1. Introduction
Agricultural intensification, particularly habitat simplification, landscape homogenization, and intensive use of pesticides and fertilizers, is leading to global declines in arthropods [1,2,3], thus decreasing the provision of ecosystem services such as natural pest control [4,5]. Organic farming is a promising approach for enhancing natural enemies of pest species and, consequently, their effectiveness in pest control [6,7,8]. However, benefits of organic farming on pest control seem to be less prominent in perennial crops such as grapevine than in annual crops [9,10] and may depend on the landscape context [6,11]. Complex landscapes with higher proportions of seminatural areas often support higher levels of natural pest control [6,12,13]. Adjacent seminatural habitats, particularly woody vegetation, can promote natural enemies such as lacewings, spiders, predatory mites, rove beetles, and hymenopteran parasitoids in vineyards [14,15]. Nevertheless, adverse effects of landscape complexity on the occurrence of natural enemies, as well as on insect pest infestations, are also possible [16,17,18,19,20] and may be explained by higher resource supply in crops such as vineyards compared to the surrounding seminatural habitats [21,22]. In addition, during specific life stages, pests may also benefit from certain resources in seminatural habitats [21].
Furthermore, local vineyard management practices such as implementation of flower-rich cover-crop mixtures can enhance abundance of predatory mites, hymenopteran parasitoids, spiders, earwigs, and carabids [20,23,24]. Flower strips promote natural pest control in adjacent fields when tailored to the requirements of the target natural enemy taxa [25]. Thus, it can be expected that natural pest control is enhanced in vineyards sown with diverse cover-crop mixtures. However, it may be important to distinguish the effects of cover-crop mixtures relative to bare ground or relative to spontaneous vegetation in inter-rows as some authors showed higher arthropod diversity in vineyards with native ground cover [26]. Benefits of cover-crops over spontaneous vegetation have been studied less than their benefits relative to bare ground.
The European grapevine moth Lobesia botrana (Denis and Schiffermüller, 1775) (Lepidoptera: Tortricidae) is one of the major grapevine pests in Europe. In Europe, two to four generations of the polyphagous L. botrana [27] occur per year, with typically two (rarely three) generations occurring in Austria [28]. Larvae of the first generation feed on inflorescences, while those of the following generations damage berries, often resulting in Botrytis cinerea infections. Several taxa, including Dermaptera, Hemiptera, Neuroptera, Diptera, and Coleoptera, as well as ants and several families of spiders and mites, predate on L. botrana [29,30,31]. Furthermore, numerous parasitic Hymenoptera, particularly Trichogramma species and the ichneumonid Campoplex capitatior, attack different stages of L. botrana [32,33,34]. Several of these natural enemies are susceptible to fungicides such as sulfur and copper, both of which are frequently applied in organic viticulture instead of the predominant synthetic fungicides applied in conventional or integrated vineyards [35,36,37,38]. As fungicides are more effective when sprayed preventatively than curatively [39,40], they are the most frequently used pesticides in viticulture with several sprayings per year. There is growing demand from winegrowers for less harmful synthetic fungicides, which is reflected in comparably low nontarget effects of most of the synthetic fungicides [41]. Thus, it is unclear whether the widely observed benefits of organic farming to natural enemies and pest suppression [6] are present in current viticulture.
The aim of this study was to investigate the combined effects of organic farming, cover-crop management, and landscape composition on natural pest control of grape berry moths. We hypothesize that predation pressure on L. botrana is promoted by (i) organic compared to integrated management, (ii) diverse cover-crop mixtures, and (iii) heterogenous landscapes with high percentage of woody seminatural habitats. Furthermore, we aimed to identify the most important predators of L. botrana in Austrian vineyards. 2. Materials and Methods 2.1. Study Sites
We investigated 16 pairs of vineyards situated between the western shore of Lake Neusiedl and the Leithaberg hills (47°54′55″ north (N); 16°41′40″ east (E)) in eastern Austria (Figure 1). Each vineyard pair consisted of one vineyard under organic and one under integrated pest management. Inter-row management of cover-crops differed in both organic and integrated vineyards, resulting in three types of cover-crop management: species-rich cover-crop mixtures (20–34 species seeded), species-poor cover-crop mixtures (4–9 species), and spontaneous vegetation (no seeding of cover-crops for at least 5 years). The climate of the study region is warm temperate [42]; in 2019, the average temperature was 12.4 °C and total annual precipitation was 414 mm, which was warmer and dryer in comparison with the last 10 years (11.6 °C and 574 mm) [43]. While large continuous parts of the landscape consist of vineyards (Figure 1), winegrowers manage mostly small (0.25–1.5 ha; on average 0.74 ± 0.66 ha), long, and elongated units (hereafter “vineyards”) consisting of only a few rows which were organized in a trellis system.
In each vineyard, vegetation parameters were recorded in spring (April) and summer (July). Vegetation cover (%) was visually estimated in one inter-row per vineyard in four 1 × 1 m sub-plots. Vegetation height was measured 10 times in the corresponding row and the two adjacent inter-rows with the drop disc method [44] in spring and summer, using a round sanding pad with a surface of 0.04 m2 and a weight per unit area of 1.9 kg/m2. Vineyard management information (including spraying regimes and tillage practices) was collected through personal semistructured interviews with winegrowers of the studied vineyards. Grape berry moths were controlled with mating disruption pheromones in the study region. Area-related acute pesticide toxicity load contact (aAPTLc) for applied pesticides was calculated on the basis of contact acute median lethal dose (LD50) values for honeybees according to Möth et al. [45]. Management information for organic vs. integrated vineyards and different cover-crop managements are provided in Table 1 and Table 2 (for more detailed information, see Table S1, Supplementary Materials).
2.2. Predation Rate Assessment
To assess the pest control potential of grape berry moths, we exposed sentinel cards consisting of both eggs and pupae of L. botrana. For rearing of L. botrana, we followed the methods of Markheiser et al. [46]. Inside of the rearing containers, retainers were installed to allow oviposition on exchangeable polyethylene strips. Egg-laden strips were harvested after 24 h. Eggs were distributed relatively evenly, resulting in an average number of 52 ± 17 eggs per strip. Pupae were harvested from rearing cups. Five pupae were attached to each strip using duct tape (HEB19L10GC, TOOLCRAFT, Conrad Electronic SE, Hirschau, Germany). The remaining adhesive surface was covered with sand to prevent predators from sticking. Sentinel cards were stored at 4 °C until exposure.
To determine predation rates, sentinel cards were attached to randomly selected 1 year old branches and were exposed there for 72 h. We exposed five sentinel cards per vineyard four times between June and August 2019 (3 June, 1 July, 30 July, 26 August) aligning with four phenological stages of the vines (full flowering, berry touch, veraison, and before harvest). The numbers of eggs and pupae were counted before and after exposure (for more detailed information, see Table S1, Supplementary Materials).
To determine the most important predators of L. botrana eggs and pupae, additional sentinel cards were exposed, and predation was monitored with four cameras in one of the vineyard pairs (one organic and one integrated). This was repeated eight times between June and August of 2019, resulting in 64 camera observations. We used a camera system consisting of a raspberry pi computer (Raspberry Pi Foundation, UK) and a camera module with two infrared light-emitting diodes (IR-LEDs; Electreeks, Dresden, Germany). A power-bank (Voltcraft PB-19) allowed the camera system to run for 24 h in the vineyards. The camera systems were placed in plastic containers to protect them from moisture and mounted on wooden poles which were driven into the ground with a distance of about 30 cm between cameras and sentinel cards. The cameras were programmed to take a picture every 10 s for 24 h. 2.3. Landscape Analysis
Landscape composition was analyzed in 500 m buffers around each studied vineyard. According to the available base maps and field mapping, land use was categorized following the EUNIS (European Nature Information System) habitat type classification [47] and later digitized in ArcGIS 10.6 [48]. Relative proportions of habitat types were calculated in ArcGIS 10.6, whereas landscape indices were computed with the R package “landscapemetrics” [49]. Due to our paired design, landscape composition was very similar in each pair of organic and integrated vineyards. The “average” landscape composition was characterized by 60.5% ± 16.6% agricultural area, of which 44.3% ± 15.7% was planted with vineyards, and 29.4% ± 13.7% seminatural habitats, of which 13.4 ± 15.0% were woody. The average distance of the studied vineyards to the next woody seminatural habitat was 23.4 ± 19.3 m, and the Shannon landscape diversity index was 1.49 ± 0.23.
2.4. Data Analysis
We summed predation data over all sampling dates and replicates per vineyard, resulting in one observation for each vineyard. All statistical analyses were done in R version 3.6.3 [50]. The distribution of response and predictor variables was checked visually using “qqp” (R package car) [51]. Multicollinearity among these predictor variables was evaluated by calculation of correlation matrices (function “corrplot”, R package corrplot) [52]. Correlation of predictor variables with factorial management options (organic/integrated; cover-crop management) was evaluated using linear and generalized linear models according to distribution of response variables (functions “lm” and “glm”). Summer vegetation and bare ground cover, amount of compost and artificial fertilizer, number of applications with pesticides in general, sulfur, copper, synthetic fungicides, insecticides, and herbicides, as well as aAPTLc, were correlated with the farming type and were, therefore, not included in the modeling process (compare Table 1). Effects on egg and pupae predation rates were analyzed using linear mixed-effect models (function “lmer”, package lme4) [53]. Models contained “vineyard pair” as a random factor and “cover-crop” (species-poor/species-rich/spontaneous), “management” (organic/integrated), and “proportion of woody seminatural habitats” as fixed predictor variables. A post hoc test was performed to differentiate significances in the variable “cover-crop” (“Tukey”, function “glht”, package multcomp) [54]. Assumptions were checked for all models using graphical validation procedures [55].
3. Results
On average, 85.6% of L. botrana eggs and 82.5% of L. botrana pupae were predated during the sampling period. Contrary to our expectations, predation of L. botrana pupae was increased on average by 10% in integrated compared to organic vineyards (Table 3, Figure 2A). Furthermore, predation was 10% higher in vineyards with spontaneous vegetation compared to species-poor cover-crops, with species-rich cover-crops showing intermediate values (Table 3, Figure 2B). Landscape composition had no clear effect on the predation of L. botrana pupae. Predation of L. botrana eggs was not influenced by vineyard management, implementation of cover-crops, or landscape composition (Table 3, Figure 2C,D). Predation rates of L. botrana pupae increased during summer, while egg predation rates slightly decreased during the same period (Figure 3).
We observed 455 arthropod individuals on the exposed sentinel cards, of which 178 individuals of 18 taxa actively predated or parasitized L. botrana. Predation and parasitism mainly occurred at dusk or throughout the night (88% nocturnal pupae predation, 60% nocturnal egg predation/parasitism; Table 4). Dominant predators were earwigs (Forficulidae), bush crickets (Orthoptera: Tettigoniidae), and ants (Formicidae). While ant densities were higher in organic than in integrated vineyards, densities of earwigs were higher in integrated vineyards, which was in accordance with the positive effect of integrated farming on L. botrana pupae predation (Table 4). For Orthoptera, more individuals were recorded in the organic vineyard, but the number of species was equal in both management types (n = 4). Selected photographs of the most frequent predators are displayed in Figure 4.
4. Discussion
Pupae predation increased over the season from a range of 55–62% during full flowering of grapevine to 80–95% before harvest. The increase in canopy architecture in the course of this vegetation period offers more habitat for natural enemies [56,57]. Furthermore, in correspondence to their life cycle, several natural enemies are more active during summer than during spring (e.g., bush crickets). A slight decrease in predation rates in early July and late August could be observed for both L. botrana pupae and eggs, which may be correlated to high temperatures during August. Hot weather conditions may impact parasitoids and predators and result in changes in feeding niches [58,59]. Nevertheless, predation rates were generally relatively high with about 80% for pupae and 85% for eggs. For comparison, Pennington et al. [29] detected L. botrana egg predation rates of about 35% in Germany, while, in France, on average 42% of eggs and 86% of larvae were predated [11]. The difference in predation rates could be attributed to either the landscape-scale usage of mating disruption pheromones against grape berry moths in the Austrian study region (i.e., covering both organic and integrated vineyards for over 10 years), thereby reducing the insecticide use drastically, whereas, in Bordeaux, insecticides were applied both in organic and in conventional vineyards [11]. Furthermore, the small size of the elongated vineyards in our study region consisting only of a few vine rows could lead to a larger contact area between vineyards and surrounding seminatural areas (i.e., stronger edge effects), which could facilitate natural pest control in comparison to larger, more quadratic shaped vineyards in Bordeaux [11] and the Palatinate winegrowing region [29]. The positive influence on pest control in elongated fields with a higher perimeter-to-area ratio was also shown in other studies for annual cropping systems [4,60,61]. This effect can be attributed to shorter distances from edges to fields and a larger contact zone between crop fields and adjacent seminatural habitats.
Counterintuitively, organic farming did not enhance natural pest control, but actually reduced pupae predation rates. This can be explained by the higher number of pesticide applications in organic vineyards that include a high frequency of nonspecific fungicides such as copper and sulfur, resulting in aAPTLc values that were twice as high as those in integrated vineyards (see Table 1). Sulfur is well known for its negative effects on a wide variety of natural enemies in viticulture with one of the highest IOBC (International Organisation for Biological and Integrated Control) toxicity ratings [38]. Fungicide applications with copper, sulfur, and potassium bicarbonate also reduced the number of natural enemies and egg predation in Germany [29]. Moreover, Muneret et al. [11] found increased egg predation but unaltered larval predation on grape berry moths with decreasing pesticide use, although pesticide use was lower in organic compared to conventional vineyards in France. Pesticide input was twice as high in conventional compared to organic vineyards in this French study [19]. This difference in pesticide input in organic vs. conventional/integrated vineyards could be related to different pesticide use in Austria and France. In Bordeaux, 6% of the applied pesticides were insecticides against grape berry moths and leafhoppers [19], whereas, in Austria, insecticides were only applied once in two vineyards. In general, fungicides are the most commonly applied pesticides in viticulture, representing 96% of all applications [62]. Due to the fact that mainly pesticide application frequency led to differences between organic and conventional viticulture in our study, we highlight the impact of fungicide toxicity to nontarget organisms. Reduced pesticide applications and/or implementation of less harmful substances are a promising approach to enhance natural pest control in vineyards [10,29] and should be considered in agri-environmental schemes.
We detected the highest pupae predation rates in vineyards with spontaneous vegetation cover. Contrastingly, L. botrana egg predation rates were higher in Germany in an experimental vineyard sown with flower-rich cover-crops compared to spontaneous vegetation [33]. Native cover-crop species enhanced arthropod diversity in South African vineyards [26] and natural enemy abundance and predation on light brown apple moth in Australia [63]. Furthermore, predator abundances of spiders, earwigs, and ants are negatively affected by tillage intensity [24,64,65]. Moreover, higher L. botrana infestations were recorded in vineyards which were frequently tilled compared to those planted with cover-crops in Italy [65]. In our study, bare soil vineyards were absent, but tillage intensity was lowest in vineyards with spontaneous vegetation, which could also explain the higher predation rates in those vineyards. Furthermore, herbicides were only applied in four integrated vineyards with species-poor cover-crops (only underneath the vines). Tillage frequency in the rows was higher in organic vineyards. These disturbance factors might have affected predator occurrence and pest control in our study. Possible benefits of diverse spontaneous vegetation or flower-rich cover-crops which provide resources for predatory arthropods should be considered in agri-environmental schemes in viticulture.
Unexpectedly, neither egg predation nor pupae predation was affected by landscape composition. Similarly, L. botrana infestation and predator abundance were not affected by proportion of seminatural habitats in France [19,64], while L. botrana egg predation even decreased with increasing proportion of seminatural habitats [11]. In the same region, Papura et al. [31] showed that harvestmen (which are important predators of grape berry moths) populations increased with increasing proportions of seminatural habitats at the landscape scale. Gonçalves et al. [66] observed a general decrease in predator abundance with increasing proportions of seminatural habitats. In the same study, ant abundance in vineyards increased with an increasing proportion of large-scale vineyards (500–750 m radius) and small-scale seminatural habitats (125–250 m radius). Contrarily, Thomson and Hoffmann [15] found increased abundance of natural enemies and parasitism of pest moth eggs in vineyards adjacent to woody vegetation in Australia. We assume that perennial crops such as vineyards provide enough food resources and shelter for agrobiont species such as earwigs and ants to accomplish their whole life cycle within the field, mitigating the effects of surrounding landscapes [66,67,68,69]. Spillover effects between seminatural habitats and crops that are observed in annual crops may be less relevant in vineyards [70]. In particular, when diverse vegetation cover is implemented in vineyard inter-rows, landscape effects may become negligible [20,71].
Even though the pictures of natural enemies of L. botrana were taken in only two of the studied vineyards and are, therefore, not representative for the whole study region, they provide valuable insights into the range of natural enemies of L. botrana. We captured 178 natural enemies predating actively on L. botrana in photographs, highlighting particularly the pest control potential of earwigs, ants, and bush crickets. Camera observations from vineyards in New Zealand revealed highest predation activities in grapevine canopies from earwigs [72]. Similarly, Pennington et al. [29] confirmed L. botrana egg predation by ants, earwigs, and green lacewings with camera-surveilled sentinel cards. Interestingly, we detected the highest activity of natural enemies at dusk and at night, which agrees with the results of Frank et al. [72], finding 50–60% nocturnal predation activity.
Earwigs prey on lepidopteran pest eggs, larvae, and pupae [72,73], but may be problematic in vineyards when occurring at high densities due to possible feeding on grape berries, contamination of grape bunches with feces, and spread of fungal pathogens, which decrease the must quality of the grapes [74,75]. Although earwigs can fly, their abundance on cherry trees was limited by isolation from other woody habitats [76]. In contrast, earwig abundance was affected neither by plant species richness or landscape composition nor by organic vs. conventional management in apple orchards [67]. However, pesticide reduction in apple orchards enhanced earwigs and other natural enemies and, thus, the control of woolly aphids [77]. In accordance with their reliance on ground vegetation during their early life stages, earwigs were more abundant in Spanish vineyards with spontaneous vegetation compared to bare soil and sown flower-rich cover-crops [24]. In our study, integrated vineyards received less fungicides and, therefore, had lower toxicity values, which accordingly promoted earwig occurrence and L. botrana predation. Thus, higher earwig occurrence and, correspondingly, more natural pest control can be expected in vineyards with minimal disturbance in terms of soil tillage and pesticide load.
Ants can impede the biological control of mealybugs and aphids, protecting them from natural enemies while feeding on their honeydew [65,78]. Due to this fact, ants are undesired in some winegrowing regions. Nevertheless, native ant communities did not affect other arthropod predators and predation rates on moth pests in Australian vineyards [79]. In addition, ants are major natural enemies of various pests, including moths, in blueberry, corn, and grasslands in the United States (US) [80]. Ant densities were not influenced by landscape compositions in cherry orchards in Switzerland or in vineyards in Portugal [66,81], but abundances were increased in organic vs. conventional vineyards and under implementation of cover-crops vs. tillage in Italy [65,82]. Ants were also more prevalent on the recorded sentinel cards in the organic vineyards in this study, which could be attributed either to ants’ higher tolerance toward pesticide toxicity or to avoidance strategies, as seen by higher earwig abundance in integrated vineyards.
Many bush crickets, such as the two Phaneroptera species observed in this study as the most dominant predators of L. botrana pupae (Table 4), are omnivores that can feed both on (young) plant parts and on pests of grapevine [83,84,85]. Other bush crickets (Meconema meridionale, M. thalassinum, and Tettigonia viridissima) are almost exclusively carnivorous [86] and known to prey on pests such as leaf miners, chrysomelids, and green leafhoppers [87,88,89]. Interestingly, our study is the first to show the large potential of bush crickets for grape berry moth control in Austrian vineyards, whereas bush crickets themselves are sometimes considered pests in other regions such as California [84,85].
5. Conclusions
We found small but positive effects of spontaneous vegetation and integrated farming on natural pest control of L. botrana pupae in Austrian vineyards. The comparably negative effect of organic viticulture is most likely related to the negative nontarget effects of frequent sulfur (and copper) applications on arthropods in combination with the avoidance of strongly damaging insecticides by integrated winegrowers. The long-term use of mating disruption pheromones against the grape berry moths has greatly reduced the necessity of insecticide use in the study region. This shows that management practices such as organic farming, which are often considered positive for biodiversity and pest control, need to be judged on a case-by-case basis. Furthermore, fungicide use also varies within organic and integrated vineyards, indicating a potential for fungicide reduction. New, fungus-resistant varieties offer an interesting opportunity for more sustainable viticulture by allowing fungicide reductions of up to 95% [57]. Furthermore, agri-environmental schemes (e.g., Austrian agri-environmental program) should promote the use of spontaneous vegetation cover or species-rich cover-crop mixtures to increase biodiversity and associated ecosystem services such as natural pest control in vineyards.
Enlarge this image.Figure 2. Differences in predation rates of L. botrana pupae (A,B) and eggs (C,D) between management systems (A,C) and implementation of cover-crops (B,D). Model predicted means and standard errors are displayed. Significant differences according to Tukey test are indicated by different letters.
Enlarge this image.Figure 3. Mean predation rates of L. botrana pupae and eggs in organic and integrated vineyards for four sampling dates (3 June 2019, 1 July 2019, 30 July 2019, 26 August 2019).
Enlarge this image.Figure 4. Predators photographed on sentinel cards. Selected pictures of (A) Formicidae, (B) Forficula auricularia, (C) Phaneroptera nana (male), and (D) Tettigonia viridissima (female).
| Organic | Integrated | |
|---|---|---|
| aAPTLc | 19.95 ± 6.88 | 10.61 ± 14.93 |
| Total number of pesticide applications | 9.69 ± 1.74 | 6.31 ± 2.30 |
| Copper applications | 8.88 ± 1.89 | 1.25 ± 0.86 |
| Sulfur applications | 9.19 ± 1.64 | 4.13± 1.89 |
| Applications with synthetic fungicides | – | 5.75 ± 2.67 |
| Insecticide applications | – | 0.25 ± 0.45 |
| Acaricide applications | 0.25 ± 0.45 | 0.38 ± 0.50 |
| Herbicide applications | – | 0.31 ± 0.60 |
| Compost fertilizer (m3/ha) | 3.28 ± 5.06 | 0.63 ± 2.50 |
| Artificial fertilizer (kg/ha) | – | 31.25 ± 68.01 |
| Tillage frequency in inter-rows | 1.00 ± 0.97 | 1.19 ± 1.47 |
| Tillage frequency in rows | 2.81 ± 0.83 | 2.50 ± 1.51 |
| Years without tillage in inter-rows | 2.63 ± 1.40 | 2.31 ± 1.99 |
| Mulching frequency in inter-rows | 2.00 ± 1.32 | 2.13 ± 0.96 |
| Rolling frequency in inter-rows | 0.44 ± 0.81 | 0.81 ± 1.33 |
| Inter-row vegetation height in spring (cm) | 11.45 ± 9.90 | 10.70 ± 8.97 |
| Row vegetation height in spring (cm) | 3.83 ± 2.90 | 5.93 ± 4.23 |
| Inter-row vegetation height in summer (cm) | 10.88 ± 7.43 | 10.13 ± 8.55 |
| Row vegetation height in summer (cm) | 8.90 ± 12.30 | 6.33 ± 4.84 |
| Vegetation cover in spring (%) in inter-rows | 82.38 ± 19.44 | 80.84 ± 20.03 |
| Vegetation cover in summer (%) in inter-rows | 61.70 ± 22.85 | 40.36 ± 25.43 |
| Bare ground cover in spring (%) in inter-rows | 12.59 ± 19.59 | 11.09 ± 14.74 |
| Bare ground cover in summer (%) in inter-rows | 11.75 ± 10.31 | 20.23 ± 11.14 |
| Species-Poor | Species-Rich | Spontaneous | |
|---|---|---|---|
| Tillage frequency in inter-rows | 1.00 ± 1.21 | 1.28 ± 1.38 | 0.83 ± 0.98 |
| Tillage frequency in rows | 2.33 ± 0.89 | 3.29 ± 1.2 | 1.83 ± 1.17 |
| Years without tillage in inter-rows | 1.42 ± 1.38 | 2.29 ± 1.14 | 1.33 ± 1.37 |
| Mulching frequency in inter-rows | 2.58 ± 1.24 | 1.71 ± 1.07 | 1.83 ± 0.75 |
| Rolling frequency in inter-rows | 0.42 ± 0.79 | 1.07 ± 1.38 | – |
| Inter-row vegetation height in spring (cm) | 16.17 ± 13.62 | 7.89 ± 3.09 | 6.63 ± 2.05 |
| Row vegetation height in spring (cm) | 4.45 ± 2.98 | 3.58 ± 3.07 | 4.72 ± 2.32 |
| Inter-row vegetation height in summer (cm) | 10.14 ± 8.54 | 11.18 ± 8.27 | 8.98 ± 4.33 |
| Row vegetation height in summer (cm) | 5.31 ± 3.04 | 9.38 ± 14.19 | 9.19 ± 5.99 |
| Vegetation cover in spring in inter-rows (%) | 75.79 ± 25.19 | 86.56 ± 8.76 | 75.87 ± 28.24 |
| Vegetation cover in summer in inter-rows (%) | 44.48 ± 24.88 | 51.98 ± 29.07 | 49.14 ± 22.15 |
| Bare ground cover in spring in inter-rows (%) | 13.75 ± 21.40 | 8.31 ± 7.64 | 13.06 ± 17.74 |
| Bare ground cover in summer in inter-rows (%) | 14.44 ± 9.79 | 16.23 ± 12.83 | 18.80 ± 10.13 |
| Herbicide applications in rows | 0.42 ± 0.67 | – | – |
| Management (Integrated/Organic) | Implementation of Cover-Crops (Species-Poor/Species-Rich/Spontaneous) | Proportion of Woody Seminatural Habitats | ||||
|---|---|---|---|---|---|---|
| χ² | p | χ² | p | χ² | p | |
| L. botrana eggs | 1.69 | 0.193 | 1.28 | 0.528 | 0.01 | 0.918 |
| L. botrana pupae | 11.76 | <0.001 | 6.46 | 0.040 | 0.52 | 0.469 |
| Individuals Captured on Photos | Individuals Involved in Predation or Parasitism | Predated L. botrana Pupae | Predation or Parasitism Incidents on L. botrana Eggs | |||||
|---|---|---|---|---|---|---|---|---|
| Organic | Integrated | Organic | Integrated | Organic | Integrated | Organic | Integrated | |
| Acari | ||||||||
| Anystidae | – | 2 (0) | – | 2 (0) | – | – | – | 2 (0) |
| Trombidiidae | – | 2 (1) | – | 2 (1) | – | – | – | 2 (1) |
| Araneae | ||||||||
| cf. Cheiracanthium sp. | 7 (7) | 9 (9) | 2 (2) | 3 (3) | – | – | 2 (2) | 3 (3) |
| cf. Drassodes sp. | – | 1 (1) | – | – | – | – | – | – |
| cf. Ebrechtella tricuspidata | 2 (0) | – | 1 (0) | – | – | – | 1 (0) | – |
| cf. Marpissa muscosa | – | 3 (0) | – | – | – | – | – | – |
| cf. Philodromus sp. | 1 (1) | – | 1 (1) | – | – | – | 1 (1) | – |
| cf. Pseudicius encarpatus | – | 2 (0) | – | – | – | – | – | – |
| cf. Salticidae | 1 | 6 (0) | – | – | – | – | – | – |
| Cheiracanthium sp. | 6 (6) | – | 1 (1) | – | 1 (1) | – | – | – |
| Salticidae | 1 (0) | – | 1 (0) | – | – | – | 1 (0) | – |
| Salticus sp. | 1 (0) | – | – | – | – | – | – | – |
| Coleoptera | ||||||||
| Carabidae | 6 (6) | 2 (2) | 2 (2) | 2 (2) | 7 (7) | 4 (4) | – | – |
| Coccinellidae | – | 1 (0) | – | – | – | – | – | – |
| Curculionidae | 1 (0) | – | – | – | – | – | – | – |
| sp. | 1 (0) | 1 (0) | – | – | – | – | – | – |
| Dermaptera | ||||||||
| Forficula auricularia | 38 (36) | 57 (51) | 16 (15) | 34 (30) | 16 (12) | 52 (46) | 9 (7) | 8 (6) |
| Diptera | ||||||||
| sp. | 13 (1) | 6 (1) | – | – | – | – | – | – |
| Hymenoptera | ||||||||
| Formicidae | 95 (24) | 118 (22) | 46 (20) | 13 (2) | 6 (1) | – | 27 (9) | 13 (2) |
| parasitic wasp | 17 (16) | 21 (15) | 16 (16) | 15 (11) | – | – | 16 (16) | 15 (11) |
| Lepidoptera | ||||||||
| sp. | – | 1 (0) | – | – | – | – | – | – |
| Neuroptera | ||||||||
| Chrysopidae (adult) | – | 1 (1) | – | 1 (1) | – | – | – | 1 (1) |
| Chrysopidae (larvae) | 2 (2) | – | 2 (2) | – | – | – | 2 (2) | – |
| Opiliones | ||||||||
| sp. | 1 (1) | – | – | – | – | – | – | – |
| Orthoptera | ||||||||
| Leptophytes albovittata | – | 1 (1) | – | – | – | – | – | – |
| Meconema meridionale | – | 2 (2) | – | 2 (2) | – | 9 (9) | – | – |
| Meconema thalassinum | – | 2 (2) | – | 2 (2) | – | 3 (3) | – | – |
| Oecanthus pellucens | 1 (1) | – | – | – | – | – | – | – |
| Phaneroptera falcata | 7 (6) | – | 5 (4) | – | 15 (13) | – | – | – |
| Phaneroptera nana | 4 (4) | – | 3 (3) | – | 13 (13) | – | – | – |
| Tettigonia viridissima | 1 (1) | 4 (4) | 1 (1) | 3 (3) | 5 (5) | 10 (10) | – | – |
Supplementary Materials
The following are available online at https://www.mdpi.com/2075-4450/12/3/220/s1: Table S1. Detailed vineyard management and predation data for 32 studied Austrian vineyards.
Author Contributions
J.M.R., M.H.E., S.M., C.H., and S.W. conceptualized the ideas and designed the methodology; C.H.'s lab delivered sentinel cards; T.H. and S.M. performed the experiment; A.W. determined arthropods at order or family level; M.K. identified orthoptera and S.K. identified spider specimens from photos; J.M.R. led the data analysis and writing. All authors contributed critically to the drafts and gave final approval for publication. All authors have read and agreed to the published version of the manuscript.
Funding
This study is part of the project "SECBIVIT" funded through the 2017/2018 Belmont Forum and BiodivERsA joint call for research proposals, under the BiodivScen ERA-Net COFUND program, and with the following funding organizations: Agencia Estatal de Investigación (Ministerio de ciencia e innovación/Spain), Austrian Science Fund (FWF grant number I 4025-B32), Federal Ministry of Education and Research (BMBF/Germany), VDI/VDE-IT Projektträger, French National Research Agency (ANR), Netherlands Organization for Scientific Research (NWO), National Science Foundation (NSF), and Romanian Executive Agency for Higher Education, Research, Development, and Innovation Funding (UEFISCDI). Open Access Funding by the Austrian Science Fund (FWF)
Institutional Review Board Statement
Not applicable.
Data Availability Statement
All data are provided in the article and the Supplementary Materials.
Acknowledgments
We are grateful to all collaborating winegrowers and to Argyroula Tsormpatzidou for rearing Lobesia botrana and preparing sentinel cards. We would like to thank Markus Redl, Ahmad Aldelemi, Elias Holzknecht, Lina Weissengruber, Lisa Sitavanc, and Vincenzo Diecidue for support during field work and Božana Petrovic for landscape mapping.
Conflicts of Interest
The authors declare no conflict of interest.
1. Hallmann, C.A.; Sorg, M.; Jongejans, E.; Siepel, H.; Hofland, N.; Schwan, H.; Stenmans, W.; Müller, A.; Sumser, H.; Hörren, T.; et al. More than 75 percent decline over 27 years in total flying insect biomass in protected areas. PLoS ONE 2017, 12, e0185809.
2. Sánchez-Bayo, F.; Wyckhuys, K.A.G. Worldwide decline of the entomofauna: A review of its drivers. Biol. Conserv. 2019, 232, 8-27.
3. Seibold, S.; Gossner, M.M.; Simons, N.K.; Blüthgen, N.; Müller, J.; Ambarlı, D.; Ammer, C.; Bauhus, J.; Fischer, M.; Habel, J.C.; et al. Arthropod decline in grasslands and forests is associated with landscape-level drivers. Nature 2019, 574, 671-674.
4. Bianchi, F.J.J.A.; Booij, C.J.H.; Tscharntke, T. Sustainable pest regulation in agricultural landscapes: A review on landscape composition, biodiversity and natural pest control. Proc. R. Soc. B Biol. Sci. 2006, 273, 1715-1727.
5. Gurr, G.M.; Wratten, S.D.; Luna, J.M. Multi-function agricultural biodiversity: Pest management and other benefits. Basic Appl. Ecol. 2003, 4, 107-116.
6. Bengtsson, J.; Ahnström, J.; Weibull, A.-C. The effects of organic agriculture on biodiversity and abundance: A meta-analysis: Organic agriculture, biodiversity and abundance. J. Appl. Ecol. 2005, 42, 261-269.
7. Puig-Montserrat, X.; Stefanescu, C.; Torre, I.; Palet, J.; Fabregas, E.; Dantart, J.; Arrizabalaga, A.; Flaquer, C. Effects of organic and conventional crop management on vineyard biodiversity. AEE 2017, 243, 19-26.
8. Muneret, L.; Mitchell, M.; Seufert, V.; Aviron, S.; Djoudi, E.A.; Pétillon, J.; Plantegenest, M.; Thiéry, D.; Rusch, A. Evidence that organic farming promotes pest control. Nat. Sustain. 2018, 1, 361.
9. Bruggisser, O.T.; Schmidt-Entling, M.H.; Bacher, S. Effects of vineyard management on biodiversity at three trophic levels. Biol. Conserv. 2010, 143, 1521-1528.
10. Reiff, J.M.; Ehringer, M.; Hoffmann, C.; Entling, M.H. Fungicide reduction favors the control of phytophagous mites under both organic and conventional viticulture. AEE 2021, 305, 107172.
11. Muneret, L.; Auriol, A.; Thiéry, D.; Rusch, A. Organic farming at local and landscape scales fosters biological pest control in vineyards. Ecol. Appl. 2018, 29, e01818.
12. Veres, A.; Petit, S.; Conord, C.; Lavigne, C. Does landscape composition affect pest abundance and their control by natural enemies? A review. AEE 2013, 166, 110-117.
13. Paredes, D.; Rosenheim, J.A.; Chaplin-Kramer, R.; Winter, S.; Karp, D.S. Landscape simplification increases vineyard pest outbreaks and insecticide use. Ecol. Lett. 2021, 24, 73-83.
14. Serée, L.; Rouzes, R.; Thiéry, D.; Rusch, A. Temporal variation of the effects of landscape composition on lacewings (Chrysopidae: Neuroptera) in vineyards. Agric. For. Entomol. 2020, 22, 274-283.
15. Thomson, L.J.; Hoffmann, A.A. Vegetation increases the abundance of natural enemies in vineyards. Biol. Control. 2009, 49, 259-269.
16. Gonçalves, F.; Carlos, C.; Aranha, J.; Torres, L. Does habitat heterogeneity affect the diversity of epigaeic arthropods in vineyards? Agric. For. Entomol. 2018, 20, 366-379.
17. Judt, C.; Guzmán, G.; Gómez, J.A.; Cabezas, J.M.; Entrenas, J.A.; Winter, S.; Zaller, J.G.; Paredes, D. Diverging Effects of Landscape Factors and Inter-Row Management on the Abundance of Beneficial and Herbivorous Arthropods in Andalusian Vineyards (Spain). Insects 2019, 10, 320.
18. Karp, D.S.; Chaplin-Kramer, R.; Meehan, T.D.; Martin, E.A.; DeClerck, F.; Grab, H.; Gratton, C.; Hunt, L.; Larsen, A.E.; Martínez-Salinas, A.; et al. Crop pests and predators exhibit inconsistent responses to surrounding landscape composition. Proc. Natl. Acad. Sci. USA 2018, 115, e7863-e7870.
19. Muneret, L.; Thiéry, D.; Joubard, B.; Rusch, A. Deployment of organic farming at a landscape scale maintains low pest infestation and high crop productivity levels in vineyards. J. Appl. Ecol. 2018, 55, 1516-1525.
20. Wilson, H.; Miles, A.F.; Daane, K.M.; Altieri, M.A. Landscape diversity and crop vigor outweigh influence of local diversification on biological control of a vineyard pest. Ecosphere 2017, 8, e01736.
21. Tscharntke, T.; Karp, D.S.; Chaplin-Kramer, R.; Batáry, P.; DeClerck, F.; Gratton, C.; Hunt, L.; Ives, A.; Jonsson, M.; Larsen, A.; et al. When natural habitat fails to enhance biological pest control-Five hypotheses. Biol. Conserv. 2016, 204, 449-458.
22. Rusch, A.; Binet, D.; Delbac, L.; Thiéry, D. Local and landscape effects of agricultural intensification on Carabid community structure and weed seed predation in a perennial cropping system. Landsc. Ecol. 2016, 31, 2163-2174.
23. Burgio, G.; Marchesini, E.; Reggiani, N.; Montepaone, G.; Schiatti, P.; Sommaggio, D. Habitat managementof organic vineyard in Northern Italy: The role of cover plants management on arhtropod functional biodiversity. Bull. Entomol. Res. 2016, 106, 759-768.
24. Sáenz-Romo, M.G.; Veas-Bernal, A.; Martínez-García, H.; Ibáñez-Pascual, S.; Martínez-Villar, E.; Campos-Herrera, R.; Marco-Mancebón, V.S.; Pérez-Moreno, I. Effects of Ground Cover Management on Insect Predators and Pests in a Mediterranean Vineyard. Insects 2019, 10, 421.
25. Albrecht, M.; Kleijn, D.; Williams, N.M.; Tschumi, M.; Blaauw, B.R.; Bommarco, R.; Campbell, A.J.; Dainese, M.; Drummond, F.A.; Entling, M.H.; et al. The effectiveness of flower strips and hedgerows on pest control, pollination services and crop yield: A quantitative synthesis. Ecol. Lett. 2020.
26. Eckert, M.; Mathulwe, L.L.; Gaigher, R.; Joubert van der Merwe, L.; Pryke, J.S. Native cover crops enhance arthropod diversity in vineyards of the Cape Floristic Region. J. Insect Conserv. 2020, 24, 133-149.
27. Thiéry, D.; Moreau, J. Relative performance of European grapevine moth (Lobesia botrana) on grapes and other hosts. Oecologia 2005, 143, 548-557.
28. Svobodová, E.; Trnka, M.; Žalud, Z.; Semerádová, D.; Dubrovský, M.; Eitzinger, J.; Štěpánek, P.; Brázdil, R. Climate variability and potential distribution of selected pest species in south Moravia and north-east Austria in the past 200 years-Lessons for the future. J. Agric. Sci. 2014, 152, 225-237.
29. Pennington, T.; Reiff, J.M.; Theiss, K.; Entling, M.H.; Hoffmann, C. Reduced fungicide applications improve insect pest control in grapevine. BioControl 2018, 63, 687-695.
30. Marchesini, E.; Monta, L.D. Observations on natural enemies of Lobesia botrana (Den. & Schiff.)(Lepidoptera, Tortricidae) in Venetian vineyards. Boll. di Zool Agrar e di Bachic 1994, 26, 201-230.
31. Papura, D.; Roux, P.; Joubard, B.; Razafimbola, L.; Fabreguettes, O.; Delbac, L.; Rusch, A. Predation of grape berry moths by harvestmen depends on landscape composition. Biol. Control. 2020, 150, 104358.
32. Bagnoli, B.; Lucchi, A. Parasitoids of Lobesia botrana (Den. & Schiff.) in Tuscany. IOBC/WPRS Bull. 2006, 29, 139-142.
33. Hoffmann, C.; Köckerling, J.; Biancu, S.; Gramm, T.; Michl, G.; Entling, M.H. Can Flowering Greencover Crops Promote Biological Control in German Vineyards? Insects 2017, 8, 121.
34. Xuéreb, A.; Thiéry, D. Does natural larval parasitism of Lobesia botrana (Lepidoptera: Tortricidae) vary between years, generation, density of the host and vine cultivar? Bull. Entomol. Res. 2006, 96, 105-110.
35. Thomson, L.J.; Glenn, D.C.; Hoffmann, A.A. Effects of sulfur on Trichogramma egg parasitoids in vineyards: Measuring toxic effects and establishing release windows. Aust. J. Exp. Agric. 2000, 40, 1165-1171.
36. Thomson, L.J.; Hoffmann, A.A. Field validation of laboratory-derived IOBC toxicity ratings for natural enemies in commercial vineyards. Biol. Control. 2006, 39, 507-515.
37. G#xFC;ven, B.; Göven, M.A. Side effects of pesticides used in cotton and vineyard areas of Aegean Region on the green lacewing, Chrysoperla carnea (Steph.) (Neuroptera: Chrysopidae), in the laboratory. IOBC/WPRS Bull. 2003, 26, 21-24.
38. Nash, M.A.; Hoffmann, A.A.; Thomson, L.J. Identifying signature of chemical applications on indigenous and invasive nontarget arthropod communities in vineyards. Ecol. Appl. 2010, 20, 1693-1703.
39. Battaglin, W.A.; Sandstrom, M.W.; Kuivila, K.M.; Kolpin, D.W.; Meyer, M.T. Occurrence of azoxystrobin, propiconazole, and selected other fungicides in US streams, 2005-2006. Water Air Soil Pollut. 2011, 218, 307-322.
40. Viret, O.; Siegfried, W.; Dubuis, P.H.; Gindro, K. Falscher Rebenmehltau; Eidgenössisches Departement für Wirtschaft, Bildung und Forschung WBF, Agroscope, AMTRA: Lausanne, Switzerland, 2014; pp. 1-2.
41. Verzeichnis Zugelassener Pflanzenschutzmittel-Weinbau. Deutsches Pflanzenschutzmittelregister. Available online: https://apps2.bvl.bund.de/psm/jsp/ListeMain.jsp?page=1&ts=1610276481000 (accessed on 10 January 2021).
42. Rubel, F.; Brugger, K.; Haslinger, K.; Auer, I. The climate of the European Alps: Shift of very high resolution Köppen-Geiger climate zones 1800-2100. Meteorol. Z. 2017, 26, 115-125.
43. Wetterstatistik. BOKU Institut für Pflanzenschutz. Available online: http://rebschutz.boku.ac.at (accessed on 20 March 2020).
44. Holmes, C.W. The Massey grass meter. Dairy Farming Annu. 1974, 26-30.
45. Möth, S.; Walzer, A.; Redl, M.; Petrović, B.; Hoffmann, C.; Winter, S. Unexpected effects of local management and landscape composition on predatory mites and their food resources in vineyards. Insects 2021, 12, 180.
46. Markheiser, A.; Rid, M.; Biancu, S.; Gross, J.; Hoffmann, C. Physical factors influencing the oviposition behaviour of European grapevine moths Lobesia botrana and Eupoecilia ambiguella. J. Appl. Entomol. 2018, 142, 201-210.
47. EUNIS Habitat Type. European Environment Agency (EEA). Available online: https://eunis.eea.europa.eu/habitats.jsp/ (accessed on 29 September 2016).
48. ArcGIS Desktop. Environmental System Research Institute. Available online: http://desktop.arcgis.com/de/ (accessed on 23 October 2019).
49. Hesselbarth, M.H.K.; Sciaini, M.; With, K.A.; Wiegand, K.; Nowosad, J. Landscapemetrics: An open-source R tool to calculate landscape metrics. Ecography 2019, 42, 1648-1657.
50. The R Development Core Team. R: A language and Environment for Statistical Computing; R Foundation for Statistical Computing: Vienna, Austria, 2015.
51. Fox, J.; Weisberg, S. An R Companion to Applied Regression, 3rd ed.; SAGE Publications: Thousand Oaks, CA, USA, 2019.
52. Wei, T.; Simko, V.R. Package "Corrplot": Visualization of a Correlation Matrix. R Package Version 0.84, 2017. Available online: https://github.com/taiyun/corrplot (accessed on 13 April 2020).
53. Bates, D.; Mächler, M.; Bolker, B.; Walker, S. Fitting Linear Mixed-Effects Models Using lme4. J. Stat. Softw. 2015, 67.
54. Hothorn, T.; Bretz, F.; Westfall, P.; Heiberger, R.M.; Schuetzenmeister, A.; Scheibe, S.; Hothorn, M.T. Package 'Multcomp'. Simultaneous Inference in General Parametric Models; Project for Statistical Computing: Vienna, Austria, 2016.
55. Zuur, A.; Ieno, E.N.; Walker, N.; Saveliev, A.A.; Smith, G.M. Mixed Effects Models and Extensions in Ecology with R. In Statistics for Biology and Health; Springer: New York, NY, USA, 2009.
56. Langellotto, G.A.; Denno, R.F. Responses of invertebrate natural enemies to complex-structured habitats: A meta-analytical synthesis. Oecologia 2004, 139, 1-10.
57. Pennington, T.; Kraus, C.; Alakina, E.; Entling, M.H.; Hoffmann, C. Minimal pruning and reduced plant protection promote predatory mites in grapevine. Insects 2017, 8, 86.
58. Drieu, R.; Rusch, A. Conserving species-rich predator assemblages strengthens natural pest control in a climate warming context. Agric. For. Entomol. 2016, 19, 52-59.
59. Reinecke, A.; Thiéry, D. Grapevine insect pests and their natural enemies in the age of global warming. J. Pest. Sci. 2016, 89, 313-328.
60. Östman, Ö.; Ekbom, B.; Bengtsson, J. Landscape heterogeneity and farming practice influence biological control. Basic Appl. Ecol. 2001, 2, 365-371.
61. Kragten, S.; de Snoo, G.R. Bio-Support: Modelling the impact of landscape elements for pest control. Proc. Neth. Entomol. Soc. Meet. 2004, 15, 93-97.
62. Bereswill, R.; Golla, B.; Streloke, M.; Schulz, R. Entry and toxicity of organic pesticides and copper in vineyard streams: Erosion rills jeopardise the efficiency of riparian buffer strips. AEE 2012, 146, 81-92.
63. Danne, A.; Thomson, L.J.; Sharley, D.J.; Penfold, C.M.; Hoffmann, A.A. Effects of Native Grass Cover Crops on Beneficial and Pest Invertebrates in Australian Vineyards. Environ. Entomol. 2010, 39, 970-978.
64. Muneret, L.; Auriol, A.; Bonnard, O.; Richart-Cervera, S.; Thiéry, D.; Rusch, A. Organic farming expansion drives natural enemy abundance but not diversity in vineyard-dominated landscapes. Ecol. Evol. 2019, 9, 13532-13542.
65. Serra, G.; Lentini, A.; Verdinelli, M.; Delrio, G. Effects of cover crop management on grape pests in a Mediterranean environment. IOBC-WPR Bull. 2006, 29, 209-214.
66. Gonçalves, F.; Zina, V.; Crespo, L.; Oliveira, I.; Torres, L. Ants (Hymenoptera: Formicidae) and Spiders (Araneae) Co-occurring in the Ground of Vineyards from Douro Demarcated Region. Sociobiology 2017, 64, 404-416.
67. Happe, A.K.; Roquer-Beni, L.; Bosch, J.; Alins, G.; Mody, K. Earwigs and woolly apple aphids in integrated and organic apple orchards: Responses of a generalist predator and a pest prey to local and landscape factors. AEE 2018, 268, 44-51.
68. Ješovnik, A.; Blažević, I.; Lemić, D.; Pajač Živković, I. Ant fauna of annual and perennial crops. Appl. Ecol. Environ. Res. 2019, 17, 12709-12722.
69. Schmidt, M.H.; Tscharntke, T. The role of perennial habitats for Central European farmland spiders. AEE 2005, 105, 235-242.
70. Batáry, P.; Báldi, A.; Kleijn, D.; Tscharntke, T. Landscape-moderated biodiversity effects of agri-environmental management: A meta-analysis. Proc. R. Soc. Lond. B Biol. Sci. 2011, 278, 1894-1902.
71. Rusch, A.; Delbac, L.; Thiéry, D. Grape moth density in Bordeaux vineyards depends on local habitat management despite effects of landscape heterogeneity on their biological control. J. Appl. Ecol. 2017, 54, 1794-1803.
72. Frank, S.D.; Wratten, S.D.; Sandhu, H.S.; Shrewsbury, P.M. Video analysis to determine how habitat strata affects predator diversity and predation of Epiphyas postvittana (Lepidoptera: Tortricidae) in a vineyard. Biol. Control. 2007, 41, 230-236.
73. Buchholz, U.; Schruft, G. Räuberische Arthropoden auf Blüten und Früchten der Weinrebe (Vitis vinifera L.) als Antagonisten des Einbindigen Traubenwicklers (Eupoecilia ambiguella Hbn.) (Lep., Cochylidae). J. Appl. Entomol. 1994, 118, 31-37.
74. Huth, C.; Schirra, K.J.; Seitz, A.; Louis, F. A beneficial species becomes a pest-The common earwig Forficula auricularia (Linnaeus 1758). IOBC-WPRS Bull. 2011, 67, 249-256.
75. Kehrli, P.; Karp, J.; Burdet, J.P.; Deneulin, P.; Danthe, E.; Lorenzini, F.; Linder, C. Impact of processed earwigs and their faeces on the aroma and taste of 'Chasselas' and 'Pinot Noir' wines. Vitis 2012, 51, 87-93.
76. Bucher, R.; Hermann, J.D.; Schüepp, C.; Herzog, F.; Entling, M.H. Arthropod Colonisation of Trees in Fragmented Landscapes Depends on Species Traits. Open Ecol. J. 2010, 3, 111-117.
77. Nicholas, A.H.; Spooner-Hart, R.N.; Vickers, R.A. Abundance and natural control of the woolly aphid Eriosoma lanigerum in an Australian apple orchard. BioControl 2005, 50, 271-291.
78. Wilson, H.; Daane, K.M. Review of Ecologically-Based Pest Management in California Vineyards. Insects 2017, 8, 108.
79. Chong, C.S.; D'Alberto, C.F.; Thomson, L.J.; Hoffmann, A.A. Influence of native ants on arthropod communities in a vineyard. Agric. For. Entomol. 2010, 12, 223-232.
80. Grieshop, M.J.; Werling, B.; Buehrer, K.; Perrone, J.; Isaacs, R.; Landis, D. Big Brother is Watching: Studying Insect Predation in the Age of Digital Surveillance. Am. Entomol. 2012, 58, 172-182.
81. Stutz, S.; Entling, M.H. Effects of the landscape context on aphid-ant-predator interactions on cherry trees. Biol. Control. 2011, 57, 37-43.
82. Masoni, A.; Frizzi, F.; Brühl, C.; Zocchi, N.; Palchetti, E.; Chelazzi, G.; Santini, G. Management matters: A comparison of ant assemblages in organic and conventional vineyards. AEE 2017, 246, 175-183.
83. Thomson, L.J.; Sharley, D.J.; Hofmann, A.A. Beneficial organisms as bioindicators for environmental sustainability in the grape industry in Australia. Aust. J. Exp. Agric. 2007, 47, 404-411.
84. Varela, L.G.; Elkins, R.B.; Van Steenwyk, R.A. Evolution of Secondary Pests in California Pear Orchards under Mating Disruption for Codling Moth Control. 11th Int. Pear Symp. Acta Hort. 2011, 909, 531-542.
85. Weinberg, J.L.; Bunin, L.J.; Das, R. Application of the Industrial Hygiene Hierarchy of Controls to Prioritize and Promote Safer Methods of Pest Control: A Case Study. Public Health Rep. 2009, 124, 53-62.
86. Maas, S.; Detzel, P.; Staudt, A. Gefährdungsanalyse der Heuschrecken Deutschlands. In Verbreitungsatlas, Gefährdungseinstufung und Schutzkonzepte; Bundesamt für Naturschutz: Bonn, Germany, 2002; 401p.
87. Grabenweger, G.; Kehrli, P.; Schlick-Steiner, B.; Steiner, F.; Stolz, M.; Bacher, S. Predator complex of the horse chestnut leafminer Cameraria ohridella: Identification and impact assessment. J. Appl. Entomol. 2005, 129, 353-362.
88. Toepfer, S.; Kuhlmann, U. Survey for natural enemies of the invasive alien chrysomelid, Diabrotica virgifera virgifera, in Central Europe. BioControl 2004, 49, 385-395.
89. Vidano, C.; Arzone, A.; Anò, C. Researches on natural enemies of viticolous Auchenorrhyncha. In Meeting on Integrated Pest Control in Viticulture; A. A. Balkema: Rotterdam, The Netherlands, 1987; pp. 97-101.
Jo Marie Reiff
1,2,*,
Sebastian Kolb
1,2,
Martin H. Entling
1,
Thomas Herndl
3,
Stefan Möth
3,
Andreas Walzer
3,
Matthias Kropf
4,
Christoph Hoffmann
2 and
Silvia Winter
3
1Institute for Environmental Sciences, University of Koblenz-Landau, iES Landau, Fortstraße 7, D-76829 Landau in der Pfalz, Germany
2Julius Kühn Institute, Federal Research Institute for Cultivated Plants, Institute for Plant Protection in Fruit Crops and Viticulture, Geilweilerhof, D-76833 Siebeldingen, Germany
3Institute of Plant Protection, University of Natural Resources and Life Sciences, Gregor-Mendel-Str. 33, A-1180 Vienna, Austria
4Institute for Integrative Nature Conservation Research, University of Natural Resources and Life Sciences, Gregor-Mendel-Str. 33, A-1180 Vienna, Austria
*Author to whom correspondence should be addressed.
© 2021. This work is licensed under http://creativecommons.org/licenses/by/3.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.