in the critical photoperiod between 20 and 25°C, were investigated in order to understand the mechanisms behind a shift from bi- to trivoltine life cycles. The critical photoperiod for diapause induction was shorter in the southern trivoltine populations than in the northern bivoltine populations, and this was more marked at 25°C than at 20°C. Although the critical photoperiod showed a positive correlation with the original latitude, the correlation was relatively low at both temperatures. Conversely, temperature dependence of the critical photoperiod for diapause induction correlated negatively with the original latitude. The trivoltine populations showed greater temperature sensitivity than the bivoltine populations. These results suggest that an increase in temperature sensitivity of the diapause response to photoperiods was involved in the shift to a trivoltine life cycle. The crossing experiments suggested that the photoperiodic control of diapause induction and its temperature dependence are under polygenic control without sex-linkage. Received: 29 October 1996 / Accepted: 26 February 1997     

Performance of Sclerodermus brevicornis,a parasitoid of invasive longhorn beetles,when reared on rice moth larvae

Biological control efficiency can be improved by developing effective mass‐rearing systems to produce large numbers of high‐quality parasitoids. This study explored an alternative host for rearing Sclerodermus brevicornis (Kieffer) (Hymenoptera: Bethylidae), a potential biocontrol agent for the suppression of exotic and invasive wood‐boring longhorn beetle (Coleoptera: Cerambycidae) populations in the European agroforestry ecosystems. We tested larvae of the rice moth, Corcyra cephalonica Stainton (Lepidoptera: Pyralidae), as host for the parasitoid. We quantified the probability and timing of host attack and parasitism as well as reproductive success, offspring production, and the characteristics of adult offspring. As S. brevicornis is a quasi‐social species (multiple females, communally produced offspring broods), we also explored the effects of varying the number of females to which individual hosts were presented, with the aim of determining the optimal female‐to‐host ratio. As time to host attack can be a limiting factor in S. brevicornis rearing protocols, we tested the use of adult females of another bethylid species, Goniozus legneri Gordh, to paralyse C. cephalonica larvae prior to presentation. We identified the conditions within our experiment that maximized offspring production per host and offspring production per adult female parasitoid. We found that C. cephalonica is suitable as a factitious host and, as it is considerably more straightforward for laboratory rearing than cerambycid species, it is a good candidate for adoption by future S. brevicornis mass‐rearing and release programmes.     

Dispersal patterns of exotic forest pests in South Korea

Abstract Invasive species have potentially devastating effects on ecological communities and ecosystems. To understand the invasion process of exotic forest pests in South Korea, we reviewed four major species of exotic forest pests: the pine needle gall midge (Thecodiplosis japonensis), pine wilt disease caused by the pine wood nematode (Bursaphelenchus xylophilus), the fall webworm (Hyphantria cunea) and the black pine bast scale (Matsucoccus thunbergianae). We consider their biology, ecology, invasion history, dispersal patterns and related traits, and management as exotic species. Among these species, the dispersal process of fall webworm was linear, showing a constant range expansion as a function of time, whereas the other three species showed biphasic patterns, rapidly increasing dispersal speed after slow dispersal at the early invasion stage. Moreover, human activities accelerated their expansion, suggesting that prevention of the artificial movement of damaged trees would be useful to slow expansion of exotic species. We believe that this information would be useful to establish management strategies for invasion species.     

营养对不同地理种群周氏啮小蜂生物学特性的影响

【目的】研究补充营养对周氏啮小蜂海南本土地理种群和北京地理种群的生物学参数是否有差异。【方法】设置不同的营养(10%蜂蜜、10%蔗糖、10%葡萄糖、水、空白)分别饲喂周氏啮小蜂,统计2个地理种群的寄生率、羽化率、出蜂量、寿命。【结果】2个地理种群的周氏啮小蜂羽化后不久即可进行交配,补充10%蜂蜜、10%蔗糖、10%葡萄糖能显著提高2个地理种群的寄生率、羽化率、出蜂量、雌雄蜂寿命,补充不同的营养对两个地理种群的雌雄比、发育历期的影响差异不显著;饲喂10%蜂蜜的海南地理种群寄生率最高(84.60%),饲喂10%葡萄糖的海南地理种群羽化率最高(97.47%),饲喂10%葡萄糖的海南地理种群出蜂量最高(60.03头),饲喂10%葡萄糖的海南地理种群雌、雄蜂的寿命均为最高,分别为9.13和8.53d。营养和地理种群的交互作用对周氏啮小蜂雄蜂的寄生率、羽化率、出蜂量、雌雄比、雌雄蜂寿命具有显著影响,而对周氏啮小蜂的发育历期无显著影响。【结论】补充营养可不同程度促进周氏啮小蜂生殖力、寿命及寄生率,对寄生蜂繁育和利用其进行生物防治具有一定的意义。     

北京地区美国白蛾时空分布变化及其影响因素

美国白蛾是我国农林对外重大检疫对象之一，已经对我国的生态和经济造成了巨大损失，且十分难以防治。基于地统计学和地理信息系统原理，通过半变异函数分析，选取最优拟合模型，利用克里金插值法对2008-2016年北京地区美国白蛾的种群时空分布特征进行制图，并结合气象数据，运用冗余分析探究了美国白蛾种群动态变化与气候因子的关系。结果表明：（1）空间特征上，美国白蛾种群呈现聚集分布，分布趋势为东部、南部高，西部、北部少，主要集中在海拔400m以下的地区；（2）时间特征上，北京地区的美国白蛾种群一年3代，单年内越冬代数量远大于第一代和第二代，第一代和第二代种群数量相近，到次年越冬代种群数量回升，依此呈现周期性变化；（3）冗余分析结果显示影响北京地区美国白蛾种群变化与3月份平均相对湿度、7月份平均气温、上一年8月份最高温度呈正相关关系，与2月份日照时数、4月份最高温度、上一年9月份最低温度呈负相关关系；（4）插值结果表明在北京东部和南部边界与河北省交界处分布有一个较大的美国白蛾种群，能够影响该地区的美国白蛾种群数量。     

Host plant, host plant chemistry and the polyembryonic parasitoid Copidosoma sosares: indirect effects in a tritrophic interaction

Host plant identity and host plant chemistry have often been shown to influence host finding and acceptance by natural enemies but comparatively less attention has been paid to the tritrophic effects of host plant and host plant chemistry on other natural enemy fitness correlates, such as survivorship, clutch size, body size, and sex ratio. Such studies are central to understanding both the selective impact of plants on natural enemies as well as the potential for reciprocal selective impact of natural enemies on plant traits. We examined the effects of host plant and host plant chemistry in a tritrophic system consisting of three apiaceous plants (Pastinaca sativa, Heracleum sphondylium and H. mantegazzianum), the parsnip webworm (Depressaria pastinacella) and the polyembryonic parasitic wasp Copidosoma sosares. All of these plants produce furanocoumarins, known resistance factors for parsnip webworms. Furanocoumarin concentrations were correlated neither with the presence nor the number of webworms on a given plant. Concentrations of two furanocoumarins were negatively associated with C. sosares fitness correlates: isopimpinellin with the likelihood that a given webworm would be parasitized and xanthotoxin with both within‐brood survivorship (of all‐male and mixed‐sex broods) and clutch size. Brood sex ratio and body sizes of individual wasps were not correlated with furanocoumarin chemistry. Because additive genetic variation exists in P. sativa for furanocoumarin chemical traits, these are subject to selection by webworms through herbivory. Third trophic level selective impacts on furanocoumarin traits may include selection for reduced production of those chemicals that affect parasitoid survivorship yet do not influence host plant choice by the herbivore. That such might be the case is suggested by patterns of furanocoumarin production in populations of P. sativa with different histories of infestation; in the Netherlands, where parasitism rates of webworms by C. sosares are high, plants produce lower levels of all linear furanocoumarins and proportionately less isopimpinellin than do midwestern U.S. populations of P. sativa, where natural enemies of the webworm are effectively absent.     

Survey of the native insect natural enemies of Hyphantria cunea (Drury) (Lepidoptera: Arctiidae) in China

The fall webworm, Hyphantria cunea (Drury) (Lepidoptera: Arctiidae), is an invasive and important pest in China. Investigations on insect natural enemies have been conducted from 1996 to 1999 in five provinces and one municipality of China in order to select effective species for biological control. Two carabid predators (Coleoptera) and 25 parasitoid species were found, among which 23 were parasitic wasps (Hymenoptera), including five hyperparasitic species and two tachinid flies (Diptera). The two carabids preyed on young larvae inside webs, two braconid wasps parasitized larvae, and 18 parasitoid species attacked the fall webworm during the pupal and/or 'larval-pupal' stages. Among these parasitoids, there were one genus and nine species that are new to science and four species new to China, which were described and published by the senior author Yang. The average parasitism rates of fall webworm pupae were 25.8% and 16.1% in the overwintering generation and the first generation (summer generation), respectively. These findings reveal that these natural enemies play an important role in the natural control of the pest. Chouioia cunea Yang (Hymenoptera: Eulophidae), a gregarious pupal endo-parasitoid, was recommended as a promising biological control agent against the fall webworm in China.     

No inbreeding depression in laboratory‐reared individuals of the parasitoid wasp Allotropa burrelli

Inbreeding depression is a major concern in almost all human activities relating to plant and animal breeding. The biological control of pests with natural enemies is no exception, because populations of biocontrol agents experience a series of bottlenecks during importation, rearing, and introduction. A classical biological control program for the Comstock mealybug Pseudococcus comstocki (Hemiptera: Pseudococcidae) was initiated in France in 2008, based on the introduction of an exotic parasitoid, Allotropa burrelli Mues. (Hymenoptera: Platygastridae), a haplodiploid parasitoid imported from Japan. We evaluated the sensitivity of A. burrelli to inbreeding, to optimize rearing and release strategies. We compared several morphological and life‐history traits between the offspring of siblings and the offspring of unrelated parents. We took into account the low level of genetic variability due to the relatively small size of laboratory‐reared populations by contrasting two types of pedigree: one for individuals from a strain founded from a single field population, and the other generated by hybridizing individuals from two strains founded from two highly differentiated populations. Despite this careful design, we obtained no evidence for a negative impact of inbreeding on laboratory‐reared A. burrelli. We discussed the results in light of haplodiploid sex determination and parasitoid mating systems, and classical biological control practices.     

European field collections and Canadian releases ofCeranthia samarensis (Dipt.: Tachinidae), a parasitoid of the gypsy moth

A programme to collect, import and release into Canada the gypsy moth parasitoid,Ceranthia samarensis (Diptera: Tachinidae) is described. The parasitoid's potential for biological control in Canada is also discussed. The parasitoid was collected in Europe by exposing experimental gypsy moth larvae in areas where local gypsy moth populations were at low densities. Following field exposure, the host larvae were returned to the laboratory and parasitoids reared from them. This technique has shown thatC. samarensis is the suffers 7–16% hyperparasitism. From 83–90% of theC. samarensis typically enter diapause as pharate adults within the puparia. Laboratory tests of post-exposure host rearing conditions indicate that constant temperatures disrupt the normal parasitoid diapause and that this effect can not be offset by use of either static long or short photoperiods or natural daylengths. Shipping and cold-storage procedures for puparia are described. Post-storage time to emergence of adultC. samarensis decreased with longer cold storage periods and with higher post-storage incubation temperatures. Emergence requires 112 degree-days above a threshold of 8°C after a period of at least 8 months cold storage. Releases of adultC. samarensis into field cages at four locations in southern Ontario are documented. While dissection of host larvae from the field cages has failed so far to demonstrate evidence of parasitism, we remain hopeful that some establishment of the parasitoid has occurred.      

Potential for lab rearing of <Emphasis Type="Italic">Apanteles taragamae</Emphasis>, the larval endoparasitoid of coconut pest <Emphasis Type="Italic">Opisina arenosella</Emphasis>, on the rice moth <Emphasis Type="Italic">Corcyra cephalonica</Emphasis>

A lab rearing technique was standardised for Apanteles taragamae Viereck (Hymenoptera: Braconidae), the early larval parasitoid of the coconut leaf-eating caterpillar, Opisina arenosella Walker on the alternate host Corcyra cephalonica Stainton (Lepidoptera: Pyralidae). The parasitoid took 23.3 ± 3.2 days to complete the egg to adult period. Adult longevity for males and females was 15.3 ± 4.6 and 13.8 ± 4.6 days respectively. Fecundity was 14.8 ± 4.3 eggs per female. The percentage parasitism was 60.6 ± 5.7 on the alternative host C. cephalonica and 64.6 ± 5.5 on the natural host O. arenosella. Eight- to ten-day-old caterpillars were the ideal stage of C. cephalonica for rearing A. taragamae. The results indicated the amenability of rearing A. taragamae on C. cephalonica in the laboratory.     

Bionomics of Opius bellus (Hymenoptera: Braconidae), an endoparasitoid of Anastrepha fraterculus (Diptera: Tephritidae) in fruit-growing areas of Northwestern Argentina

Opius bellus is a neotropical larval-prepupal parasitoid known to attack the pestiferous fruit fly, Anastrepha fraterculus. Due to interest in the use of native parasitoids in forthcoming fruit fly biocontrol programmes in Argentina, O. bellus was colonised for the first time using laboratory-reared A. fraterculus larvae. A series of experiments were conducted to (1) best achieve an efficient parasitoid rearing by determining optimal larval host age, host:parasitoid ratio and host exposure time and (2) assess their potential as biological control agents by determining reproductive parameters. The most productive exposure regimen was: 7–9 d-old (early and middle third-instars) A. fraterculus larvae for 4 h at a 4:1 host:parasitoid ratio; this array of factors was sufficient to achieve the highest average adult emergence (48%) and an offspring sex ratio at equitable proportion. Increasing both host:parasitoid ratio further than 4:1 and the host exposure time beyond 4 h did not significantly enhance parasitoid female offspring yield. Females produced eggs for 29.5 ± 1.4 days. At 32 days of age, 50% of the females were still alive. The majority of the progeny were produced by females between 20 and 24 d-old. At 26°C, gross fecundity rate, net reproductive rate, intrinsic rate of increase and mean generation time were 20.7 ± 4.2 offspring/female, 9.6 ± 2.5 females/newborn females, 0.06 ± 0.01 females/female/day and 8.4 ± 0.2 days, respectively. The long lifespan and reproductive parameters suggest that this parasitoid species has suitable attributes for mass-rearing.