Abstract
The spotted-wing drosophila (SWD), Drosophila suzukii (Matsumara) (Diptera: Drosophilidae), is a serious global pest. Understanding the drivers for its success is fundamental to develop sustainable management tools. Here we aim to gain further understanding of environmental influences, seasonal patterns, and landscape complexity that could promote population growth and dynamics of SWD in the Andean region. To achieve this, traps baited with apple cider vinegar were placed in the Andean region of Patagonia, where soft-skinned fruit farming is a key activity and SWD is well established. Traps were deployed in four transects, covering cultivated areas and non-crop habitats. Trap inspections were conducted twice per month during two years, with all SWD counted and sexed. Bycatch was also recorded. We observed SWD high abundances in summer and autumn across most environments, and sustained populations in the peripheral forest and wild blackberries year-round. Farms near forests experienced higher SWD populations in summer compared to those farther away. Successful management of this global pest should consider neighboring areas to farms as part of the deployed tactics. Incorporating this knowledge to future management strategies and predictive models for SWD could help reduce this pest´s damage, while minimizing the use of pesticides.
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Introduction
The spotted-wing drosophila (SWD), Drosophila suzukii (Matsumura) (Diptera: Drosophilidae), is a successful invader that generates serious negative impacts in fruticulture globally1. Native to southeast Asia, in the last decades the species has invaded many regions of the world including Europe and North America in 20082,3, South America in 20134,5, and northern Africa in 20176. Due to a combination of factors, which include the increased global trade in commercial goods, lack of effective control measures, the high reproductive rate of the species, its ability to move, and the wide range of plants it can attack, the species has increased its invaded range remarkably. In 2014 SWD was first detected in the Patagonia (Argentina), and in subsequent years, the species spread considerably in the country7,8. The relatively recent arrival of SWD to the region represents a serious concern, as is the case in many other fruit-producing regions at a global scale1.
Adults of the SWD are small, measure 2–3 mm and have a clear sexual dimorphism: female individuals are characterized by their serrated and sclerotized ovipositor, while males have a dark spot near the distal end of their wings. The species is polyphagous, and unlike other fruit flies that typically target damaged or overripe fruits, SWD females can lay eggs in fruits that are still attached to the plant either ripe or unripe9,10,11. They utilize their serrated ovipositor to pierce the fruit’s epidermis, causing physical damage and exposing the fruit to pathogens9,12, and lay their eggs inside the fruit. Hosts include both wild and cultivated plants, with soft-skinned crops such as strawberries, raspberries, and blueberries being the most affected, while within stone fruits, cherries and peaches are also used1,13. The species has a relatively short life cycle, with adult female reaching sexual maturity and oviposition capacity in as little as one or two days after pupation, resulting in up to 15 generations per year if conditions are favorable10,14,15. The species can tolerate a wide range of environmental conditions, with populations peaking toghether with the fruiting season and surviving winter mostly in the adult form, as a cold-tolerant morphotype16. The species is especially sensitive to temperature, with larval development being favored by temperatures between 16 and 25 °C and female oviposition within a range of 18 to 30 °C. Furthermore, increased relative humidity promotes oviposition and adult lifespan15. This sensitivity promotes populations in humid and cooler areas such as forests17,18,19.
Currently, management of SWD includes, in addition to the undesired use of pesticides, the widespread adoption of sustainable tactics such as cultural practices (e.g. drip irrigation and incorporation of weed matts), post-harvest measures (e.g. freezing fruit) and manipulation of their behavior through non-specific attractive and/or repellent chemical signals (e.g. mass-trapping, attract and kill)1. Despite these measures, SWD management is proving to be challenging in many regions of the world16. Factors such as organic production, baits not being specific (resulting in low efficiency in addition to affecting non-target species) and resistance to insecticides have hindered successful management in many regions1,20. In addition to these drawbacks, other sustainable strategies such as biocontrol through natural enemies and the sterile male technique are under development/research21,22. Additionally, inter-annual population fluctuations due to changing climatic conditions adds another layer of complexity to this challenging scenario17,23.
Given the current context and our still insufficient knowledge about the pest dynamics and promoters for population growth, it is important to develop a solid understanding of the fly’s biology and ecology at local scales. Previous studies, mostly conducted in Europe and North America have investigated drivers for population growth in these regions, but the pests biology and ecology in South America is still underrepresented24,25. In this context, the present study is aimed at describing variations of SWD adult abundance in relation varying environmental and climatic conditions in order to establish seasonal patterns in relation to habitat use. Here we aim to evaluate the effects that drive species abundance in relation to host availability through the year, including non-crop and crop hosts and their proximity to forest edges. Ultimately, this information will help advancing global ecological understanding of this pest within heterogenous landscapes to tailor and enhance SWD management strategies.
Results
General phenology
A total of 166.543 SWD were captured throughout the two years of sampling, with 80.939 females and 85.604 males. Additionally, 93.167 individuals of other insect species were found in traps. A strong seasonality for the three insect groups was observed with maximum levels occurring in late summer and autumn for SWD, and spring for other insect species (Fig. 1). Our results indicate higher overall abundances in the first sampling cycle (June 2021–2022) than in the second one (June 2022–2023) for SWD females (cycle 1 = 42 females/trap/capture date; cycle 2 = 19 females/trap/capture date z = -16; p < 0.0001), males (cycle 1 = 44 males/trap/capture date; cycle 2 = 21 males/trap/capture date z = -17; p < 0.0001), and “other species” (cycle 1 = 39 individuals/trap/capture date; cycle 2 = 31 individuals/trap/capture date z = -7; p < 0.0001). Mean temperatures showed typical continental seasonality with the highest records in the summer month of February (29 °C) and coldest in the winter, during the month of August (-1 °C).
Mean number of individuals captured monthly during the sampling period in vinegar baited traps including all environments sampled, with monthly average maximum and minimum temperatures obtained from data loggers placed in the field.
Environments and seasons
The sum of captured SWD females and males varied with Environment (Χ2 = 25.8; d.f. = 5; p < 0.0001) and Season (Χ2 = 824; d.f. = 3; p < 0.001). The overall number of SWD females was statistically different than male of SWD captures (z = 0.04; d.f. = 1; p < 0.001). Upon closer inspection, differences were found within and between sexes depending on the Environment and Season. More females than males were found overall in Cherries and Rosehip, and in Spring. In all other environments and seasons there were no differences between the sexes on SWD captures. Female fly captures varied with environments (Χ2 = 15.8; d.f. = 5; p < 0.01) and seasons (Χ2 = 785.2; d.f. = 3; p < 0.001). Similarly, male fly captures varied with environments (Χ2 = 19.0; d.f. = 5; p < 0.01) and seasons (Χ2 = 1150.5; d.f. = 3; p < 0.001). Captures of other insect species also resulted in significant differences between seasons (Χ2 = 1505.2; d.f. = 3; p < 0.001) and environments (Χ2 = 18.0; d.f. = 5; p < 0.01) (Fig. 2, Table A1, Table A2).
Effect of Environment and Season on captured female and male Drosophila suzukii and other insect species. Different lowercase letters indicate statistical differences within insect groups (i.e., red for SWD females, blue for SWD males and grey for other species) between different environments or seasons. ***, ** or NS above bars indicate statistical significances between male and female SWD within individual environments or individual seasons (* = p < 0.05; ** = p < 0.01; *** = p < 0.001; NS = p > 0.05).
Additionally, significant interaction effects were found between season and environment in the number of females (Χ2 = 322.2; d.f. = 15; p < 0.001), males (Χ2 = 296.1; d.f. = 15; p < 0.001), and other insect species (Χ2 = 136.3; d.f. = 15; p < 0.001). Contrasts were carried out for each of the insect groups (i.e., female SWD, male SWD and other species) considering the interaction between season and environment. Since comparisons are numerous and their interpretation can be complex, we present data, firstly aggregated within environments with contrasts made between seasons, and secondly, we aggregate data within seasons and contrasts made between environments (Fig. 3, Table A3). Within Environments, both SWD females and males showed the highest capture levels in summer and autumn, except for Native Forest, where flies were captured in similarly high level through the four Seasons. Captures in Cherries were high as of spring for females and summer for males. Captures in Rosehip were relatively low. Other insect species captured resulted in a different capture pattern than SWD, with the highest captures registered in spring for most environments, and winter and autumn with the lowest levels (Fig. 3).
Mean captures of Drosophila suzukii females, males and other insect species in vinegar-baited traps in different seasons (winter, spring, summer and autumn) and environments (berries, cherries, native forest, rosehip, tree curtain and wild blackberry). For better interpretation and visualization, the same capture data is presented in two different ways: one contrasting Seasons within Environments and the second one, contrasting Environments within Seasons. Different letters above data points represent statistical differences (p < 0.05) within boxes.
Spotted-wing drosophila abundance observed from a seasonal point of view, indicates that capture levels for female and male during winter were similar, with significantly more flies captured in the Native Forest and Wild Blackberry. Spring capture kept high mainly in the Native Forest. In summer capture levels were constant (i.e., no statistical differences) across Environments. In autumn, flies were captured consistently throughout Environments. Fly populations were high in Native Forest in winter and spring, whereas summer and autumn captures were similar through the different environments (Fig. 3).
Distance to forest edge
The number of SWD captured in traps was affected negatively by the increasing distance from the native edge to the point of capture during spring for SWD males and other species, and during summer for SWD females and males (Fig. 4, Table A4).
Effect of the distance between the sampled location to the forest edge (the variable was scaled) of Drosophila suzukii females, males and other insect species captured in vinegar traps. For both SWD sexes the effect was statistically significant in summer, registering lower captures as the distance of the trap to the edge of the forest increased. Additionally, a marginal significant effect was observed in spring for SWD males. * = p < 0.05, ** = p < 0.01, *** = p < 0.001, NS = p > 0.05. Even though in the model the Distance to the native edge was scaled, for clarity purpose in the figure the variable was back transformed.
Accumulated degree days and humidity
The weather in farms vs. forest edges resulted in significant differences depending on seasons (Fig. 5, Table A5). Relative humidity was higher (+3%) in winter in the forest edge, while lower (−3%) in summer. Maximum temperatures were consistently higher in farms during the whole year (1 °C), while minimum temperatures were consistently lower in farms (1 °C) relative to the forest. Accumulated degree days were higher in Spring and Autumn in farms (4 degree-days) vs. the forest.
Comparison of climatic variables (RH relative humidity, Max maximum temperatures; Min minimum temperature and Deg. days: Accumulated degree days) in the forest edge and farmed areas, obtained from data loggers placed in these two environments. Pairwise comparisons between the two environments were carried out with matched pairs t-test (** = p < 0.01 = **; p < 0.001 = ***; p > 0.05 = NS).
The number of captured insects was affected by the interaction between the degree days accumulated during the capture period and the average relative humidity for the same period for SWD females (z = 1.98; p < 0.05) and males (z = 2.33; p < 0.05). That is, the number of captured insects increased more steeply as degree days are accumulated depending on the average relative humidity (Fig. 6, Table A6).
Effect of accumulated degree days and mean relative humidity on Drosophila suzukii females and males (GLMM with negative binomial distribution). To represent graphically the interaction between accumulated degree days and relative humidity, we grouped this last term in three categories represented by red (Relative humidities above 82%), blue (Relative humidities between 70% and > 82%) and green (Relative humidities below 70%). Color coding was used irrespective of the significance of the interaction. Even though the model was performed with scaled response variables, here we plot it with the back-transformed variables.
Discussion
Given that current SWD management practices can have variable results, there is an urgent need to obtain quality information in relation to the relevance of different environments on the pest’s temporal patterns to tailor tactics to specific region and construct solid predictive population models. Our two-year study, indicates the species has a marked seasonality depending on the environment. As expected, SWD, a generalist species, is present in relatively high population levels in summer and autumn in all environments sampled, while in winter and spring the species concentrates in the native forest and wild blackberries. The studied region, despite being set in the Andes Mountain range, has mild winters due to its low altitude. The combination of these climatic conditions (capture levels of SWD females and males were driven significantly with increased accumulated degree days and higher levels of humidity), along with a complex vegetation matrix that includes native forest and patches of the invasive blackberry, contributes to observed high abundances of SWD.
The high quantities of flies captured in our vinegar traps were also observed in previous studies using similar traps baited with apple cider vinegar in invaded regions. A study conducted in Germany, during seven years using vinegar traps, registered 756.768 male and female SWD (1081 flies/trap /year), with maximum capture levels of ca. 2000 individuals/trap/15 days in forest edges17. This is similar to our observations where we registered 166.543 male and females captured (1601 flies/trap/year). Our record capture was of 3076 male and female SWD captured in a single trap in wild blackberries. A second study carried out in the US across several states, resulted in variable levels of captures. States that were affected SWD (Arkansans, North Carolina and Arkansas) had capture levels of between 30 and 53 flies /trap/week, whereas our weekly average was for the equivalent period was of 39 flies/trap/week26. A third study carried out in Northeast China resulted in an overall average 24 flies/week/trap27. Despite the differences in sampling protocols, the overall capture levels seem to be similar in both regions.
Fly abundances were notably high in the Native forest and Wild blackberries, whereas these abundances were found to be at intermediate levels in the Tree curtains and interestingly lowest in Berry farms and Cherry trees. Spotted-wing drosophila was more abundant during 2021–2022 (first sampling cycle) than during 2022–2023 (second one). The drivers for the differences we observed between years are unknown. Although it was not part of the scope of the present study, one possible reason could have been favorable climatic conditions during the cycle prior to the beginning of our study (i.e. 2020–2021). At a seasonal level, flies were more abundant in summer and reached the highest level in autumn, peaking in the month of May, while the lowest levels were found in winter and spring. Our results contradict previous field studies15 indicating that females can outnumber males in winter. We observed similar numbers of females and males in winter and only in spring we found more females than males. It’s important to note that we did not measure infestation levels in fruit nor economic impact, and that the use of vinegar traps to monitor SWD can be misleading to calculate actual sex ratios and even population levels. This is because fly behavioral responses to traps are context and seasonal dependent and can be affected by factors such as temperature, humidity or resource availability28,29. In this scenario, estimations of actual population levels need to consider that summer morph flies prefer ripe fruit rather than vinegar traps, therefore our results during the fruiting season are probably underestimated. Conversely the winter morph does not discriminate30. Furthermore, capture experiments carried out in tart cherry orchards by Kirkpatrick31 calculated that for every fly captured, there were 192 free ones in an area of 2.7 ha during the fruiting season. In this context our capture results need to be interpreted with caution.
Over the course of our two-year study, in traps baited with apple cider vinegar, we captured nearly twice as many SWD individuals than all other insect species combined (166.543 vs. 93.167 individuals respectively). Even though this broad insect category lacks the desired taxonomic detail since it grouped all specimens that fell in traps that were not identified as SWD, it indicates the relative high abundance of the pest vs. other insects attracted to vinegar or those that simply fell in traps by accident. This difference also highlights the contrasting phenology between both groups. The category of “Other insects” peaks in spring while the SWD in late summer and autumn. This information could be useful when developing new behavioral manipulation tactics based on vinegar baits (e.g. mass trapping or attract and kill), with our results suggesting that, for instance, the use of vinegar-based baits should be minimized in spring to avoid negative impacts on these other insect species, nevertheless the efficiency of deployment needs to be evaluated in full.
A detailed analysis of SWD abundance in the forest edges shows consistently high population levels year-round, making it the only environment studied with stable and high fly abundances. Contrastingly, in all other environments, SWD was found in reduced abundances in winter and spring particularly. Our study confirms observations from previous researchers, indicating that forests can act as reservoirs for SWD12,18,32, with landscape complexity promoting fly abundance33. The native forest that surrounds the productive valley, appears to serve as a year-round reservoir for the SWD due to its lower thermal amplitude compared to cultivated areas. It is known that the fly is highly sensitive to dry weather and temperature extremes15, and this environment, as in other invaded areas, appears to provide favorable micro-climatic conditions, food, in addition to oviposition substrates. In the forest, temperatures are lower in the summer and higher in winter when compared to farms. Interestingly farms have higher humidity levels during summer, which is unexpected, but could be the result of the artificial irrigation taking place in the berry fields. Our results show that locations closer to the forest experienced higher fly abundances than those further away in the summer months exclusively. Other studies found similar patterns with results indicating that farms closer to more complex environments, had higher fly populations by the effect of daily and seasonal spillover19,34,35,36. Further studies are needed to fully understand the available resources (food and oviposition substrates in the forest).
Wild blackberries seem to offer not only refuge for the SWD in colder months, probably due to its dense branch structure, but also serve as substrate for oviposition, stimulating the high population levels observed in traps associated to this environment/species. Rubus ulmifolius is a highly invasive plant native to Europe and Asia and found in high densities in the studied area37. It grows on the sides of roads and vacant land between cultivated areas. This opportunistic species can reproduce sexually and asexually, growing rapidly up to 3 m tall, bearing high fruit densities, especially in late summer, thus offering an ideal SWD population growth substrate.
Previous studies have also found marginal Blackberry plants promoting SWD population levels38,39. As in other parts of the world, this species, when left unmanaged can reach high densities in areas such as abandoned fields and roadsides, resulting in an especially good candidate for maintaining and driving fly populations. A more detailed analysis is warranted to fully understand the effect of wild blackberries on the high densities observed. Our study did not measure fruit infestation in crop areas, therefore the correlation between adult flies and larval infestation needs to be confirmed in berry farms.
Interestingly, the abundance of SWD adults captured in baited traps located in Berry farms does not stand out compared to other environments during the fruiting season. The heterogenous landscape in which berry farms are located, the proximity to forest edges, and the presence of the invasive blackberry may influence the relatively low capture levels observed in Berry farms during the coldest months. Expectedly, in months where berry plants bear no fruits, farms have the lowest capture levels, conversely in summer and autumn, when berries ripen, farms had comparable levels of capture to all other environments. Previous studies have found that wild blackberries were as or more susceptible to SWD oviposition at all ripeness stages than the cultivated blackberries38.
In this challenging context, management strategies in the Andean region should contemplate area-wide pest management12,40. This approach seeks to coordinate sustainable and preventive strategies, targeting not only cultivated areas but also urban, uncultivated, and wild sectors to which the pest has access, thus preventing pest development in sites close to crops and minimizing pesticide use. Landscape structure (i.e., composition and configuration) greatly influences the abundance, distribution, diversity, and population dynamics of insects. Certain factors, such as changes in resource availability over time, SWD dispersal patterns, and the selection of specific environments while searching for food, shelter, or oviposition sites, are relevant to consider when adapting or developing new management tools and plans to specific crops and areas to maximize the likelihood of success1.
Our study suggests that managing SWD in such diverse landscapes with mild climates, will be especially challenging due to high SWD levels year-round and its presence in all sampled environments, which seem to provide abundant resources and favorable conditions such as the native forest and wild blackberry. In this context, an area-wide control and tools such as sterile male and biological control agents will be1. The continued use of cultural approaches and tactics that involve baits will be essential, but will be not sufficient. Additional actions coordinated at regional levels with strong support from local and regional goverments, encompassing an Area Wide management approach, will be essential24,41. In this sense, as technologies become available, the timely combination of the sterile insect technique successfully applied in other regions42 together with effective augmentative release of parasitoids1,43 and behavioral manipulation methods using push–pull or mass trapping (during the winter season in non-crop habitats such as forest edges)44, could help in the reduction of fly populations levels in the Andean region. Additionally, managing key alternative hosts at the local level such as the wild blackberry, will be essential to complement the actions taken to reduce pest population levels in fruit-producing regions of the Andes. During this process, incorporating further knowledge on the pest biology into these future management strategies will be fundamental in reducing the population of this pest at the regional level, while minimizing the use of pesticides.
Materials and methods
Study site
The study was conducted in the Andean region of Patagonia regionally known as “Comarca Andina” (Patagonian Andean Shire, PAS), between June 30, 2021, and June 16, 2023. The region, located between latitudes 41°09’ and 42°20’ S, encompasses the localities of El Bolsón, El Hoyo, and Lago Puelo (Fig. 1). The region has a rich agricultural history spanning over 60 years, with raspberry (Rubus idaeus L.) farming being the backbone of its economy. The PAS region represents Argentina’s primary berry-producing area, distinguished by its high concentration of organic raspberry farmers45.
The region’s agricultural success is supported by its unique geographical and ecological characteristics. Situated in low valleys (approximately 200 m.a.s.l.), the area features fertile soils and is characterized by a diverse, heterogeneous landscape combining crop and non-crop habitats. Mixed native forests border the valley edges, while the lowland areas comprise a complex matrix of urban settlements, agricultural patches, and multipurpose grasslands. Due to its low elevation, the region experiences milder winters and warmer summers compared to surrounding areas, creating favorable conditions for berry cultivation.
Traps and transects
To sample SWD adults, 52 translucent plastic containers (500 ml) with lids were used. These containers had 8 perforations of 3 mm diameter in the upper third of the container and were filled with 200 ml of apple cider vinegar (Casalta, Argentina). These traps were arranged in 4 transects (Fig. 7) extending from the adjacent forest to the center of the productive valley including the peripheral forest, agricultural areas and semi-urban zones. The transects were laid out loosely to accommodate the terrain’s irregularities, the arrangement of farms, and general accessibility. Consequently, the lengths, relative positions, and trap spacing varied among transects.
© OpenStreetMap contributors, available under the Open Database License (ODbL). Aerial view of the study area Comarca Andina, Argentina, -42.038369, -71.527287. Retrieved May 20, 2024 from https://www.openstreetmap.org/search?query=bolson#map=12/-42.0564/-71.4916. Modified by ASM using JMP v. 17.1.0 and Krita v. 4.4.1.
The Patagonian Andean Shire is in Northern Patagonia (Argentina), and is set in low valleys with moderate temperatures, ideal for berry farming. A sampling protocol consisting of 52 traps set in 4 transects was set up near El Bolsón and El Hoyo to investigate Drosophila suzukii spatiotemporal dynamics. Traps were assigned to different environments, including berry farms, cherries, native forest, rosehip, tree curtains and wild blackberries. Satellite images generated with Mapbox
Traps were hung in different habitats (i.e., “Environments”) which included: Raspberry farms (n = 12), Cherries (Prunus avium L., n = 9), Native forest (the edges of the productive valley are delimited by a hard edge composed of a mixed forest, with species such as Austrocedrus chilensis D. Don, Luma apiculata Burret, Nothofagus domeyii Oerst, n = 4), Rosehip (Rosa rubiginosa L., n = 7), Tree curtains (small patches of tall trees, mainly poplars (Populus spp.) and pine trees (Pinus spp), positioned strategically to minimize the effect of wind on crops, n = 7) and Wild blackberries (Rubus ulmifolius Schott, an invasive berry found in high densities in this particular region, n = 13) (Table 1). Within each of the 4 transects, the distance to the “native edge” was recorded for each trap (i.e., “distance to native edge”), considering the trap placed at the forest edge as distance = 0 m, with distances increasing toward the center of the valley. Although not all environments could be represented in all transects, we ensured placement of one trap in “Native forest” and at least one in a “Berry farm” per transect.
Traps were hung 1.6 m above the ground, shaded most of the day by branches and inspected at 15-day intervals for 2 years. At each inspection, the vinegar from traps was filtered through a fine mesh strainer to retain all captured insects, which were preserved individually in 96% ethanol for later classification in the laboratory under a binocular microscope. After filtering, traps were re-baited with new vinegar (200 ml). In case of trap damage (due to for example, sun deterioration or wind action), the whole trap was replaced. All SWD individuals found in traps per date were counted and sexed. Furthermore, all other insects found in traps were counted and classified as “other species”, with no further taxonomic classification.
Temperature and relative humidity sensors/loggers (Onset Computer Corporation, USA) were placed in the field. We positioned two data loggers per transect: one located in the forest edge and the second one in a berry farm, both in proximity to the traps (< 2 m). Sensors were hung at 1.6 m from the ground, below a plastic disc (6 cm diameter) that covered the sensor from direct sunlight. The sum of daily degree days was calculated for each sensor location and revision interval (ca. 15 days), using the 7.2 minimum temperature threshold as specified by Kamiyama46. Note that during short periods some of the dataloggers failed, resulting in minimal data loss.
Data analysis
Overview
We investigated the magnitude of the variables of interest in modulating the captured insects via a series of models. Depending on the response and effect of interest, as response variables we used the number of insects captured (SWD females, SWD males or other species of insects), while Season (winter, spring, summer and autumn), Environment (berries cultivated in farms, cherries, native forest, rosehip, tree curtains and wild blackberries), Distance to native edge and Climatic variables (accumulated degree days and relative humidity) were used as independent variables. Models also included random factors: Trap code (1–52, as categoric variable), Transect (1–4, as categoric variable) nested in Locality (El Bolsón, El Hoyo), and Cycle (first and second sampling year, as categories). The proceess for model selection was based on Akaike’s information criterion while the validation was done using the DHARMa package to asses model fit. All statistical analyses were performed with R Software version 4.4.147. Generalized linear mixed models were fitted using the glmmTMB package v. 1.1.948. For some models, post hoc pairwise comparisons were made using Tukey´s HSD test (R package: emmeans, function: pairs) to establish contrasts between the different levels of the independent variables of interest49.
General phenology
To test the effect of Sampling cycle on the number of captured SWD females, males and other species, we performed three GLMMs, with Negative Binomial distribution and log link function, with the number of captures of each insect group as response variables, Sampling cycle as explanatory variable, and Locality and Transect as random factors.
Environment and season
To test for general variations of female and male SWD captures due to the Environment and Season independently, we did GLMMs with Negative Binomial distribution and log link function and evaluated the number of insects captured as the response variable, sex as the independent variable and either Season or Environment as random factors: Environment when Season was evaluated as main effect and Season when Environment was evaluated as main effect. We also included as random factors Sampling Cycle and Locality, Transect and Trap code. Using the same model rationale, variations in the captures of other insect species were also evaluated against Environment and Season. We then evaluated the effect of the interaction of Environment and Season on female, male and other species. These last models contemplated the Sampling cycle, Locality, Transect and Trap code as random factors.
Distance to forest edge
The effect of the distance of the traps to the native forest edge was evaluated with a GLMM with a Negative Binomial distribution and log link function. Response variables were females, males and other insect species independently. As the predictor we contemplated the scaled distance between the trap (for each value the mean was subtracted and divided by the standard deviation) and the edge of the forest in meters. Captures from traps located in the native forest (distance = 0 m) were not included in this analysis. Given the contrasting seasonal behaviour of insects, the distance effect was analyzed by Season. As random factors we used Sampling cycle, Locality and Transect.
Accumulated degree days and humidity
Climate data on different seasons across the two years was firstly analyzed to compare data acquired by data loggers in forest edges vs. farms. For this, statistical comparisons were carried out using pairwise t-tests with data paired between data loggers placed in the same transect for the forest edge and the farm. Secondly the effect of weather variables on SWD captures was also evaluated. For this two GLMMs with a Negative Binomial distribution and log link function were carried out: as response variables we used the number of SWD (males or females) captured during each revision interval in traps associated to data loggers as the response variable. As explanatory variables we used the interaction between the accumulated degree days and the mean Relative Humidity. Both factors were scaled (the mean was subtracted from each value and divided by the standard deviation), and as random factors we included Cycle and Location/Transect.
Data availability
Data available upon reasonable request to ASM.
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Acknowledgements
We would like to thank the private-land owners in the PAS that welcomed us to their farms to conduct the study: Chacra Aitué, Chacra Castrillo, Chacra Castiñeria, Chacara Arroyo Claro, Chacra Graziosi, Chacra Delgado, Chacra de Szudruk, Chacra La Huala and Chacra Las Acacias.
Funding
This research was funded by ImpaCT.AR N18 (MINCyT Argentina), Proyecto Disciplinario 106, Proyecto Disciplinario 101 and Proyecto local (Instituto Nacional de Tecnología Agropecuaria Argentina).
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Conceptualization AM, DF, MM, MG and VC; All authors planned and conducted the field sampling; FF identified the specimens in the lab. AM and MM carried out the statistical analysis. Resources VC, MM, AC and AM. AM wrote the first draft of the manuscript. All authors have read and agreed to the published version of the manuscript.
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Martínez, A.S., Germano, M.D., Chillo, V. et al. Understanding key population drivers of the spotted wing Drosophila in cultivated and natural areas in the Andes. Sci Rep 15, 6208 (2025). https://doi.org/10.1038/s41598-025-90147-4
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DOI: https://doi.org/10.1038/s41598-025-90147-4
