Potential host fruits for Drosophila suzukii: olfactory and oviposition preferences and suitability for development

Drosophila suzukii (Matsumura) (Diptera: Drosophilidae), the spotted wing drosophila, is a pest endemic to Southeast Asia that invaded the Americas and Europe in 2008. In contrast to most of its congeners, D. suzukii possesses a serrated ovipositor that allows it to lay eggs in unwounded commercial fruits, resulting in severe revenue losses for the industry. The purpose of this study was to determine the susceptibility of known host fruits, including cherry, strawberry, blueberry, and grape, and potential host fruits, such as banana and apple, to attack by D. suzukii. Based on the responses to volatile cues offered in a six‐choice olfactometer, the preference of female D. suzukii was ranked in the following order: strawberry = cherry > banana = apple = blueberry = grape, but in no‐choice and choice oviposition tests, the preferences were ranked as follows: cherry > strawberry = blueberry > grape = banana > apple. Furthermore, we reconfirmed that D. suzukii mainly targets rotten fruit for feeding and ripe fruit for oviposition, and females preferred fruits with intensive mechanical damage. Based on developmental parameters, apple was the least suitable host. This study has implications for the control of D. suzukii, especially in mixed fruit orchards, by providing a promising avenue for exploiting behaviour‐based control tools and emphasizing the importance of phenology in host fruit susceptibility.     

Susceptibility of cold hardy grapes to Drosophila suzukii (Diptera: Drosophilidae)

Drosophila suzukii (Diptera: Drosophilidae), known commonly as spotted wing drosophila, is a vinegar fly originating from South‐East Asia and a major pest to many soft‐skinned fruits. Due to the species recent arrival in North America in 2008, many fruit varieties are yet untested for susceptibility to infestation. While previous work has focused on Vitis vinifera, this study aimed to determine grape susceptibility of cold hardy varieties based on hybrids of V. labrusca, V. riparia and V. vinifera. Field sampling was conducted in Southern Wisconsin (USA) vineyards to establish adult and larval abundance and determine whether the number of adults caught in traps correlates with fruit infestation. Host susceptibility was further assessed through no‐choice bioassays of both intact and damaged fruits. The field study found D. suzukii adults present in all varieties, low larval abundance and no correlation between adult abundance and larval presence. Peak adult abundance occurred mid‐season between veraison and harvest, while larval infestation rates were highest near harvest. In laboratory no‐choice tests, significantly more eggs, larvae and adults occurred in damaged than undamaged grapes. In damaged grapes, larvae and adult abundance was comparable between varieties and to the highly susceptible control of undamaged raspberry; however, D. suzukii developed significantly faster in raspberry than grapes. Fruit characteristics (°Brix, titratable acidity, pH) in grapes were uncorrelated with D. suzukii performance. Together, these findings suggest that cold hardy grapes are overall resistant to D. suzukii if intact and highly susceptible if damaged.     

Metagenomic analysis reveals changes of the Drosophila suzukii microbiota in the newly colonized regions

The spotted wing drosophila, Drosophila suzukii (Matsumura) (Diptera: Drosophilidae) is a highly polyphagous pest of a wide variety of wild or cultivated berry and stone fruit. Originating from Southeast Asia, it has recently invaded a wide range of regions in Europe and North America. It is well known that insect microbiotas may significantly influence several aspects of the host biology and play an important role in invasive species introduction into new areas. However, in spite of the great economic importance of D. suzukii, a limited attention has been given so far to its microbiota. In this study, we present the first in‐depth characterization of gut bacterial diversity from field (native and invasive range) and lab‐reared populations of this insect. The gut bacterial communities of field insects were dominated, regardless of their origin, by 2 families of the phylum Proteobacteria: Acetobacteraceae and Enterobacteriaceae, while Firmicutes, mainly represented by the family Staphylococcaceae, prevailed in lab‐reared population. Locality was the most significant factor in shaping the microbiota of wild flies. Moreover, a negative correlation between diversity and abundance of Enterobacteriaceae and the time elapsed since the establishment of D. suzukii in a new region was observed. Altogether our results indicate that habitat, food resources as well as the colonization phase of a new region contribute to shape the bacterial communities of the invasive species which, in turn, by evolving more quickly, could influence host adaptation in a new environment.     

Drosophila suzukii in Michigan vineyards,and the first report of Zaprionus indianus from this region

Drosophila suzukii is a new invasive pest that in recent years has become established in the Great Lakes region of the United States. Understanding the level of infestation in potentially susceptible crops is an important first step for planning appropriate management responses. This study was conducted in 2010–2012 to determine the infestation potential of this pest in native Vitis labrusca, French hybrid and V. vinifera grape cultivars grown in Michigan vineyards. Drosophila suzukii adults were reared out of collected grape samples in all 3 years, comprising a low proportion of all emerged drosophilids in each of the years. This trend was also found in vacuum sampling, conducted in 2011, with the majority of flies collected being non‐D. suzukii drosophilids. Another recently introduced invasive fly species, Zaprionus indianus, was also reared out of grape samples collected in 2012. While the results of this study indicate no immediate threats to commercial grape production from D. suzukii, further research is needed to elucidate possible secondary effects that this species may have on vineyards, such as the introduction of diseases to the fruit.     

Screening of 25 different natural crop protection products against Drosophila suzukii

Drosophila suzukii is a major pest of soft‐skinned fruits, and insecticides are often used to prevent fruit damage caused by oviposition. As D. suzukii produces many generations per year, repeated insecticide applications are required. Furthermore, D. suzukii attacks ripening and ripe fruits shortly before harvest. Therefore, the use of synthetic insecticides is limited by long pre‐harvest intervals and maximum residue limits. To be able to offer producers immediate and sustainable solutions, we tested 25 natural crop protection products with three different application methods in a laboratory screening. We show that application method is an important factor for the efficacy of the tested products. Of six natural insecticides, only Spinosad was toxic for D. suzukii and reduced the oviposition on treated blueberries. The tested oil products had no control effect and products based on different entomopathogenic fungi and Bacillus thuringiensis rather enhanced oviposition. Mineral products (Kaolin, CaCO₃, Ca(OH)₂ and clinoptilolith) applied as spray solutions were not toxic, but significantly reduced oviposition on blueberries. We provide the first study in which different application methods have been used to compare numerous, commercially available, natural crop protection products with different modes of action against adult D. suzukii. Our findings provide consultants and producers with important insights for the development of sustainable pest control strategies against D. suzukii.     

Behavioral evidence for contextual olfactory‐mediated avoidance of the ubiquitous phytopathogen Botrytis cinerea by Drosophila suzukii

Herbivorous insects may benefit from avoiding the smell produced by phytopathogens infecting plant host tissue if the infected tissue reduces insect fitness. However, in many cases the same species of phytopathogen can also infect host plant tissues that do not directly affect herbivore fitness. Thus, insects may benefit from differentiating between pathogen odors emanating from food and nonfood tissues. This is based on the hypothesis that unnecessarily staying attentive to pathogen odor from nonfood tissue may incur opportunity costs associated with not responding to other important survival functions. In this study adults of Drosophila suzukii Matsumura, an invasive larval frugivore, showed reduced attraction to the odor of raspberry fruit, a food tissue, when infected with Botrytis cinerea Pers., a ubiquitous phytopathogen, in favor of odors of uninfected raspberry fruit. Moreover, D. suzukii oviposited fewer eggs on infected raspberry fruit relative to uninfected raspberry fruit. Larval survival and adult size after eclosion were significantly reduced when reared on B. cinerea‐infected raspberry relative to uninfected fruit. Interestingly, when the behavioral choice experiment was repeated using Botrytis‐infected vs. ‐uninfected strawberry leaves, a nonfood tissue, in combination with fresh raspberry fruit, odor from B. cinerea‐infected leaves did not reduce D. suzukii attraction to raspberries relative to raspberries with uninfected leaves. These behavioral results illustrate the important role context can play in odor‐mediated interactions between insects, plants and microbes. We discuss implications of our findings for developing a repellent that can be useful for the management of D. suzukii.     

Olfactory responses of Drosophila suzukii females to host plant volatiles

Drosophila suzukii Matsumura, an endemic pest in southeast Asia, has invaded Europe and the U.S.A. Unlike most of its closely related sibling species, the serrated ovipositor of D. suzukii permits ovipositing in undamaged fresh fruits. In the present study, volatiles are identified from host plants that are potentially involved in D. suzukii host recognition and oviposition behaviour. It is shown that mated females are attracted to volatiles emitted from intact fruits. The antennally‐active suite of compounds released from the fresh fruits is identified by gas chromatography coupled with electroantennographic detection, as well as gas chromatography‐mass spectrometry. In olfactometer bioassays, mated females are significantly attracted to an electroantennographically active volatile, isoamyl acetate, when tested at 10 µg of synthetic compound in a rubber septa, which has a release rate comparable to that of fresh fruits. In addition, a genomic survey shows that D. suzukii not only possesses the full repertoire of genes encoding odorant receptors activated by isoamyl acetate in D. melanogaster, but also that one of the genes, OR67a, is represented by five duplicated copies. These results indicate that D. suzukii uses olfactory cues to select oviposition sites. The identification of volatiles emitted by host fruits that attract D. suzukii may aid in the development of a selective and efficient synthetic lure for monitoring this pest. As a close relative of Drosophila melanogaster, D. suzukii provides a unique opportunity for understanding the physiological mechanisms involved in the shift of this species from use of rotten to ripe fruits for oviposition.     

Spotted wing drosophila (Drosophila suzukii) utilization and dispersal from the wild host Asian bush honeysuckle (Lonicera spp.)

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水果害虫斑翅果蝇体内微生物菌群研究进展

斑翅果蝇是一种在全球范围内造成危害的重要水果害虫,其主要分布于亚、美、欧三大洲。斑翅果蝇的产卵器可以刺破水果表皮,将卵产在未完全成熟的水果中,卵孵化为幼虫后,幼虫取食水果,直接降低产量,从而对水果产业造成损失。近年以来,越来越多的研究表明昆虫微生物对宿主昆虫影响很大。例如昆虫微生物可以调控寄主昆虫的生长发育、个体适应性及生殖等。昆虫与其共生微生物间的关系成为昆虫生物学研究的热点内容。本文综述了近些年关于斑翅果蝇微生物多样性的研究,探讨了微生物菌群及内共生菌Wolbachia对斑翅果蝇生长发育、行为、生殖、抗病毒等的影响,以便为寻找控制斑翅果蝇种群的策略提供参考依据。     

Six cryptic species on a single species of host plant: morphometric evidence for possible reproductive character displacement

Abstract 1. Diversification of some highly host‐specific herbivorous insects may occur in allopatry, without shifts in host use. Such allopatric divergence may be accelerated by sexual selection operating on courtship displays. Wing size and shape may affect visual and vibrational courtship displays in tephritid fruit flies. Geometric morphometric methods were used to examine wings of six sympatric cryptic species in the neotropical genus Blepharoneura. All six species feed on flowers of the same species of host (Gurania spinulosa), a neotropical vine in the Cucurbitaceae. Three of the fly species court and mate in close proximity on the host. Thus, courtship behaviours could serve as important reproductive isolating mechanisms. Two sets of hypotheses were tested: (i) species differ in wing shape and wing size; and (ii) species are sexually dimorphic in wing size and wing shape. Wing size differed among a few species, but wing shape differed significantly among all six species. Sexual dimorphism in wing size was found in only one species, but sexual dimorphism in wing shape was found in two of the three species known to court on the same host plant. In the two sexually dimorphic species, wing shape differed among males, but not among females. This suggests that selection for reproductive character displacement might accelerate divergence in wing shape.     

Capacity of Japanese Asobara species (Hymenoptera; Braconidae) to parasitize a fruit pest Drosophila suzukii (Diptera; Drosophilidae)

Drosophila suzukii is a pest of soft fruit such as cherry, strawberry or blueberry and recently colonized North America and Europe from Asia. In this study, we assessed the utility of Japanese Asobara species as agents for the biological control of this pest species by examining their host use in nature and their capacity to parasitize this pest species. From Japan, eight Asobara species including putative three undescribed species were found; Asobara japonica was recorded from all over Japan, Asobara tabida from high altitude areas in central and northern Japan, Asobara rossica and Asobara rufescens from central to northern Japan, three undescribed species from central to western or southern Japan and Asobara pleuralis from a subtropical island of Japan. Among them, an undescribed species Asobara sp. TK1 may be useful as an agent for the biological control because it was recorded only from D. suzukii. All of the remaining seven species were generalists mainly using drosophilid species associated with fermenting fruits, and four of them had no or very low abilities to parasitize D. suzukii, indicating that these seven species are not or less appropriate as agents for biological control.     

Influences of blackberry margins on population dynamics of Drosophila suzukii and grape infestation in adjacent vineyards

Understanding the dynamics of pest insect populations in relation to the presence of non‐crop habitats and infestation levels of adjacent crops is essential to develop sustainable pest management strategies. The invasive pest species Drosophila suzukii (Diptera: Drosophilidae) is able to utilize a broad range of host plants. In viticulture, scientific risk assessment for D. suzukii has only recently started and studies assessing the effects of field margins containing wild host plants on D. suzukii population dynamics and on infestation risks in adjacent vineyards are lacking. Thus, in a one‐year field study, the role of different field margins on fly abundance and crop infestation in adjacent vineyards of Vitis vinifera, variety “Pinot Noir,” were investigated. Different monitoring methods were conducted to assess fly distribution, sex ratio and grape infestation in 14 vineyards adjacent to field margins containing either blackberry (BB) Rubus spp. or non‐host (NH) plants. Our results show that blackberries strongly enhanced D. suzukii abundance within field margin vegetation all year long, whereas fly abundance in vineyards adjacent to BB margins was just enhanced in some seasonal periods. Moreover, the influence of BB margins was limited by distance. However, high fly numbers in BB field margins did result in zero egg infestation of “Pinot Noir” berries. These results may have important implications for winegrowers to make efficient management decisions: regardless of high abundance of adult D. suzukii, only grape berry monitoring can assess the actual infestation risk and the potential need to take management action.     

A review on temperature and humidity effects on Drosophila suzukii population dynamics

1. Drosophila suzukii is an invasive polyphagous pest of wild and cultivated soft‐skinned fruits, which can cause widespread economic damage in orchards and vineyards.
2. The simulation and prediction of D. suzukii's population dynamics would be helpful for guiding pest management. Therefore, we reviewed and summarized the current knowledge on effects of air temperature and relative humidity on different life cycle parameters of D. suzukii.
3. The literature summary presented shows that high oviposition rates can occur between 18 and 30 °C. Temperatures between 16 and 25 °C resulted in fast and high egg‐to‐adult development success of more than 80%. Oviposition and adult life span were positively affected by high relative humidity; however, the factor humidity is so far rarely investigated.
4. We assume that this is one reason why relative humidity usually is not considered in modelling approaches, which are summarized herein. The high number of recently published research articles on D. suzukii's life cycle suggests that there is already a lot of knowledge available on its biology. However, there are still considerable research gaps mentioned in the literature, which are also summarized herein.
5. Nevertheless, we conclude that sufficient temperature data in the literature are suitable to understand and predict population dynamics of D. suzukii, in order to assist pest management in the field.

     

Diet quality mitigates intraspecific larval competition in Drosophila suzukii

The invasive frugivore Drosophila suzukii (Matsumura) (Diptera: Drosophilidae) utilizes a wide range of host plants and damages important fruit crops, including blueberries, cherries, blackberries, raspberries, and strawberries. Field infestations of D. suzukii often exceed one larva per berry, suggesting that intraspecific competition may frequently occur. Because dietary resources are also likely to vary across the host range of D. suzukii, we designed a laboratory assay to measure larval performance across diets of varying quality: a standard artificial diet, a fruit‐based medium, a low‐protein, and a low‐carbohydrate diet. We manipulated egg density across these diets to provide increasing levels of competition and measured larval performance by observing survival to pupation and adulthood, and development times for both life stages. Although increasing density generally negatively impacted D. suzukii performance across diets, the magnitude of these impacts varied by diet type. Drosophila suzukii performance was generally similar in fruit and standard diets, although larval development was more rapid in fruit diets at lower densities. Even at low densities (5 or 10 eggs per arena), survival was reduced and development time increased in low‐protein diets relative to standard and fruit diets. At the two highest larval densities (20 or 40 eggs per arena), survivorship was reduced in low‐carbohydrate diets as compared to standard and fruit diets. There is evidence that larvae compensated in both low‐quality diets by extending development time, which could have consequences for population dynamics. Population models for use in D. suzukii management may need to account for both host nutritional quality and relative competition to accurately predict turnover and geographic expansion.     

Invasive host for invasive pest: when the Asiatic cherry fly (Drosophila suzukii) meets the American black cherry (Prunus serotina) in Europe

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Life‐history trade‐offs under different larval diets in Drosophila suzukii (Diptera: Drosophilidae)

Most larval drosophilids eat the microorganisms that develop in rotting fruit, a relatively protein‐rich resource. By contrast, the spotted‐wing Drosophila suzukii Matsumara (Diptera: Drosophilidae) uniquely develops in ripening fruit, a protein‐poor, carbohydrate‐rich resource. This shift in larval nutritional niche has led to D. suzukii being a significant agricultural pest in the U.S.A. and Europe. Although occupying a new niche may benefit a species by reducing competition, adaptation in host use may generate trade‐offs affecting fitness. To test the hypothesis that fitness trade‐offs will change with adaptation to novel larval diets, D. suzukii larval development on either a diet of a fresh, ripe blueberry (a natural host) or standard artificial Drosophila media (protein‐rich) is compared and the effect of diet on development time from egg to adult, adult body size and male wing spot area, and female fecundity is assessed. Larval development time differs, with larvae on the blueberry emerging as adults earlier than those on the artificial medium, although other fitness measures do not vary between the two diets. In addition, the faster development time on a blueberry does not trade off with body size as expected, although early fecundity is delayed in females that develop on blueberries. Thus, adaptation to a novel larval diet environment does not come at a cost to the ability to develop in protein‐rich resources.     

Seasonal monitoring of Drosophila suzukii and its non-crop hosts in Wuhu,Eastern China

Drosophila suzukii (Matsumura) (Diptera: Drosophilidae) is a serious pest that prefers fresh fruits and is native to Southeast Asia. In our study, apple cider vinegar bait traps were used to capture and monitor the population dynamics of this native pest in Wuhu City, China, from May/June 2017 to May 2018. The research was conducted at 15 locations in two fruit orchards in Wuhu. Traps caught more adults in general in a Meiling blueberry orchard than in a Xicun mixed orchard, and the highest trap counts occurred near harvest time (October). Females had more mature eggs from September to November, and the number of mature eggs declined thereafter. We found several non-crop hosts, which can provide food and reproductive resources for D. suzukii and are common in forests and field margins. By comparing the number of captured adults in the Meiling and Xicun orchards, we found that blueberry was preferred by D. suzukii among the fruits in our search. Fruit ripening times differed among crops; therefore, fly populations moved between crop and non-crop habitats during the year or had varying population dynamics on different crops in different seasons. The D. suzukii population and the number of mature eggs decreased in summer and winter but increased in spring and autumn. Drosophila suzukii had higher survival rates with blueberry than those with other fruits, and D. suzukii could use four non-crop species growing around the orchards as host plants.     

Effects of sweet alyssum flowers and their volatile compounds on Drosophila suzukii (Matsumura) in the laboratory

Drosophila suzukii (Matsumura) is a major global pest of soft fruit crops. Based on field observations, we tested in the laboratory whether sweet alyssum (Lobularia maritima (L.)) flower volatiles and their major constituent compounds, acetophenone and benzaldehyde, repelled D. suzukii flies. Volatiles from cut flowers and acetophenone reduced numbers of D. suzukii attracted to raspberries, and acetophenone reduced numbers of larvae in the raspberries. Testing of sweet alyssum plantings or dispensing acetophenone to repel D. suzukii in fields and lower fruit infestation should be conducted.     

Nutritional geometry and fitness consequences in Drosophila suzukii,the Spotted‐Wing Drosophila

Since its arrival to North America less than a decade ago, the invasive Spotted‐Wing Drosophila (Drosophila suzukii) has inflicted substantial economic losses on soft fruit agriculture due to its ability to oviposit into ripening fruits. More effective management approaches for this species are needed, but little is known about the factors that influence behavioral choices made by D. suzukii when selecting hosts, or the consequences that their offspring experience when developing in different environments. Using a nutritional geometry methodology, we found that the ratio of proteins‐to‐carbohydrates (P:C) present in media greatly influenced adult D. suzukii behavior and subsequent offspring development. Whereas adult flies showed a strong bias in their oviposition and association behaviors toward carbohydrate‐rich foods, larval survival and eclosion rate were strongly dependent on protein availability. Here, we explore the preference–performance hypothesis (PPH), in which females are predicted to oviposit on medias that provide the greatest offspring benefits, in regard to its relevance in D. suzukii behavior and consequences for management. Our results provide valuable insight into the ecology and evolution of this species that may hopefully lead to more effective management strategies.     

绒毛白蜡二态型果实的扩散特征

多态型果实或种子的出现对植物种群的扩散具有重要的意义。绒毛白蜡(Fraxinus velutina)的果实具有二态型特征,主要表现在果翅数量上不同,分别定义为二翅型和三翅型果实,为了比较两类果实在风传扩散时的差异,研究了两类果实的形态、果翅结构和扩散距离及扩散时长。在大型封闭地下室内,以电扇在不同速度档位产生的气流作为风源,分别从2、1.5、1m处手动释放果实,对风速为0、4.6、6.5、7.3m/s时的果实扩散距离及扩散时长进行了比较;并在此基础上对果实的形态特征与扩散特征进行了线性相关分析。结果表明:在同一高度及相同风速下,三翅型果实的水平扩散距离都极显著的大于二翅型,但其相应的扩散时长都小于二翅型。在相同情况下,三翅型的果实沉降速度显著高于二翅型。两类果实随着释放高度的增加,其扩散距离和扩散时长都相应的增加;随着风速的升高,其扩散距离及扩散时长都相应的增加。三翅型果实质量显著高于二翅型,相反,三翅型果翅长与宽都显著小于二翅型。两种翅型的果翅细胞结构都一样,细胞内部都呈现气囊状,果翅表面沿纵轴方向有流线型的纵棱。通过直线相关分析发现,翅型是对扩散距离和扩散时长影响最显著的形态特征;与果实释放高度相比,风速是影响绒毛白蜡果实扩散距离与扩散时长最显著的环境因素。绒毛白蜡三翅型果实比二翅型果实传播的远,关键在于其具有三翅,三翅对阵风瞬间响应,使得沉降速度较二翅型高,可以在瞬时风的作用下,快速传播到较远的距离。三翅型与二翅型在扩散方式上的结合增强了绒毛白蜡的生存与定殖机会。