The role of ecological infrastructure on beneficial arthropods in vineyards

Weeds and non-cultivated plants have a great impact on abundance and diversity of beneficial arthropods in agriculture. The main aim of this work was to study the influence of the ecological infrastructure (meadows and weedy margins) on the arthropod composition in vineyard surrounding landscape. Research was carried out from May to October during three years. Sampling took place in the ecological infrastructure of three differently managed vineyards (organic, integrated and extensive). Three zones were chosen in each vineyard (3 m, 10 m, and 30 m from the edge of the vineyard). Samples were taken using a standardised sweep net method. In total, we captured 6032 spiders and 1309 insects belonging to 4 orders and 10 families. Arthropod fauna was numerically dominated by Aranea (82.1%); among insects, Coleoptera was the most abundant taxonomic group (10.6%); Neuroptera showed the lowest value (0.88%). Significant differences were found between sites and zones. Organic vineyard showed the highest abundance of arthropods (92.41% were spiders) and in the integrated vineyard there was a 23% of insects. Both the highest abundance of arthropods and the highest Shannon Index value (2.46) was found 3 m away from the edge of the vineyard. Results showed that spiders were the dominant arthropods and ladybugs the dominant insects. Weedy strips near the edge of the vineyard contained a high number of insects and spiders. Our results support the importance of weedy margins in enhancing the population of arthropods as well as in biodiversity promotion. Well-managed field margins could play important role in biological control of vineyard pests. Additional key words: spiders; beneficial insects; diversity; weeds Abbreviations used: ED (extensive vineyard); H’ (Shannon Diversity Index); IB (integrated vineyard); OP (organic vineyard) Citation: Franin, K.; Barić, B.; Kuštera, G. (2016). The role of ecological infrastructure on beneficial arthropods in vineyards. Spanish Journal of Agricultural Research, Volume 14, Issue 1, e0303. http://dx.doi.org/10.5424/sjar/2016141-7371. Received: 13 Jan 2015. Accepted: 11 Feb 2016. Copyright © 2016 INIA. This is an open access article distributed under the terms of the Creative Commons Attribution-Non Commercial (by-nc) Spain 3.0 Licence, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Funding: The authors received no specific funding for this work Competing interests: The authors have declared that no competing interests exist. Correspondence should be addressed to Kristijan Franin: kfranin@unizd.hr


Introduction
Intensification of agriculture results in habitat destruction and has a negative effect on biodiversity.According to Pérez-Bote & Romero (2012), biodiversity in agricultural habitats is influenced by the surrounding landscape.A diverse plant community can influence beneficial arthropod populations by providing food or habitat resources that might not be found in a simple plant comunity (Costello & Daane, 1998).Clough et al. (2007) found that in arable land, biodiversity depends on recolonization from surrounding perennial habitats, which serve as overwintering habitats and contain alternative resources for arthropods.Beneficial organisms that are not resident in vineyards all year round must recolonize on a seasonal basis, most 2 The first site, Posedarje OP (44.2032 °N, 15.4319 °E) was an organic vineyard (0.5 ha) surrounded with meadows and low intensity grasslands.In this vineyard the soil was tilled and was managed without pesticides or syntetic fertilizers.The second vineyard (5 ha), Bastica IB (44.1582 °N, 15.4362 °E) had the soil surface covered mainly with weed plants, was not tilled, and was mowed several times during the growing season.This site was situated in a large agricultural area, and was mostly surrounded with vineyards, orchards and arable land under vegetable production.Organic fertilizers were used every three years, whereas syntetic fertilizers were used each year.Copper and sulphur as well as some pesticides (folpet, dimetomorph, probineb and tiamethoxam) were applied against major grape pests.The third site, Dolac ED (44.1343 °N, 15.2528 °E) had 0.2 ha, and represented an extensive system of grape production.The soil was tilled once during vegetational season.Fertilizers and pesticides were used.The vineyard was part of a landscape consisting of small vineyards, olive orchards and vegetable gardens (mosaic of small fields).
In each site, plant and arthropod communities were analyzed at 3 m (zone A), 10 m (zone B) and 30 m (zone C) from the edge of the vineyard (Fig. 1).Zone A, the vineyard edge, consisted mostly of weeds.Zones B and C consisted of meadows and field paths.Field margins and meadows were mowed twice during vegetational season (May and July).In order to maintain the ecological infrastructure fertilizers or pesticides were not used.

Plant comunities
Plant comunities were estimated using the phytosociological method of Braun-Blanquet (1965).Samples as plants that reduce yields by competing with crops or by harbouring pests and plant pathogens (Penagos et al., 2003).Increased diversity has been the rationale for enhancing biological control of arthropod pests through habitat management (Norris & Kogan, 2005).The same authors (Norris & Kogan, 2000) indicated that weed cover enhances the number and activity of spiders and ground beetles.In their research on dicotyledonous weeds, Wilson & Aebisher (1995) reported that the density of most arthropod species decreased significantly as distance from crop edge increased from 0 to 128 m.Some authors (Winkler, 2005;Bàrberi et al., 2010) have reviewed the importance of vegetation diversity for enhancing populations of beneficial arthropods in cropland.Wyss (1996), Simon et al. (2010) and Song et al. (2010) reported a positive effect of plant comunity diversification on beneficial arthropods in orchards.Non-crop habitats bordering agricultural fields in Europe have been found to have a favourable effect on a number of beneficials as spiders, ladybugs, and syrphids (Hillocks, 1998;Ernoult et al., 2013).Woodcock et al. (2008) showed the positive effects of composition and diversity of plants around the field margins on ground beetle diversity.Fields with a dense weed cover and high diversity usually have more predaceous and parasitic arthropods than weed-free fields (Speight & Lawton, 1976).Even now a lot of grape producers destroy weeds not only in fields but also in the surrounding landscape, such as field margins, field patches and non-cultivated areas.In the Zadar County (Croatia) vineyards, typical grape production is organized in monoculture, what leads to landscape simplification and decrease of predatory arthropod population.Vegetation surrounding the fields has a great impact on predator abundance in the vineyards.The main goal of this paper was to examine the influence of vegetation (weed) structure on predatory insects and spiders of three vineyards.

Study area
Field work was carried out in the Ravni Kotari area, near Zadar (Croatia, Northern Dalmatia).Climate is Mediterranean (Csa type) with temperate and wet winters and dry and hot summers (Bolle, 2003).Three different sites (organic vineyard, vineyard in extensive management, and vineyard in integrated management) were researched between 2010 and 2012.Mean temperatures and rainfall during the years of research were, respectively, 14.07°C, 1130.9 mm/yr (2010), 15.02°C, 420.7 mm/yr (2011) and 14. 96°C, 798.8 mm/yr (2012).The role of ecological infrastructure on beneficial arthropods in vineyards were collected in June and September.In each zone, three plots of 1 m 2 were chosen randomly, avoiding the edges and their proximities.Plant species were identified using the Croatian Flora (Rogosic, 2011).The abundance of weeds in the sample plot was recorded.
All the records were tabulated for each site for further analysis of data and to discover relationships between insects and the vegetational structure of ecological compensation areas.

Sampling methods and arthropod identification
Arthropod samples were collected every two weeks between the beginning of the May and the beginning of October.All samples from areas surrounding the vineyards (ecological infrastructure) were taken when weather conditions were appropriate (sunny weather, dry vegetation, day period between 9.30 am and 12.00 pm) using a standardised sweep net method.The sweep net was applied in a standard way, taking 50 sweeps at each weed transect.The sweep net had a diameter of 40 cm, fitted with a heavy cloth suitable for use in dense vegetation (Zurbrügg & Frank, 2006).Samples were collected and examined in the laboratory.Arthropods were stored in 70% ethanol until identification.Adult insects were identificated with help of entomological handbooks and publications.Larva were counted and determined to family lavel.Spiders were only counted.

Data analyses
Nonparametric (Kruskal-Wallis ANOVA, Spearman Rank Correlation), one-way ANOVA method was used to compare number and composition of arthropods between localities and years of research (Statistica 6.1, StatSoft Inc., 2003).Biodiversity among sites and zones was compared using Shannon diversity index (H'), which is based on the number of individuals at the family level (Magurran, 1988).

Arthropod composition and abundance
Altogether 7341 arthropods were collected and classified into Arachnida (Aranea) and Insecta during the three years of research.The number of arthropods across the years of the study was significantly different (Kruskal-Wallis test, H=18.97, df=2, p<0.001).The highest number was recorded in 2011 and the lowest in 2012 (Table 1).The lowest number of arthropods in 2012 probably was because of dryness and reduced vegetation cover (36.19 mm of rainfall between 6 July and12 September).We also found significant differences in arthropod abundance among sites (Kruskal-Wallis test, H=27.01, df=2, p<0.001).Arthropods were more abundant in the ecological infrastructure of the integrated and extensive vineyards than in the organic vineyard.Site IB showed the greatest number of individuals in comparison with other sites (Table 2).Arthropod abundance also varied (Kruskal-Wallis test, H=47.39,df=8, p<0.001) among zones.The highest abundance was recorded in zone A of all localities (Table 3).Arthropod fauna was dominated by spiders (82.10%).The highest number of spiders were found in OP followed by ED and IB (Table 4).A total of 1309 insects representing four orders (Coleoptera, Diptera, Heteroptera and Neuroptera) and 10 families were collected (Table 4).Insect composition was dominated by Coccinellidae (9.13%) whereas Reduviidae were rare, representing 0.13% of the total of arthropods.Comparisons of abundances showed differences among arthropods (Kruskal-Wallis test, H=1710.20,df=10, p<0.001) for Aranea, Coccinellidae, Syrphidae and Reduviidae, whereas for Anthocoridae, Chrysopidae, Cantharidae, Carabidae, Geocoridae, Miridae and Nabidae significant differences were not found (Table 5).In Heteroptera composition Miridae dominated (2.31%), followed by Anthocoridae (1.39%).Geo-  2).The H' varied among sites and zones (Fig. 3b).The higher arthropod abundance was associated with greater compositional and structural diversity of veg-  5 The role of ecological infrastructure on beneficial arthropods in vineyards etation, which was particularly linked with weeds.The highest diversity was noticed in zone A of all sites (Fig. 3a).To compare the number of plant species and the arthropod abundance Spearman rank order correlation was used.Although there was no statistically significant correlation between the number of plant species and the arthropod abundance, regression analysis showed a positive trend (Fig. 4).

Plant comunities
Altogether, 41 plant species belonging to 13 families (Table 6) were identified.Site ED showed the highest number of species, followed by IB and OP.In IB and ED the highest percentage (39.0%) of plant species was in the zone A (vineyard edge) as opposed in OP, where only eight species (19.5%) were found.These plants mostly belong to the weed flora.Among families Poaceae showed the highest abundance (22.2%), followed by Asteraceae (18.3%),Fabaceae (14.3%),Apiaceae (9.1%) and Cichoriaceae (7.9%).The most abundant plant species among all localities was Avena fatua.The lowest abundance was recorded in OP (zone B) represented by only four species (Briza maxima L., Dorycnium herbaceum Vill, Dittrichia viscosa L. and Aegilops spp.).Our analysis showed that flora in zone A was predominantly composed of dicotyledones (Asteraceae, Fabaceae, Apiaceae).Zones B and C also comprised species from these families except OP (B and C), where Poaceae dominated.

Discussion
This work explored the influence of ecological infrastructure and plant composition on arthropod population and diversity.Arthropod communities clearly differed between sites and were dominated by Aranea.In agricultural landscapes, spiders are generally most diverse in semi-natural habitat (Duelli et al., 1999).In this research, spiders were most abundant at the site OP, especially in zone C (pastures and meadows at wood vicinity) as suggested by Isaia et al. (2006).Bruggisser et al. (2010) reported that spider and plant richness was not higher in organic compared to conventional farming.The main reason for spider dominance is probably their broader diet and their ability to survive a long period without prey (Costello & Daane, 1999).Spiders also may benefit from higher weed populations (especially ED and BI sites), which provide higher structural complexity and potentially increase the availability of herbivore prey (Schmidt et al., 2005;Woodcock et al., 2013).We noticed that dry vegetation also affected to a high number of spiders and predaceous insects.Among Coleoptera the most abundant family was Coccinellidae presented mostly by Hippodamia spp.particularly in zone IB(C), possibly as a result of presence of their prey on plants such as Dau-   cus carota (Burgio et al., 2006).In California vineyards, Daane et al. (2008) also found Hippodamia spp.and Scymnus spp. as important predators of mealbugs.Kopta et al. (2012) reported that plants like Amaranthus retroflexus L., Centaurea cyanus L. Daucus carotta L., and Foeniculum vulgare L. were present in almost all sites where ladybugs were found in high number.These plants provide alternative food sources such as pollen and nectar from extrafloral nectaries.As Raymond et al. (2000), we also found ladybugs (all developmental stages) on Chenopodium spp.Gaigher & Samways (2010) indicated that abundance of carabids was higher in organic than in the integrated vineyard.O' Rourke et al. (2008) and Eyre et al. (2012) reported that crop rotation and diverse crop habitats increased Carabidae activity, density and diversity.Their conclusions correspond with our results.The highest abundance of Carabidae found at site IB may lay in the fact that integrated vineyard was surrounded with arable land producing grains and vegetables with a lot of weed strips.Management of weed strips appears to increase the availability of food for carabids and results in enhanced reproduction (Zangger, 1994;Zangger et al., 1994).The other reason probably lays in the fact that The role of ecological infrastructure on beneficial arthropods in vineyards ground surface of this vineyard (IB) was managed with cover crops and mulched several times during the vegetational period (Thomson & Hoffmann, 2007).As Burgio et al. (2006) reported, sampling by sweep net is able to collect only terrestial Carabidae present in the weed canopy, and not those on the soil.Green lacewing (Chrysopidae) showed preference to weed margins where plants such as Chenopodium album L., Convolvulus arvensis L. and Anthemis arvensis L. are found (Ruby et al., 2011).Beside, as food source, some weeds as Trifolium pratense L., Centaurea cyanus L., Papaver rhoeas L. and Vicia spp.seem suitable for lacewings as oviposition site.Our data agree with those reported by Eichenberger (1991), who also found lacewings on the plants above mentioned.Diptera from family Syrphidae were always more abundant in zone A of all sites where Apiaceae and Asteraceae dominated (Tooker et al., 2006).Syrphidae prefer grassy strips based on total botanical diversity (Speight, 2008).
Plants from these families (Apiaceae and Asteraceae) are known as nectar and pollen producers in great amounts so they play an important role in Syrphidae attraction (Branquart & Hemptinne, 2000;Rebek et al., 2005;Morales & Kohler, 2008;van Rijn & Wäckers, 2010).As expected, the low number of syrphids at OP could be due to the low presence of flowering weeds.
Costello & Daane (1999), Nicholls et al. (2000Nicholls et al. ( , 2008) ) and Altieri et al. (2005) also reported several dominant Heteroptera predators such as Nabis spp., Orius spp.and Geocoris spp. in the ecological infrastructure of vineyards.Insect predators such as Anthocoridae and Geocoridae prefer thrips, aphids, lepidopteran and hemipteran eggs and spider mites.High number of Anthocoridae was found at site IB (A) at the vicinity of apple orchard.One potential explanation is that these predators are strongly associated with aphids, mites and thrips which are always present in apple orchards (Rieux et al., 1999;Burgio at al., 2006;Gadino et al., 2012).Prischmann et al. (2005) found no significant differences in Heteroptera abundance between commercially managed and unmanaged vineyards.Daane et al. (2008) also found these bugs as not commonly present in large numbers in vineyards.Miridae were represented by Macrolophus spp.and Dicyphus spp.We noticed a relationship between Macrolophus spp.and the plant Ditrichia viscosa (L.).Greuter (Asteracea) as has also been documented in Greece (Perdikis et al., 2007).That can explain a higher number of these bugs in DE and OP, while in site IB D. viscosa was not present.
This study shows that 'plant rich' weedy margins (zone A) can enhance the abundance of some predators.Our results agree with some other studies showing that the introduction of flowering plants into agricultural settings leads to increased arthropod abundance (Rebek et al., 2005;Walton & Isaacs, 2011).Higher arthropod diversity was associated with greater compositional diversity of weed cover (Benton et al., 2003;Gaigher & Samways, 2010).Our results showed that the number of total insects was lower in meadows and pastures than in wildflower strips of field paths and weedy areas, what is similar to the results of Zurbrügg & Frank (2006).In almost all localities, vegetation structure was the best explanatory factor for insect distribution, abundance, and species richness.Our results are similar to the results reported in other studies of arthropods in organic and intergrated vineyards (Gaigher & Samways, 2010).The best plant families for preserving predators (Coccinellidae, Syrphidae and Chrysopidae) are Apiaceae, Asteraceae and Chenopodiaceae (Fiedler et al., 2008;Bertolaccini et al., 2011).Some studies also showed that organic management systems increased the arthropod abundance and richness but not the diversity (Clark, 1999).Overall, these results suggest that despite the assertion that organic fields contribute to increase biodiversity, arthropod abundance and diversity also depend on plant composition.Sites and zones with higher number of weed plants species especially those with attractive flowers obviously provide favourable conditions for natural enemies.Conservation and attendance of ecological infrastructure such as weedy margin can serve as habitat for beneficial fauna.Therefore it can play an important role in increasing the vineyard production quality.
In summary, this study shows the importance of noncultivated areas on the abundance of predatory arthropods.Ecological infrastructure, especially weed margins, field paths and sorrounding wildflower areas, are important components of the vineyard sistem as they enhance the plant abundance and diversity.Despite the vineyard management, our conclusion is that plant

Figure 1 .
Figure 1.Map of the study site with zones A, B and C.

Figure 3 .
Figure 3. Shannon diversity index (H') in the sites and zones of research.

Figure 4 .
Figure 4. Relationship between the number of plant species and the number of arthropods.

Table 1 .
Comparison of captures within years of research.

Table 2 .
Arthropod abundance within sites of research.

Table 3 .
Comparison of captures within sites and zones.

Table 4 .
Arthropod abundance in ecological infrastructure of vineyard.

Table 5 .
Comparison among arthropod orders and insect families.

Table 6 .
Plant communities in zones (percentage of species).