SHORT COMMUNICATION

 

Laboratory evaluation of nine highbush blueberry cultivars susceptibility to Drosophila suzukii (Matsumura, 1931) in the Southwestern Spain

 

José M. Molina (Molina, JM)

Sergio Pérez-Guerrero (Pérez-Guerrero, S)

IFAPA, Centro “Las Torres”, Laboratorio de Entomología. Crta. Sevilla-Cazalla de la Sierra, Km 12,2. 41200 Alcalá del Río (Sevilla). Spain.

 

 

 

 

Abstract

Aim of study: To determine how susceptible the most used Southern highbush blueberry (SHB) cultivars were to the spotted wing Drosophila (SWD), Drosophila suzukii (Matsumura, 1931) (Diptera: Drosophilidae) as well as those recently introduced to Southwestern Spain.

Area of study: Southwestern Spain (Huelva province). 

Material and methods: Nine of the SHB cultivars which were recently introduced in Southwestern Spain and the most used ones were selected: ‘Arana’, ‘Camellia’, ‘Kirra’, ‘Mayra’, ‘Misty’, ‘O'Neal’, ‘Sharpblue’, ‘Star’ and ‘Ventura’. In order to determine how susceptible the cultivars were to SWD, no-choice tests were performed under laboratory conditions. In addition, berry size, berry firmness, ºBrix, and pH were recorded in order to assess what influence these variables had on oviposition preference by SWD. 

Main results: Mean clutch size and mean number of emerged adults in ‘Star’ were significantly higher than in the other tested cultivars. ‘Mayra’, ‘Camellia’ and ‘Ventura’ received the lower clutch sizes and mean number of emerged adults. Mean developmental time (egg to adult) differed significantly among tested cultivars and were highest in ‘Camellia’ than in the other tested cultivars. Only firmness and pH were correlated with SWD infestation as females tend to oviposit more eggs in softer fruits than in firmer fruits. Results also showed that a higher pH increased the emergence of adults and shortened the egg to adult developmental time.  

Research highlights: Our results showed significant differences in the susceptibility of SHB to SWD. This information may help design IPM programs and in making recommendations for blueberry crops as planting of low-chill cultivars expands. 

Additional key words: spotted wing Drosophila; invasive pest; berry crops; pest-resistant; integrated pest management; sustainable agriculture.

Abbreviations used: GLMs (generalized linear models); SHB (Southern highbush blueberry); SWD (spotted wing drosophila).

Authors’ contributions: Designed and performed the tests: JMM and LA. Wrote the paper: JMM and SPG. All authors contributed to the statistical analyses, read and approved the final manuscript.

Citation: Molina, JM; Avivar, L; Pérez-Guerrero, S (2020). Short communication: Laboratory evaluation of nine highbush blueberry cultivars susceptibility to Drosophila suzukii (Matsumura, 1931) in the Southwestern Spain. Spanish Journal of Agricultural Research, Volume 18, Issue 2, e10SC03. https://doi.org/10.5424/sjar/2020182-16100

Received: 26 Nov 2019. Accepted: 11 Jun 2020.

Copyright © 2020 INIA. This is an open access article distributed under the terms of the Creative Commons Attribution 4.0 International (CC-by 4.0) License.

Funding Agencies/Institutions Project/Grant
IFAPA CAPDR Junta de Andalucia (Spain)

AVA.301201.6 (Obj. 3)

 AVA201601.10 (Line 2)

Competing interests: The authors have declared that no competing interests exist.

Correspondence should be addressed to Sergio Pérez-Guerrero: sergio.perez@juntadeandalucia.es


 

CONTENTS

Abstract

Introduction

Material and methods

Results

Discussion

Acknowledgements

References

IntroductionTop

The spotted wing Drosophila (SWD), Drosophila suzukii (Matsumura, 1931) (Diptera: Drosophilidae), is an invasive frugivorous pest native to South East Asia, which was first detected in Southern Europe (Spain and Italy) and continental USA in 2008, and currently affects a wide range of important crops in Europe and America, especially berries (Asplen et al., 2015). Unlike other Drosophila species, SWD infests healthy ripening fruits, and inserts eggs with its serrated ovipositor (Walsh et al., 2011) so larvae feed and develop inside the fruits, which then become unmarketable, resulting in dramatic reductions in fruit production and economical losses in berry production in Europe (Cini et al., 2012) and North America (Goodhue et al., 2011). Among the wide range of SWD hosts, blueberries are one of the most susceptible crops (Cini et al., 2012; Gargani et al., 2013) and 30%–40% of production is lost.

Southern highbush blueberry cultivars (SHB) are tetraploid interspecific hybrids developed in the USA by adding genes from several blueberry species to the Northern highbush blueberry (Vaccinium corymbosum L.). As it has lower chilling requirements and ripens earlier, SHB can be planted in drier and hotter climates (Lang, 1993; Brevis et al., 2008). SHB cultivars are planted in significant amounts at present in the Southern states of North America (Florida, Georgia, and California), Mexico, Ecuador, Peru, Chile, Argentina, Australia, Morocco and Spain (Bañados, 2009; Lobos & Hanckonck, 2015; Scalzo et al., 2016). In Southwestern Spain (Huelva province), SHB cultivars were introduced on a commercial scale in the 1990s. Currently, crop production is well established there and increasing as the local environment is suitable for them and they are highly profitable (Bañados, 2009). They occupy an area of approximately 3,410 ha and total production was 42,522 tons in 2017 (AGAPA, 2018). Hence, blueberries are an important socio-economic driver in the region.  

The use of pest-resistant or tolerant varieties and hybrids in plant production is fundamental to Integrated Pest Management (IPM) programs, can significantly reduce the need for insecticides, and helps environmentally-friendly crop management. Selecting resistant crop cultivars or ones with a low susceptibility to pests is still a major agri-environmental concerns and a preventive method for reducing the cost of pesticide control and the negative effects of using synthetic products (Sharma & Ortiz, 2002). Several authors have analyzed the susceptibility of berries and other crops cultivars (blueberries, raspberries, blackberries, strawberries, cherries and grapes) to SWD (Lee et al., 2011; Linder et al., 2014; Ioriatti et al., 2015; Gong et al., 2016; Hemer et al., 2016; Baser et al., 2018). There has been little research into the susceptibility of blueberries to SWD. Lee et al. (2011) showed no significant differences among California blueberry cultivars in terms of number of eggs laid and developing SWD, although there were variations in development percentage (number of developing SWD/ number of eggs laid) and these were higher in ‘Star’ than in ‘Misty’ and ‘O'Neal’ cultivars. Kinjo et al. (2013) showed softer fruits cultivars were more vulnerable to SWD females than firmer ones. Recently, Stringer et al. (2017) determined the range of resistance or non-preference available in sundry sources of blueberry germplasm and detected antibiosis in some of the blueberry hosts tested. In the berry market where new varieties are constantly developed and sold, it is crucial to know how resistant the crop cultivars that grow in a given region are when developing an IPM program, especially for crops in different geographical areas with varying soil types, climatic conditions and agronomic methods (Sharma & Ortiz, 2002). Thus, in this study there was an assessment of how susceptible the most used SHB cultivars were to SWD as well as those recently introduced to Southwestern Spain, with a no-choice test under laboratory conditions. Additionally, blueberry traits (fresh weight, firmness, pH and sugar content) were recorded in order to assess what influence these variables had on oviposition preference by SWD.

Material and methodsTop

Insects and berries

The SWD adults used in the bioassays came from an experimental colony established in the IFAPA Las Torres Laboratory of Entomology (Alcalá del Río, Seville; Spain) from larvae collected from infested raspberry f ields in Huelva (Southwestern Andalusia). The colony was reared on berry fruits (blueberries and raspberries). Individuals from naturally infested fruits (also collected in Huelva) were introduced into the colony several times during rearing to prevent endogamy, and ensure genotypic diversity. The insects were kept at 22 ± 1 Cº, 65% RH, and 16:8 h (L:D) photocycle in 0.3 m3 cages (BugDorm® 1; Bio-Quip Products Inc., Rancho Rodríguez, CA, USA), and provided with 5% w/v brewer’s yeast/dH2O, and 10% w/v sugar-dH2O as food sources. Nine of the SHB cultivars which were recently introduced in Southwestern Spain and the most used ones were selected: ‘Arana’, ‘Camellia’, ‘Kirra’, ‘Mayra’, ‘Misty’, ‘O'Neal’, ‘Sharpblue’, ‘Star’ and ‘Ventura’. Berries from ‘Camellia’, ‘O'Neal’, ‘Misty’, ‘Sharpblue’, and ‘Star’ were collected from plants growing at the IFAPA ‘El Cebollar’ Experimental Station (Moguer, Huelva). Commercial berries from ‘Arana’, ‘Kirra’, ‘Mayra’, and ‘Ventura’ (FresDoñarosa; Superexport Cia. Agraria S.L.; Huelva, Spain) were used in the bioassays. Finally, fruit ripe for consumption from the nine cultivars were used in the bioassays.

Laboratory assays

In order to assess how susceptible the cultivars were to SWD, no-choice tests were performed under laboratory conditions. Berries were rinsed with distilled water, air dried, and examined before testing with a stereomicroscope (x20, Leica MZ6, Leica Microsystems, Germany) to ensure there were no bruises or SWD infestation. In each test, 8 berries were exposed for 24 hours to 5 female and 4 male SWD in a 0.3 m3 cage (BugDorm® 1; Bio-Quip Products Inc., Rancho Rodríguez, CA, USA). After exposition, the berries were removed from the cage, and the number of eggs per berry (clutch size) were counted. Each fruit was separately placed in a polystyrene tube with a piece of moistened foam at the bottom and kept under laboratory conditions (22 ± 1 ºC, 60 ± 5% RH, and a 16:8 h (L:D) photocycle) for 21 days, recording the number of emerged adults. Clutch size, number of adults emerged, sex and the time from egg to adult development (days) were also recorded. A total of six replicates per cultivar was established.

Fruit samples (12-20 per cultivar) from the same batches in the no-choice test were analysed to measure weight (g fresh weight), firmness (skin penetration force, g mm-2), pH and sugar content (ºBrix). Fruit firmness was measured in grams force (gf) using a manual penetrometer (Effegi® tr FDP 500 g; Italy) fitted with a 1 mm Ø blunted needle. For each blueberry, two measurements in the middle of the berry were recorded and averaged. Sugar content was determined by puncturing and squeezing individual fruits and placing a drop of juice on a portable refractometer (Eclipse®, Bellingham & Stanley Ltd., UK). After sugar content was recorded, juice was obtained by crushing the berries two by two, and pH was measured using a Crimson pH-meter basic 20 (Alella, Spain).

Statistical procedures

Since clutch size, number of adults emerged, and days of development, did not fulfil normality conditions nor linearity of residuals, generalized linear models (GLMs) were ran to test the effects of different cultivars using the R v. 3.1.3 software package. GLMs were carried out separately, including total number of eggs and total number of adults as dependent variables, and cultivars as the factor fitted to a Poisson distribution with a log link function. GLMs with interaction terms were also performed including cultivars and adult sex as factors, and days of development as the dependent variable fitted to a Poisson distribution with a log link function. Where differences were detected by GLM, multiple comparisons, post-hoc Tukey HSD tests (p<0.05) were performed using the “glht” function in the “multcomp” package. GLM procedures used the Wald statistic (‘‘z’’) value and Pr([|z|) to analyse the effects each factor had on the response variable to test the hypothesis that the corresponding parameter (regression coefficient) was zero (Crawley, 2005).

Given that fruit weight, firmness, pH, and sugar content of berries matched normality and linearity of residuals, a one-way ANOVA (p<0.05) was used to determine differences in berry traits among cultivars. When statistical differences were detected, their means were separated by Tukey´s honestly significant difference (HSD) test (p <0.05) The correlation between berry traits and SWD infestation data were conducted using a non-parametric Spearman's rank correlation coefficient (ρ).

 

Inducing drought stress tolerance in crop plants

Under drought stress conditions, plants have developed various mechanisms for drought resistance (avoidance and tolerance). The deleterious effects of drought stress on plants are mainly related to osmotic and oxidative stresses induced by drought. In order to cope with osmotic stress, plants synthesize and accumulate neutral and nontoxic compound (compatible solutes or osmolytes) in cytoplasm along with certain inorganic ions in vacuoles (Abid et al., 2018). The accumulation of compatible solutes maintains cell hydrated state and membrane structural integrity and stabilizes structural and functions of macromolecules (Hoekstra et al., 2001). These compatible solutes include several compounds such as proline, glycine betaine and soluble sugars. In addition to its role in osmotic adjustment, proline plays important roles as a cell redox balancer, a free radical scavenger and a cytosolic pH buffer (Ali et al., 2017) and reduces photo-damage in thylakoid membranes (Lawlor & Cornic, 2002).

Drought induces oxidative stress via the production of ROS including superoxide radical (O2−•), hydrogen peroxide (H2O2), and hydroxyl radical (OH) that cause oxidative damage to lipids, proteins, and DNA (Schieber & Chandel, 2014). Enzymatic and non-enzymatic antioxidants are involved in cellular defense mechanism responses for ROS detoxification. Superoxide dismutases (SOD) covert O2−• stress through dismutation reaction of O2 and H2O2 (Schieber & Chandel, 2014). As a result, H2O2 can be converted into H2O and O2 by catalase (CAT) and specific peroxidases (POX) (Roychoudhury et al., 2012). Non-enzymatic antioxidants mainly include ascorbate (AsA), flavonoids, glutathione (GSH), and carotenoids (Foyer & Noctor, 2012). Overall, the coordinated antioxidant activity associated to increased activities of SOD and CAT, together with a modulation of the AsA-GSH cycle, reduces drought stress-induced oxidative damage in crops (Zandalinas et al., 2017).

For achieving enhanced crop drought tolerance, three prominent plant breeding approaches (conventional breeding, marker-assisted breeding, and genetic engineering) have been performed (Ashraf, 2010). Plant hormones are active members of the signal compounds involved in the induction of plant stress responses. In the last decade, a lot of work has been done to understand plant hormone-mediated abiotic stress tolerance, using physiological, biochemical, genetic, molecular, and genomic approaches for crop breeding and management, including exogenous application of plant growth regulators (De Ollas et al., 2015; Muñoz-Espinoza et al., 2015; De Ollas et al., 2018). In addition to phytohormones, seaweed extracts, biochar, osmoprotectants, plant growth promoting rhizobacteria (PGPR) and nanoparticles have been applied to induce drought tolerance in crop plants (Ali et al., 2017). Among various strategies adopted to counter drought-induced damage in plants, use of NMs has been proved promising (Khan et al., 2017).

 

ResultsTop

Significant differences in mean clutch size and emerged adults were detected among cultivars (z=7.6, p< 0.001 and z=7.5, p<0.001 respectively; Fig. 1). Post-hoc tests showed that mean clutch size in ‘Star’ (64.7 ± 5.7 eggs per berry) was significantly higher than in the other tested cultivars (z=11.5, 13.7, 8.9, 10.9, 7.9, 11.7, 6.5 and -13.7 respectively; p<0.001 in all cases). ‘Sharpblue’ and ‘Kirra’ also showed high clutch sizes (30.3 ± 5.0 and 28.5 ± 9.3 eggs per berry, respectively) but there were no signif icant differences between them (z=0.5; p>0.05). Berries from ‘Mayra’, ‘Camellia’ and ‘Ventura’ had the lowest mean clutch size (4.3 ± 2.0, 7.0 ± 2 and 7.0 ± 1.6 eggs per berry, respectively; Fig. 1). A similar pattern was found with the emerged adults. A significantly higher number of f lies emerged from ‘Star’ berries (39.7 ± 4.0 adults per berry) with respect to the other cultivars tested (z=9.7, 10.2, 7.9, 7.6, 5.7, 9.2, 4.9 and -10.7 respectively; p<0.001 in all cases). Once again, ‘Mayra’, ‘Camellia’ and ‘Ventura’ displayed the lowest mean number of emerged adults (2.3 ± 1.9, 2.2 ± 1.2 and 3.7 ± 1.0 adults per berry, respectively) with no significant differences between them (z= 1.5; p>0.05; Fig. 1).

Mean developmental time (egg to adult) was 14.4±0.1 days; with significant differences among cultivars (z=2.4, p<0.05). Developmental time was higher in ‘Camellia’, and significantly different to that in the other cultivars (z=3.4, -3.8, -4.6, -3.9, -4.2, -3.3, -4.8 and -3.4 respectively; p<0.05 in all cases). Egg to adult developmental time was slightly shorter in males (14.3±0.1 days) than in females (14.6±0.1 days), but there were no signifi-cant differences between sexes and their interaction with the cultivars (z=0.8 and -0.6 respectively; p>0.05 in both cases; Fig. 2).

Berries from the different cultivars varied in their quali-ty attributes (Table 1). Berry size (expressed as g fresh weight) differed significantly among cultivars (F8,99=33.5; p<0.001) with ‘Camellia’ showing the highest value and ‘O’Neal’ the lowest. Firmness also differed significant-ly (F8,99=49.3; p<0.001) with the minimum, 105.6±2.1 g mm-2, for ‘Sharpblue’, and the maximum, 294.8±4.5 g mm-2, for ‘Kirra’. Results also showed significant diffe-rences in their sugar content (F8,99=3.9; p<0.001). ‘Mayra’ and “Misty” had the highest and lowest sugar contents respectively. Similarly, there were significant differences in their pH values (F8,45=7.3; p<0.001), with the lowest ones in ‘Camellia’, and the highest in ‘Arana’.

In general, no correlation between berry attributes, clutch size and number of emerged adults was found. Results only showed a negative correlation between clutch size and firmness (Spearman’s ρ=-0.205; p<0.05) and a positive one between number of adults emerged and pH (ρ=0.512; p<0.05). Furthermore, a negative correla-tion was found between egg to adult developmental time and pH (ρ=-0.582; p<0.05).

 

Figure 1. Mean number of eggs laid and adults emerged of Drosophila suzukii per berry from nine Southern highbush blueberry obtained in the no-choice assays after exposing of 8 berries to 5 females and 4 males of D. suzukii over 24 hours. Error bars indicate standard error of the mean.

 

 

Figure 2. Mean developmental time (egg to adult) of males and females Drosophila suzukii from nine Southern highbush blue-berries in the no-choice tests. Error bars indicate standard error of the mean.


 

DiscussionTop

To date there has been little research into the susceptibility of SHB to SWD. Overall, the results obtained herein showed that the nine SHB cultivars in this study were susceptible to SWD oviposition, and suitable for larval development although there were some differences among them. Few studies have identified pest-resistant SHB cultivars, which suggests that commercially-available blueberry cultivars lack meaningful genetic resistance to SWD (Stringer et al., 2017; Rodríguez-Saona et al., 2018; 2019). Results showed that when the ‘Star’ cultivar was exposed to SWD, significantly more eggs and emerged adults were detected with respect to the other cultivars. In contrast, Lee et al. (2011) found no significant di-fferences in the number of eggs laid among 12 California SHB cultivars including ‘Star’, Misty’, ‘O'Neal’ and ‘Sha-rpblue’ (also included in this paper). However, they were found significant differences in the development percen-tage, the highest of which were in ‘Star’ and ‘Sharpblue’. Our results also showed that ‘Mayra’, ‘Camellia’ and ‘Ventura’ were less susceptible to SWD, with the lowest values for clutch size and number of emerged adults. In fact, out of all the cultivars ‘Camellia’ showed the longest developmental time (egg to adult) compared to the remaining cultivars in this study. Currently, ‘Star’ and ‘Ventura’ are among the most frequently used blueberry cultivars in Southwestern Spain (http://www.estrategiaprovincial-huelva.com/). Laboratory results obtained herein indicate that there could be substantial differences in their susceptibility to SWD in contrast to previous results obtained by Lee et al. (2011). However, further research and field observations are required to confirm these differences in susceptibility and any potential practical applications. Berry traits in SHB cultivars are largely determined by genetics, modified not just by selection and breeding (Ehlenfeldt & Martin, 2002; Rodríguez-Saona et al., 2018), but also by cultural practices (Forney, 2001; Stückrath et al., 2008; Angeletti et al., 2010, Lee et al., 2015; Little et al., 2018). Blueberry farming is a highly dynamic sector, in constant growth and adapted to meeting consumer demand. Consequently, new varieties of SHB cultivars, are constantly being produced and tested; therefore, to reduce SWD damage, the cultivars grown should be constantly compared and new ones screened, especially before they are planted in any specific area.

In the susceptibility to SWD infestation analysis, links were found to several physical and/or chemical fruit traits and berry firmness played a primary role in limiting SWD infestation (Lee et al., 2011; Kinjo et al., 2013). According to our results, there was a negative correlation between number of eggs laid and fruit firmness, thus indicating that SWD females tended to oviposit more eggs in softer fruits than firmer ones. Consistent with this finding, Ioratti et al. (2015) and Baser et al. (2018) found a negative correlation between the number of eggs laid and berry skin penetration force when they analyzed the susceptibility of grape varieties to SWD. In addition, other factors were significant. Stringer et al. (2017), working with blueberry genotypes and cultivars, reported a positive correlation between SWD clutch size and berry weight. Gong et al. (2016) also found variations in the emergence of SWD among strawberry accessions, which correlated with fruit diameter. Our results found no correlation between clutch size, number of emerged adults and berry fresh weight. So, other factors may then be more influential in determining differences in clutch size and emerged adults among the blueberry cultivars tested herein. Previous studies on the effects fruit sugar content has on SWD oviposition have yielded variable results. Lee et al. (2011, 2016), and Stringer et al. (2017) reported a positive correlation between oviposition and °Brix of fruits. In contrast, Little et al. (2017), and Rodríguez-Saona et al. (2018) showed a preference for fruits with low sugar content. Results obtained herein showed the sugar content of the nine SHB cultivars bore no relation to SWD infestation, in line with previous results by Pelton et al. (2017) on grapes. Therefore, further laboratory and field research is required to determine the real effects sugar content has on SWD infestation.

A positive correlation was found between number of adults emerged and pH. Additionally, egg to adult developmental time and pH were negatively correlated. In general, previous studies showed a positive relationship when pH increased on SWD infested blueberries (Lee et al., 2016; Little et al., 2017; Rodríguez-Saona et al., 2018). In contrast, Pelton et al. (2017) found no correlation between pH and SWD performance in grapes. Our results are coherent with a general pattern in which less acidic blueberry cultivars were more susceptible to SWD infestation.

In summary, our results showed that the nine SHB cultivars tested in this study are susceptible to SWD oviposition, with significant differences in the number of eggs laid and emerged adults between ‘Star’ and the other cultivars, mainly ‘Camellia’ and ‘Ventura’. However, it must be stressed that blueberry cultivars should be selected on the basis of an analysis of many other relevant factors of an agricultural, socio-economic nature, and whose results do not necessarily need to concur with those reported herein. Among the fruit traits analyzed, only firmness and pH were correlated with SWD infestation. According to previous research, SWD females tend to oviposit more eggs in softer fruits than firmer ones. In addition, the higher the pH, the more adults emerged and the shorter the larval development time. Given the dynamic evolution of SHB crops in Southwestern Spain, more laboratory and field studies in this area are required and an analysis of how susceptible blueberry cultivars are to SWD would help design IPM programs.

 

Table 1. Berry traits (mean ± SE) measured from nine Southern highbush blueberries. Size (ANOVA; F8,99=33.5, p<0.01), Firmness (F8,99=49.5, p<0.01), Sugar content (ANOVA, F8,99=3.9, p<0.01) and pH (F8,45=7.3, p<0.001). Letters denote significance differences by Tukey’s HSD (p<0.05)..

AcknowledgementsTop

 

The authors wish to thank Asunción Sánchez (IFAPA “Las Torres”) for helping us in the laboratory assays.

ReferencesTop

AGAPA, 2018. Sector Frutos Rojos. Arándano. Campaña 2017/18. Agencia de Gestión Agraria y Pesquera de Andalucía, Consejería de Agricultura, Pesca y Desarrollo Rural. Observatorio de Precios y Mercados. 2 pp. https://www.juntadeandalucia.es/agriculturaypesca/observatorio/
Angeletti P, Castagnasso H, Miceli E, Terminiello L, Concellón A, Chaves A, Vicente AR, 2010. Effect of preharvest calcium applications on postharvest quality, softening and cell wall degradation of two blueberry (Vaccinium corymbosum) varieties. Postharvest Biol Technol 58: 98-103. https://doi.org/10.1016/j.postharvbio.2010.05.015
Asplen MK, Anfora G, Biondi A, Choi DS, Chu D, Daane KM, Gibert P, Gutierrez AP, Hoelmer KA, Hutchinson WD, et al., 2015. Invasion biology of spotted wing Drosophila (Drosophila suzukii) a global perspective and future priorities. J Pest Sci 88: 469-494. https://doi.org/10.1007/s10340-015-0681-z
Bañados MP, 2009. Expanding blueberry production into non-traditional production areas: Northern Chile and Argentina, Mexico and Spain. Acta Hort 810: 439-444. https://doi.org/10.17660/ActaHortic.2009.810.57
Baser N, Broutou O, Verrastro V, Porcelli F, Ioriatti C, Anfora G, Mazzoni V, Stacconi MVR, 2018. Susceptibility of table grape varieties grown in south-eastern Italy to Drosophila suzukii. J Appl Entomol 142: 465-472. https://doi.org/10.1111/jen.12490
Brevis PA, Bassil NV, Ballington JR, Hancock JF, 2008. Impact of wide hybridization on highbush blueberry breeding. J Amer Soc Hort Sci 133 (3): 427-437. https://doi.org/10.21273/JASHS.133.3.427
Cini A, Ioriatti C, Anfora G, 2012. A review of the invasion of Drosophila suzukii in Europe and a draft research agenda for integrated pest management. Bull Insectol 65: 149-160.
Crawley MJ, 2005. Statistics: an introduction using R. Wiley, Chichester, UK, 327 pp. https://doi.org/10.1002/9781119941750
Ehlenfeldt MK, Martin RB, 2002. A survey of fruit firmness in highbush blueberry and species-introgressed blueberry cultivars. HortScience 37: 386-389. https://doi.org/10.21273/HORTSCI.37.2.386
Forney CF, 2001. Horticultural and other factors affecting aroma volatile composition of small fruit. HortTechnology 11: 529-538. https://doi.org/10.21273/HORTTECH.11.4.529
Gargani E, Tarchi F, Frosinini R, Mazza G, Simoni S, 2013. Notes on Drosophila suzukii Matsumura (Diptera Drosophilidae): field survey in Tuscany and laboratory evaluation of organic products. Redia-Giornale di Zoologia 96: 85-90.
Gong X, Bräcker L, Bölke N, Plata C, Zeitlmayr S, Metzler D, Olbricht K, Gompel N, Parniske M, 2016. Strawberry accessions with reduced Drosophila suzukii emergence from fruits. Front Plant Sci 7: 1880. https://doi.org/10.3389/fpls.2016.01880
Goodhue RE, Bolda M, Farnsworth D, Williams JC, Zalom FG, 2011. Spotted wing drosophila infestation of California strawberries and raspberries: Economic analysis of potential revenue losses and control costs. Pest Manage Sci 67: 1396-1402. https://doi.org/10.1002/ps.2259
Hemer S, Briem F, Hecht A, Herzog K, Eben A, Vogt H, 2016. Variety-depending susceptibility of cherries to Drosophila suzukii according to fruit firmness and other ripening parameters. 9th Young Scientists Meeting, Quedlinburg, Germany, Nov 09-11, Berichte aus dem Julius Kühn-Institut 186. pp. 12.
Ioriatti C, Walton V, Dalton D, Anfora G, Grassi A, Maistri S, Mazzoni V, 2015. Drosophila suzukii (Diptera: Drosophilidae) and its potential impact to wine grapes during harvest in two cool climate wine grape production regions. J Econ Entomol 108: 1148-1155. https://doi.org/10.1093/jee/tov042
Kinjo H, Kunimi Y, Ban T, Nakai M, 2013. Oviposition efficacy of Drosophila suzukii (Diptera:Drosophilidae) on different cultivars of blueberry. J Econ Entomol 106: 1767-1771. https://doi.org/10.1603/EC12505
Lang GA, 1993. Southern highbush blueberries: Physiological and cultural factors important for optimal cropping of these complex hybrids. Acta Hortic 346: 72-80. https://doi.org/10.17660/ActaHortic.1993.346.9
Lee JC, Bruck DJ, Curry H, Edwards D, Haviland DR, Van Steenwyk RA, Yorgey BM, 2011. The susceptibility of small fruits and cherries to the spotted wing drosophila, Drosophila suzukii. Pest Manag Sci 67: 1358-1367. https://doi.org/10.1002/ps.2225
Lee JC, Dreves AJ, Cave AM, Kawai S, Isaacs R, Miller JC, Van Timmeren S, Bruck DJ, 2015. Infestation of wild and ornamental noncrop fruits by Drosophila suzukii (Diptera: Drosophilidae). Ann Entomol Soc Am 108: 117-129. https://doi.org/10.1093/aesa/sau014
Lee JC, Dalton DT, Swoboda-Bhattarai KA, Bruck DJ, Burrack HJ, Strik BC, Woltz JM, Walton VM, 2016. Characterization and manipulation of fruit susceptibility to Drosophila suzukii. J Pest Sci 89: 771-780. https://doi.org/10.1007/s10340-015-0692-9
Linder C, Martin C, Laboisse S, Chatelain PG, Kehrli P, 2014. Susceptibility of various grape cultivars to Drosophila suzukii and other vinegar flies. Integrated protection and production in Viticulture. IOBC-WPRS Bull 105: 219-224.
Little CM, Chapman TW, Moreau DL, Hillier NK, 2017. Susceptibility of selected boreal fruits and berries to the invasive pest Drosophila suzukii (Diptera: Drosophilidae). Pest Manag Sci 73: 160-166. https://doi.org/10.1002/ps.4366
Little CM, Chapman TW, Hillier NK, 2018. Effect of color and contrast of highbush blueberries to host-finding behavior by Drosophila suzukii (Diptera: Drosophilidae). Environ Entomol 47: 1242-1251. https://doi.org/10.1093/ee/nvy102
Lobos GA, Hancock JF, 2015. Breeding blueberries for a changing global environment: a review. Front Plant Sci 6: 782. https://doi.org/10.3389/fpls.2015.00782
Pelton E, Gratton C, Guédot C, 2017. Susceptibility of cold hardy grapes to Drosophila suzukii (Diptera: Drosophilidae). J Ent Appl 141: 644-652. https://doi.org/10.1111/jen.12384
Rodriguez-Saona C, Cloonan KR, Sanchez-Pedraza F, Zhou Y, Giusti MM, Benrey B, 2018. Differential susceptibility of wild and cultivated blueberries to an invasive frugivorous pest. J Chem Ecol 45 (3): 286-297. https://doi.org/10.1007/s10886-018-1042-1
Rodriguez-Saona C, Vincent C, Isaacs R, 2019. Blueberry IPM: past successes and future challenges Annu Rev Entomol 64: 95-114. https://doi.org/10.1146/annurev-ento-011118-112147
Scalzo J, Wright G, Boettiger S, 2016. Adaptability of blueberries to lower chill growing regions in Australia. Acta Hortic 1117: 45-48. https://doi.org/10.17660/ActaHortic.2016.1117.8
Sharma HC, Ortiz R, 2002. Host plant resistance to insects: An eco-friendly approach for pest management and environment conservation. J Environ Biol 23 (2): 111-135.
Stringer SJ, Sampson BJ, Hummer KE, 2017. Screening small fruit germplasm for resistance to southern populations of invasive spotted wing drosophila, SWD (Diptera: Drosophilidae). Acta Hortic 1180: 45-52. https://doi.org/10.17660/ActaHortic.2017.1180.7
Stückrath R, Quevedo R, de la Fuente L, Hernández A, Sepúlveda V, 2008. Effect of foliar application of calcium on the quality of blueberry fruits. J Plant Nutr 31: 1299-1312. https://doi.org/10.1080/01904160802135076
Walsh DB, Bolda MP, Goodhue RE, Dreeves AJ, Lee JC, Bruck DJ, Walton VM, O'Neal SD, Zalom FG, 2011. Drosophila suzukii (Diptera: Drosophilidae): invasive pest of ripening soft fruit expanding its geographic range and damage potential. J Integr Pest Manage 1: 1-7. https://doi.org/10.1603/IPM10010