True Bugs (Heteroptera) Assemblage and Diversity in the Ecological Infrastructures Around the Mediterranean Vineyards
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Bulletin of Insectology 74 (1): 65-78, 2021 ISSN 1721-8861 eISSN 2283-0332 True bugs (Heteroptera) assemblage and diversity in the ecological infrastructures around the Mediterranean vineyards Kristijan FRANIN1, Gabrijela KUŠTERA FRANIN2, Branka MARIČIĆ1, Šime MARCELIĆ1, Marina PAVLOVIĆ1, Tomislav KOS1, Božena BARIĆ3, Žiga LAZNIK4 1Department of Ecology, Agronomy and Aquaculture, University of Zadar, Croatia 2Local action group LAURA, Biograd na Moru, Croatia 3Department of agricultural zoology, Faculty of Agriculture, University of Zagreb, Croatia 4Biotechnical Faculty, Department of Agronomy, University of Ljubljana, Slovenia Abstract One of the main tools in Integrated Pest Management (IPM) is habitat management known as ecological infrastructure. Ecological infrastructures play an important role in enhancing biodiversity in perennial plantations such as vineyards. Moreover, elements of ecological infrastructure such as weeds and flowering plants enhance the population of beneficial insects, in particular, natural enemies of vineyard pests. The study was carried out during three consecutive years in three different models (extensive, integrated and organic) in Zadar county (Croatia). The main objective of this research was to assess the effects of three types of ecological infrastructures (weed margins, wildflower strips, and Mediterranean dry pastures) on true bugs (Heteroptera) composition and di- versity. During the study period from May to October for three consecutive years (2010-2012), 4158 individuals belonging to 14 families, 30 genera and 58 species were recorded. Species richness and abundance were higher in both weedy margins and wild- flower strips. The highest number of species was found in ecological infrastructures associated with integrated vineyard. Nysius graminicola graminicola (Kolenati) was considered as the dominant species within the whole study. The most abundant predators were Macrolophus melanotoma (Costa) and Orius niger (Wolff). Unlike Mediterranean dry pastures, the population of beneficial species was also more abundant and diverse in weedy margins and wildflower strips. Our results emphasize the need for maintaining ecological infrastructures in order to enhance the biodiversity of true bugs and overall arthropod biodiversity in vineyard landscapes. Moreover, weed margins and wildflower strips seem to have an influence on attracting and conserving the beneficial Heteroptera in agroecosystems. This results could help to improve conservative biological control as a part of IPM in vineyards. Key words: biodiversity, ecological infrastructure, true bugs, vineyards, weeds. Introduction Insectary plants also known as flowering plants within and around vineyards enhance the activity and density of Integrated Pest Management (IPM) practices refer to eco- natural enemies (Landis et al., 2005; Wong and Frank, logically-based pest control (Wilson and Daane, 2017). 2013; Lu et al., 2014). Weeds can also serve as a habitat According to Naranjo et al. (2014), biological control is for insect pests, thus their presence may suppress pest a key ecosystem service of IPM. Moreover, conservation transition into the vineyard. Ecological infrastructures do biological control as a part of IPM strategy is a sustaina- not only serve as a source of natural enemies, but it can ble approach to pest management, which can contribute also reduce soil erosion and conserve water in the soil. to reduction in pesticide use (Altieri 1999; Begg et al., True bugs are an ecologically very diverse group of in- 2017). Snyder (2019) showed that conservation biologi- sects (Lundgren, 2011). Their sensitivity to ecological cal control techniques may support natural enemy biodi- factors and side effects of pesticide treatments make them versity. Furthermore, IPM promotes and preserves biodi- good indicators of ecological change (Fauvel, 1999). versity and establishes a more sustainable agroecosys- Orabi et al. (2010) in their study confirmed Heteroptera tem. One of the main problems related to vineyard pests as bioindicators of environmental conditions and change. seems to be monoculture production. Moreover, intensi- All developmental stages of these insects live in the same fied farming practices lead to a loss of species biodiver- environment (Fauvel, 1999). According to Gilbert et al. sity (Attwood et al., 2008). Among different manage- (2015), some Heteroptera are sensitive to habitat changes ment regimes, organic vineyards favour a range of taxa which makes them good indicators of habitat quality. (Hole et al., 2005). For instance, Froidevaux et al. (2017) True bugs are an important group of insects in vineyard found that abundance of arachnids in Mediterranean production, such as phytophagous insects but in particu- vineyards was positively associated with vegetation lar as natural enemies. Some authors agree that some- cover. According to Wilson and Daane (2017), non-crop times certain species of these insects can cause damage species can attract and maintain beneficial insects in ag- to grapes (Arzone et al., 1990; Paoletti, 1999; Schaefer ricultural settings and increase agrobiodiversity. Loso- and Panizzi, 2000; Leskey et al., 2012). For instance, spe- sová et al. (2003) noticed that European vineyards offer cies belonging to the genus Lygus (Miridae), Piesma a high range of plants, especially weeds around and be- (Piesmatidae) and Nysius (Lygaeidae) were found as vec- tween rows. Surrounding vegetation, meadows, weeds, tors of some important pathogens (Mitchell, 2004). and wildflower strips are components of ecological infra- Orságova et al. (2011) reported that Lygus rugulipennis structure which provide shelter to beneficial arthropods. Poppius act as a vector of some grape viruses. Except from true bug phytophagous species in vineyards, some or sites dominated by several species with high occur- authors mentioned beneficial Heteroptera species as well rence) will be less attractive to Heteroptera, particularly (Lozzia et al., 2000; Rogé et al., 2009). For instance, beneficial species. The ecological infrastructure types predatory species from the genus Orius (Anthocoridae), were: (1) weedy margins (WM) within the vineyards as a Nabis (Nabidae) and Geocoris (Lygaeidae) are important board margin situated along the vineyard rows, charac- predators of leafhoppers, spider mites, including lepidop- terized by typical weed plants, dominated mostly by an- teran and hemipteran eggs (Costello and Daane, 1999). nual and biennial dicotyledonous species and about 2 m Some Heteroptera (Anthocoridae, Miridae, Nabidae and width. The ground vegetation was mowed once in April, Reduviidae) are involved in biological control of grape (2) wildflower strips (WFS) associated with a board veg- moths (Thiéry et al., 2018). Malacocoris chlorizans etation of field paths with a distance of at least 10 to (Panzer) is known as a predator of red mites (Chuche and 20 m from the edge of the vineyard, and (3) Mediterra- Thiéry, 2014). The predatory species Nabis americoferus nean dry pastures (MDP) used for extensive livestock Carayon and Zelus renardii Kolenati also inhabit vine- (sheep and goats) grazing and dominated mostly by Po- yards (Costello and Daane, 1999). According to the data aceae. MDP were about 30 to 50 m away from the vine- of Schuman et al. (2013), some Geocoris species feed on yards. Empoasca spp. Besides this, true bugs serve as an im- portant food source for many insectivorous animals and Insect sampling and determination therefore contribute to greater agrobiodiversity (Gilbert Sampling took place from the beginning of May to the et al., 2015). Zurbrüg and Frank (2006) noticed that veg- beginning of October during three consecutive years etational structure and flower abundance are key factors (2010-2012). Samples were taken every fifteen days us- in Heteroptera richness and community structure. ing a sweep net during sunny and calm weather, between The first objective of this research was to address what 10:00 a.m. and 4:00 p.m. A sweep sample consisted of 50 type of ecological infrastructure provides the best condi- sweeps with a 40 cm diameter entomological net. Sam- tions for Heteroptera biodiversity, in particular, predatory pled bugs were stored in ethanol (70%) until the determi- species. Moreover, we wanted to select plants (habitat) nation. Identification was done using entomological pub- which could encourage beneficial organisms to provide lications (Stichel, 1955; Wagner and Weber, 1964; Wag- natural control of vineyard pests. ner, 1971; Péricart, 1987; 1998; Derjanschi and Péricart, 2006). All collected Heteroptera adults were sorted ac- cording to species level while nymphs were identified at Materials and methods a family level. Study sites Vegetation sampling The experiment was conducted in Zadar county (Croa- All vascular plant species were recorded once per site tia). According to the Köppen climate classification, the during each growing season. Plant identification was car- study sites belonged to the Mediterranean climate types ried out using the Croatian Flora (Rogošić, 2011). In or- (Csa) characterized by wet and mild winters and hot, dry der to determine the relative species abundance and plant summers (Bolle, 2003). Mean annual temperature was richness, the phytosociological Braun-Blanquet method 25 °C and precipitation was 85.3 mm. Ecological infra- was used (Poore, 1995). The standard plot size for sam- structures around three vineyards (each with a different pling that was used was approximately 30-50