The olive fruit fly, Bactrocera oleae, has been a key pest of olives in Europe and North America. We conducted the largest exploration for parasitoids associated with the fly across Sub-Saharan Africa (Kenya, Namibia, and South Africa) including some of the fly's adjoining regions (Canary Islands, Morocco, Réunion Island and Tunisia). From Sub-Saharan regions, four braconids were collected: Bracon celer, Psytallia humilis, P. lounsburyi, and Utetes africanus. Results showed that their regional dominance was related to climate niches, with P. humilis dominant in hot semi-arid areas of Namibia, P. lounsburyi dominant in more tropical areas of Kenya, and U. africanus prevalent in Mediterranean climates of South Africa. Psytallia concolor was found in the Canary Islands, Morocco and Tunisian, and the Afrotropical braconid Diachasmimorpha sp. near fullawayi on Réunion Island. Furthermore, we monitored the seasonal dynamics of the fly and parasitoids in Cape Province of South Africa. Results showed that fruit maturity, seasonal variations in climates and interspecific interactions shape the local parasitoid diversity that contribute to the low fly populations. The results are discussed with regard to ecological adaptations of closely associated parasitoids, and how their adaptations impact biocontrol.

Background

As global climate change and exponential human population growth intensifies pressure on agricultural systems, the need to effectively manage invasive insect pests is becoming increasingly important to global food security. Drosophila suzukii is an invasive pest that drastically expanded its global range in a very short time since 2008, spreading to most areas in North America and many countries in Europe and South America. Preliminary ecological modeling predicted a more restricted distribution and, for this reason, the invasion of D. suzukii to northern temperate regions is especially unexpected. Investigating D. suzukii phenology and seasonal adaptations can lead to a better understanding of the mechanisms through which insects express phenotypic plasticity, which likely enables invasive species to successfully colonize a wide range of environments.

Results

We describe seasonal phenotypic plasticity in field populations of D. suzukii. Specifically, we observed a trend of higher proportions of flies with the winter morph phenotype, characterized by darker pigmentation and longer wing length, as summer progresses to winter. A laboratory-simulated winter photoperiod and temperature (12:12 L:D and 10 °C) were sufficient to induce the winter morph phenotype in D. suzukii. This winter morph is associated with increased survival at 1 °C when compared to the summer morph, thus explaining the ability of D. suzukii to survive cold winters. We then used RNA sequencing to identify gene expression differences underlying seasonal differences in D. suzukii physiology. Winter morph gene expression is consistent with known mechanisms of cold-hardening such as adjustments to ion transport and up-regulation of carbohydrate metabolism. In addition, transcripts involved in oogenesis and DNA replication were down-regulated in the winter morph, providing the first molecular evidence of a reproductive diapause in D. suzukii.

Conclusions

To date, D. suzukii cold resistance studies suggest that this species cannot overwinter in northern locations, e.g. Canada, even though they are established pests in these regions. Combining physiological investigations with RNA sequencing, we present potential mechanisms by which D. suzukii can overwinter in these regions. This work may contribute to more accurate population models that incorporate seasonal variation in physiological parameters, leading to development of better management strategies.

The vine mealybug (VMB), Planococcus ficus (Hemiptera: Pseudococcidae), is a key insect pest of vineyards, and improvements in sustainable control of this pest are needed to meet increasing consumer demand for organically farmed products. One promising option is mating disruption. In a series of experiments conducted from 2004 to 2007, we tested the effects of mating disruption on trap captures of Pl. ficus males in pheromone-baited traps, on Pl. ficus numbers and age structure on vines, and on damage to grape clusters. From 2004 to 2005, the effects of dispenser load (mg active ingredient per dispenser) were also assessed, and dispensers were compared to a flowable formulation. Across all trials, mating disruption consistently reduced pheromone trap captures and often reduced mealybug numbers on vines and/or crop damage, regardless of the pheromone dose that was applied. Reductions in Pl. ficus densities in mating disruption plots were not accompanied by clear effects on mealybug population age structure; however, production of non-viable ovisacs by unmated females may have obscured differences in proportional representation of ovisacs. Pheromone trap captures were never lowered to zero (often called trap shut down), possibly because trials were conducted in vineyards with unusually high Pl. ficus densities. Trap-capture patterns in both treated and control plots commonly began low in April-May, increased in mid-July or August, and often decreased in September-October when post-harvest insecticides were applied. During the four-year trial, the release rate from plastic sachet dispensers was improved by industry cooperators as pheromone was released too quickly (2004) or not completely released during the season (2005-2006). The flowable formulation performed slightly better than dispensers at the same application dose. Results over all years suggest season-long coverage or late-season coverage may be as or more important than dose per hectare. Development of a dispenser with optimized season-long pheromone emission or targeted seasonal periods should be a future goal.

Determining the most likely source of an invasive pest species might help to improve their management by establishing efficient quarantine measures and heading the search of efficient biological control agents. Planococcus ficus is an invasive mealybug pest of vineyards in Argentina, California, Mexico, Peru and South Africa. This mealybug pest had a previously known geographic distribution spanning southern Europe, the Middle East, and parts of northern Africa. In North America, Pl. ficus was first discovered in the early 1990s and soon thereafter in Mexico. To determine the origin of invasive populations in North America, Pl. ficus from California and Mexico were compared with material throughout its presumptive native range in the Mediterranean region, as well as material collected from an older invasion in South Africa and recently invaded Argentina. From each sample location, genomic DNA was sequenced for the nuclear internal transcribed spacer one (ITS1) and the mitochondrial cytochrome c. oxidase one (CO1). Phylogenetic analyses of CO1, ITS1 and concatenated CO1 and ITS1 data-sets using Bayesian and neighbor-joining analysis support two major divisions: a European grouping (Europe, Tunisia, Turkey) and a Middle Eastern grouping (Israel and Egypt). The invasive populations in Argentina and South Africa align with the European group and the invasive populations in North America align with the Middle Eastern group, with one Israel sample aligning closely with the North American clade, suggesting that Israel was the origin of those populations.

The invasion of Drosophila suzukii, spotted-wing drosophila, across Europe and the US has led to economic losses for berry and cherry growers, and increased insecticide applications to protect fruit from damage. Commercial production relies heavily on unsustainable use of conventional toxic insecticides. Non-toxic insecticide strategies are necessary to alleviate the disadvantages and non-target impacts of toxic conventional insecticides and improve Integrated Pest Management (IPM). A novel food-grade gum deployed on dispenser pads (GUM dispensers) was evaluated to mitigate D. suzukii crop damage in five commercial crops and nine locations. Trials were conducted at a rate of 124 dispensers per hectare in cherry, wine grape, blueberry, raspberry, and blackberry in California and Oregon, USA during 2019 and 2020. The majority of trials with the food-grade gum resulted in a reduction of D. suzukii egg laying in susceptible fruit. In some cases, such damage was reduced by up to 78%. Overall, results from our meta-analysis showed highly significant differences between GUM treatments and the untreated control. Modeling simulations suggest a synergistic reduction of D. suzukii damage when used in combination with Spinosad (Entrust SC) insecticide. These data illustrate commercial value of this tool as a sustainable alternative to manage D. suzukii populations within a systems approach.

Temperature-dependent fecundity and survival data was integrated into a matrix population model to describe relative Drosophila suzukii Matsumura (Diptera: Drosophilidae) population increase and age structure based on environmental conditions. This novel modification of the classic Leslie matrix population model is presented as a way to examine how insect populations interact with the environment, and has application as a predictor of population density. For D. suzukii, we examined model implications for pest pressure on crops. As case studies, we examined model predictions in three small fruit production regions in the United States (US) and one in Italy. These production regions have distinctly different climates. In general, patterns of adult D. suzukii trap activity broadly mimicked seasonal population levels predicted by the model using only temperature data. Age structure of estimated populations suggest that trap and fruit infestation data are of limited value and are insufficient for model validation. Thus, we suggest alternative experiments for validation. The model is advantageous in that it provides stage-specific population estimation, which can potentially guide management strategies and provide unique opportunities to simulate stage-specific management effects such as insecticide applications or the effect of biological control on a specific life-stage. The two factors that drive initiation of the model are suitable temperatures (biofix) and availability of a suitable host medium (fruit). Although there are many factors affecting population dynamics of D. suzukii in the field, temperature-dependent survival and reproduction are believed to be the main drivers for D. suzukii populations.

Drosophila suzukii Matsumura (spotted wing drosophila) has recently become a serious pest of a wide variety of fruit crops in the United States as well as in Europe, leading to substantial yearly crop losses. To enable basic and applied research of this important pest, we sequenced the D. suzukii genome to obtain a high-quality reference sequence. Here, we discuss the basic properties of the genome and transcriptome and describe patterns of genome evolution in D. suzukii and its close relatives. Our analyses and genome annotations are presented in a web portal, SpottedWingFlyBase, to facilitate public access.

Drosophila suzukii causes economic damage to berry and stone fruit worldwide. Laboratory-generated datasets were standardized and combined on the basis of degree days (DD), using Gompertz and Cauchy curves for survival and reproduction. Eggs transitioned to larvae at 20.3 DD; larvae to pupae at 118.1 DD; and pupae to adults at 200 DD. All adults are expected to have died at 610 DD. Oviposition initiates at 210 DD and gradually increases to a maximum of 15 eggs per DD at 410 DD and subsequently decreases to zero at 610 DD. These data were used as the basis for a DD cohort-level population model. Laboratory survival under extreme temperatures when DD did not accumulate was described by a Gompertz curve based on calendar days. We determined that the initiation of the reproductive period of late dormant field-collected female D. suzukii ranged from 50 to 800 DD from January 1. This suggests that D. suzukii females can reproduce early in the season and are probably limited by availability of early host plants. Finally, we used the DD population model to examine hypothetical stage-specific mortality effects of IPM practices from insecticides and parasitoids at the field level. We found that adulticides applied during the early season will result in the largest comparative population decrease. It is clear from model outputs that parasitism levels comparable to those found in field studies may have a limited effect on population growth. Novel parasitoid guilds could therefore be improved and would be valuable for IPM of D. suzukii.