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.     

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

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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.     

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。     

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.     

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.     

Resistance of Drosophila suzukii to the larval parasitoids Leptopilina heterotoma and Asobara japonica is related to haemocyte load

Unlike other Drosophila species, the invasive Drosophila suzukii Matsumura (Diptera: Drosophilidae) shows a remarkable pest status. Among the physiological traits that may explain the high level of resistance to parasitoids of Drosophila larvae, the haemocyte load is shown repeatedly to play an important role. To determine whether haemocyte load can explain immunity resistance of D. suzukii to parasitoids, the haemocytes of parasitized and healthy larvae are quantified in two Japanese and three French populations of D. suzukii. Parasitization tests are conducted with two larval parasitoids: the paleartic Leptopilina heterotoma Thomson (Hymenoptera: Figitidae) and the Asian Asobara japonica Belokobylskij (Hymenoptera: Braconidae). Based on morphological and functional criteria, D. suzukii has classes of haemocytes similar to those described in Drosophila melanogaster. However, healthy larvae of the five populations tested possess particularly large numbers of haemocytes compared with D. melanogaster. Haemocyte load is also higher in larvae from the French populations than in the Japanese strains. The ability of D. suzukii larvae to encapsulate eggs of L. heterotoma is associated with a particularly high load of circulating haemocytes. However, it is notable that A. japonica induces a strong depression of the haemocyte population in this resistant host associated with an inability to encapsulate parasitoid eggs. The results show that the cellular immune system plays a major role in the failure of larval parasitoids to develop in most instances in larvae of D. suzukii, possibly contributing to the success of this species as an invader.     

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.     

Distribution and activity of Drosophila suzukii in cultivated raspberry and surrounding vegetation

Spotted wing drosophila, Drosophila suzukii (Matsumura) (Diptera: Drosophilidae), may utilize wild ‘Himalaya’ blackberry (HB) Rubus armeniacus Focke or other non‐crop plants as refugia and possibly exploit adjacent field margins before colonizing cultivated fruiting crops. Studies were conducted to determine the role of field margins containing HB and their effect on D. suzukii activity, density and distribution in an adjacent commercial red raspberry crop. One‐ha plots adjacent to field margins containing HB or known non‐host (NH) grass crops were established in 2011 and 2012 and replicated three times. Each plot contained two transects with monitoring traps for D. suzukii in the field margin (0 m) and spaced approximately 10 (crop boundary), 40, 70 and 100 m into the adjacent crop (n = 10 traps/plot). Field margin vegetation was treated with a 10% chicken egg white mark solution weekly from pre‐harvest until the end of harvest using a cannon sprayer. Adult D. suzukii were collected from traps weekly and analysed for the presence of the egg white mark using an egg white‐specific enzyme‐linked immunosorbent assay (ELISA). During both years, marked flies and total flies were captured in higher numbers in HB field margins, whereas virtually no flies were captured in field margins containing no known alternative host. Similarly, more flies were captured in the crop near HB than near NH. Spatial Analysis by Distance IndicEs (SADIE) and mean D. suzukii trap captures additionally displayed significantly higher fly densities in the raspberry field near HB than near NH. These results suggest that HB may contribute to elevated D. suzukii populations and pest pressure in comparison with field margins containing no known alternate host vegetation for D. suzukii. Having closely adjacent non‐crop alternate host landscapes may result in increased D. suzukii pest pressure.     

Humidity affects populations of Drosophila suzukii (Diptera: Drosophilidae) in blueberry

Temperature and humidity affect insect physiology, survival, fecundity, reproductive status and behaviour. Complementing previous work investigating the effects of temperature on adult survival and fecundity of the invasive frugivorous pest, Drosophila suzukii (Matsumura), this study was conducted to determine the effect of humidity on D. suzukii larval development, adult survival, fecundity and reproductive status using blueberry as a host substrate. The five constant humidity levels in laboratory bioassays were 20, 33, 71, 82 and 94% RH at 20.6 ± 0.2°C. As RH increased, fecundity and longevity increased. At the higher humidity levels, RH had limited impact on mean generation times (T), larval development and eclosion times. The highest net reproductive rate (R_o = 68) and highest intrinsic rate of population increase (r_m = 0.17) were both recorded at 94% RH. The reproductive status of females, as indicated by the number of mature oocytes per female, was significantly greater at 82 and 94% RH, compared to 71% RH. In addition to the laboratory procedures, we correlated field trap captures over an 81‐day summer period to relative humidity (RH) levels in close proximity to those traps. In the field, low ambient humidity levels resulted in decreased trap captures. A humidity‐dependent population model predicted lower densities of D. suzukii relative to populations at higher humidity. This study supports the hypothesis that cultural practices that minimize lower humidity levels in crops can contribute to the management of D. suzukii. Such methods may include open pruning, drip irrigation and field floor management.     

<Emphasis Type="Italic">Drosophila suzukii</Emphasis> in Southern Neotropical Region: Current Status and Future Perspectives

Non-native insect pests are often responsible for important damage to native and agricultural plant hosts. Since Drosophila suzukii Matsumura (Diptera: Drosophilidae) has become an important pest in North America and Europe (i.e., in 2008), the global production of soft thin-skinned fruits has faced severe production losses. In the southern Neotropical region, however, the first record of D. suzukii occurred in 2013 in the south of Brazil. It has also been recorded in Uruguay, Argentina, and Chile. Despite its recent occurrence in the southern Neotropical region, the fast dispersion of D. suzukii has inspired local research efforts in an attempt to mitigate the consequences of this insect pest invasion. In this forum, we explore the current status of D. suzukii in southern Neotropical regions, discussing its future perspectives. Additionally, we attempt to draft activities and a research agenda that may help to mitigate the losses caused by D. suzukii in native and commercial soft-skinned fruits produced in this region. Currently, D. suzukii appears to be well established in the south of Brazil, but considering the entire southern Neotropical region, the invasion panorama is still underinvestigated. The lack of studies and regulatory actions against D. suzukii has contributed to the invasion success of this species in this region. Considering several peculiarities of both the pest biology and the environmental of this region, the authors advocate for the need of intensive and integrative studies toward the development and implementation of area-wide integrated pest management programs against D. suzukii in the southern Neotropical region.     

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.     

Increased nutrient availability decreases insect resistance in cranberry

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Plasticity in oviposition and foraging behavior in the invasive pest Drosophila suzukii across natural and agricultural landscapes

The effects and extent of the impacts of agricultural insect pests in and around cropping systems is a rich field of study. However, little research exists on the presence and consequence of pest insects in undisturbed landscapes distant from crop hosts. Research in such areas may yield novel or key insights on pest behavior or ecology that is not evident from agroecosystem-based studies. Using the invasive fruit pest Drosophila suzukii (Matsumura) as a case study, we investigated the presence and resource use patterns of this agricultural pest in wild blackberries growing within the southern Appalachian Mountain range of North Carolina over 2 years. We found D. suzukii throughout the sampled range with higher levels of infestation (D. suzukii eggs/g fruit) in all ripeness stages in natural areas when compared with cultivated blackberry samples, but especially in under-ripe fruit. We also explored a direct comparison of oviposition preference between wild and cultivated fruit and found higher oviposition in wild berries when equal weights of fruit were offered, but oviposition was higher in cultivated berries when fruit number was equal. Forest populations laid more eggs in unripe wild-grown blackberries throughout the year than populations infesting cultivated berries. This suggests D. suzukii may change its oviposition and foraging behavior in relation to fruit type. Additionally, as D. suzukii exploits a common forest fruit prior to ripeness, further research is needed to explore how this affects wild food web dynamics and spillover to regional agroecosystems.     

Radiation effects on Drosophila suzukii (Diptera: Drosophilidae) reproductive behaviour

Female remating is a widespread behaviour, reported in several insect species. This behaviour can affect the efficiency of sterile insect technique (SIT); however, little is known about the postcopulatory behaviour of some pest species considered as candidates to be controlled by this technique, such as Drosophila suzukii (Matsumura, 1931) (Diptera: Drosophilidae). In this study, we investigated the effects of male and female sterilization on mating and remating behaviour of D. suzukii. First, we tested the occurrence of multiple mating in different combinations between sterile and fertile males and females. Then, we tested the effects of male and female sterility on female propensity to mate and remate. We found an overall low remating rate by D. suzukii females. Male sterility did not influence mating and remating likelihood; however, copula duration of sterile males was shorter compared to fertile males. On the other hand, sterile females were less likely to mate. Our findings encourage further research regarding the use of SIT to control D. suzukii.     

Effect of fruit host on wing morphology in Drosophila suzukii (Diptera: Drosophilidae): A first view using geometric morphometrics

The invasive alien fruit pest Drosophila suzukii, (Matsumura 1931) causes economic loss in soft‐skinned fruit production across Europe. After its first detection in 2008, the species has successfully expanded to a wide geographic area and invaded new host plants in a relatively short period of time. The aim of the present study was to analyze the connection between food preferences as host specialization and the morphology of D. suzukii. Population morphological variation in wings was investigated in two different host fruits (grape and strawberry) in which economic damage has been recorded. The geometric morphometric results revealed two noticeable wing shape morphotypes in D. suzukii (i.e. vein configuration) between the grape and strawberry fruits. Flies reared in grapes had wider wings, whereas flies grown in strawberries had more narrow wings. These differences in morphotype could be explained by the effects of wing aerodynamics, which affect the strength of the wings in flight. This, in turn, can lead to better dispersion within the associated fruit host. These results confirm that this extremely invasive species, found worldwide, is successful at spreading in part because of its potential to adapt rapidly under different rearing conditions. Therefore, adaptive variations in the wing shape of D. suzukii can be used to differentiate populations based on food preference (e.g. soft fruits) and can serve as an additional tool for detecting different bioecological types of D. suzukii.     

Spillover of Drosophila suzukii between noncrop and crop areas: implications for pest management

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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.     

Variation of within‐crop microhabitat use by Drosophila suzukii (Diptera: Drosophilidae) in blackberry

Drosophila suzukii Matsumara (Diptera: Drosophilidae) is an invasive vinegar fly that infests ripe and ripening soft skinned fruits. In the south‐eastern United States, blackberry (Rubus spp.) crops are heavily impacted by D. suzukii, and current management tactics rely on the use of broad‐spectrum insecticides targeted to adult populations. An improved understanding of D. suzukii biology and ecology are necessary to create sustainable management options. Knowledge of how D. suzukii interacts with resources will enable targeted management actions in the future. In this present study, we monitored larval infestation throughout the blackberry canopy and found that infestation was highest in the inner portion of the canopy and lower in more exposed locations. We also documented higher humidity within the cane canopy relative to the edge of the field. A difference in abiotic conditions may create within‐crop microhabitats that D. suzukii is able to exploit. Future research will explore how to take advantage of these microhabitats in pest management programs.     

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.