View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by Biblioteca Digital do IPB Agricultural and Forest Entomology (2019), DOI: 10.1111/afe.12352 Distribution of the spider community in the olive grove agroecosystem (Portugal): potential bioindicators ∗† ∗ † ‡ Jacinto Benhadi-Marín ,JoséA.Pereira , José P. Sousa and Sónia A.P. Santos § ∗Centro de Investigação de Montanha (CIMO), Escola Superior Agrária, Instituto Politécnico de Bragança, Campus de Santa Apolónia, 5300-253, Bragança, Portugal, †Centre for Functional Ecology, Department of Life Sciences, University of Coimbra, Calçada Martim de Freitas, 3000-456, Coimbra, Portugal, ‡CIQuiBio, Barreiro School of Technology, Polytechnic Institute of Setúbal, Rua Américo da Silva Marinho, 2839-001, Lavradio, Portugal and §LEAF, Instituto Superior de Agronomia, Tapada da Ajuda, 1349-017, Lisbon, Portugal Abstract 1 Spiders are successful natural enemies in different crops. Research on the role of spiders as natural enemies within agroecosystems needs to address the distribution of their communities across different spatial scales, as well as the dominant species. 2 We studied the spatial distribution of the community of spiders of the olive agroecosys- tem in Northeastern Portugal and investigated potential species that could be used as bioindicators of agricultural management in the olive grove. 3 We found nine functional groups (ambushers, foliage runner hunters, ground hunters, orb-web builders, sheet web builders, sensing web-builders, space web builders, stalk- ers and wandering sheet/tangle weavers) encompassing a community that changed significantly across the horizontal and vertical gradient. 4 We propose Thanatus vulgaris Simon, 1870 as potential bioindicator for the ground of the olive grove central area and Ozyptila pauxilla (Simon, 1870) for the ground of the olive grove peripheral area. 5 Adjacent shrubland areas could play an important role in biological control of pests, allowing the exchange of species and individuals with the olive crop. The role of agro- biont species as indicators of agricultural managements deserves further investigation towards the enhancement of the effectiveness of spiders within low-impact crop man- agement in arable landscapes. Keywords Guilds, indicators, margin, predators, shrubland. Introduction Furthermore, the pest suppression exerted by natural enemies can be maximized by the existence of overlapping habitat niches The suppression of pests by their natural enemies is a subject (e.g. different vertical layers such as soil, trunk and canopy) of interest for agricultural managers within sustainable farming that may allow their coexistence by reducing the intraguild practices. Agricultural landscapes are usually unstable environ- competition (Dainese et al., 2017). Hence, crop management ments for natural enemies as a result of moderate to high levels towards maintaining and promoting supplemental resources of disturbance caused by the application of cyclic and frequent can improve the effectiveness of natural enemies against pests agricultural practices (Landis et al., 2000). However, several fac- tors can drive the spatial distribution of natural enemies enhanc- (Landis et al., 2000). ing their presence within crops. For example, the occurrence Spiders encompass a group of generalist predators that feed of ecological corridors between crops, the presence of differ- mostly on insects, they are well represented within the agroe- ent patches in the surroundings of the crop, and the availabil- cosystems (Marc et al., 1999), and they have been reported as ity of within-crop microhabitats can promote the abundance and successful natural enemies in different crops such as apple (Wyss action of natural enemies in the crop as a result of spillover (i.e. et al., 1995; Isaia et al., 2008), pear (Pekár et al., 2015), cotton movement between crop and noncrop patches), the existence of (Ghavami, 2008), wheat (Oelbermann & Scheu, 2009) and Bras- shelter and supplementary food (Nicholls et al., 2001; Blitzer sica L., 1753 (e.g. broccoli and cauliflower) (Hooks et al., 2003). et al., 2012; Benhadi-Marín et al., 2018; Michalko et al., 2019). Research on the role of spiders as natural enemies within agroecosystems needs to address not only the distribution of Correspondence: Jacinto Benhadi-Marín. Tel.: 00351915720198; their communities across different spatial scales (e.g. vertical e-mail: [email protected] and horizontal patterns), but also the structure of the community © 2019 The Royal Entomological Society 2 J. Benhadi-Marín et al. by knowing which species are dominant within the agricultural type in the study region and corresponds to a typical Mediter- landscape. Samu and Szinetár (2002) defined agrobionts as those ranean habitat named ‘matos’ (shrublands) characterized by the species that reach high dominance in crops. These species can herbaceous stratum dominated by plants belonging to Asterceae, be indicators of arable habitats and could be used to monitor the Poaceae and Fabaceae families; the shrub stratum dominated by quality and sustainability of the agroecosystem. plant species such as Cistus ladanifer L., Cytisus sp., Lavan- The olive tree cultivation (Olea europaea L. 1753) is an dula sp., Rosmarinus officinalis L., Rubus ulmifolius Schott and agricultural activity with high economic, social and cultural Crataegus monogyna Jacq; and the tree stratum dominated by importance along the Mediterranean Basin where 95% of the Quercus rotundifolia Lam., Quercus pyrenaica Willd. and Arbu- global production of olive oil is located (FAOSTAT, 2018). The tus unedo L. The study sites are located in the Mediterranean olive fruit fly Bactrocera oleae (Rossi, 1790) (Diptera: climatic zone, Csa-type according to the Köppen–Geiger clas- Tephritidae) is the key pest of the tree and their larvae develop in sification (Peel et al., 2007), which is characterized by hot and the fruits, whereas pupae overwinter in the soil and adult flies are dry summers and mild and moist winters. The sampling area is long-living and mobile (Civantos, 1999). Prays oleae (Bernard, located within a region with a mean annual rainfall of 776 mm 1788) (Lepidoptera: Praydidae) is another olive tree pest that and a mean annual temperature of 13.8 ∘C (Fick & Hijmans, completes its life cycle in the canopy (Civantos, 1999). Both of 2017). these species can be consumed by spiders both in the canopy as The five study sites form a polygon of30km2 with a max- well as at the ground level (Morris et al., 1999). imum and minimum separation between groves of 9.71 km Within the olive grove agroecosystem, several studies have and 0.39 km, respectively. The olive groves were rain fed: two been carried out encompassing different aspects of the biology, of them were conducted under the Integrated Production sys- diversity and taxonomy of spiders, as well as an investigation of tem (Cedães 1 and Cedães 2) and three of them were con- the influence of agricultural management and landscape on the ducted under the organic farming system (Guribanes, Romeu, community of spiders. In this context, Cárdenas and Barrientos and Valbom-dos-Figos). More details regarding the study sites (2011) provided a list of 142 spider species within the olive grove are provided in the Supporting information (Table S1). in Andalusian (southern Spain) groves; Cárdenas et al. (2015) found that organic farming favoured the abundance and diversity of canopy spiders compared with the integrated pest management Sampling of Araneae and conventional systems. Picchi et al. (2016) found a negative correlation between the abundance of the olive fruit fly and The horizontal distribution of the community of ground spiders cursorial and sheet web spiders, as well as a significant effect of was studied by sampling three areas: two areas were located in the adjacent semi-natural habitat type on the spider family com- the olive groves (a central area and a peripheral area close to the position in Italy. Also, Cárdenas (2008) developed preliminary hedgerow with the shrubland area) and a third area was located studies concerning the use of spiders as potential bioindicators in the shrubland. The central and peripheral areas within the of agricultural management in the olive grove agroecosystem. grove were located 150 m apart, whereas the peripheral and the Thus, there is an increasing interest on the role of spiders as shrubland areas were spaced 100 m apart. The ground spiders natural enemies of olive pests; however, studies regarding the were sampled using four pitfall traps placed in each sampling composition of the community of spiders within the olive grove area. Each trap consisted of a plastic cup (top diameter 115 mm, and its surrounding landscape and their potential as bioindicators height 130 mm) dug into the ground and filled with 250 mL of agricultural practices are still scarce. The present study aimed of ethylene glycol (anti-freeze liquid) as a preservative. A lid to (i) characterize the spatial distribution of the community of supported by iron wires was placed over each trap to exclude spiders and (ii) identify agrobiont species that can be further used rain, debris and small vertebrates. Pitfall traps were placed in as bioindicators of agricultural management in the olive grove. the south side of the canopy at 50 cm from the trunk (olive Our working hypothesis was that the community of spiders tree in the grove or shrub or tree in the shrubland) and were is unequally distributed across