The key role of inter-row vegetation and ants on predation in Mediterranean organic vineyards

https://doi.org/10.1016/j.agee.2021.107327Get rights and content

Highlights

  • Vegetation cover is a biodiversity friendly practices that can provide ecosystem services in agrosystems.

  • We evaluated its influence on sentinel prey predation in Mediterranean vineyards.

  • We found an overall 29 % increase in predation events in vegetated vineyards, both on the ground and on the vine trunk.

  • 96 % of the 80 % observed predation events involved Mediterranean ant species.

Abstract

Biodiversity-friendly farming practices are taking centre stage, with herbicide use sparking major public debate on human health. Vegetation cover is increasingly used to enhance agroecosystem biodiversity and functions, providing important ecosystem services like biological pest control. However, further information is required on the relationship between vegetation cover, natural enemies, and pest predation. Using a sentinel prey experiment set up in 26 Mediterranean organic vineyards, we analysed the response of generalist predators, and the associated final predation and dynamics under three inter-row management types: bare soil, one out of two inter-rows vegetated and all inter-rows vegetated. Predation on sentinel prey was monitored on the ground and on the vine trunk throughout the daytime and after a night of exposure. Generalist predator abundance was quantified using pitfall traps. Final sentinel prey predation both on vine trunks and on the ground were significantly higher in fully vegetated vineyards, with a shorter prey survival time than in tilled vineyards. Both diurnal and nocturnal predation were significantly related to increased vegetation cover and richness. Moreover, 96 % of the identified predation events involved ants. We demonstrated the key role of vegetation cover in improving the predation function through a spill-over from the inter-row to the grapevine. Contrary to what is commonly observed in agrosystems, we clearly identified ants as the predominant predator both on the ground and on the vine trunk. Our study has important implications for Mediterranean vineyard management, promoting vegetation as a nature-based solution. Sustainable management of vineyard vegetation favouring the natural predator community may contribute to a reduction in pesticide use and fossil fuel consumption.

Introduction

A standard practice in conventional viticulture is the removal of inter-row vegetation using herbicides to reduce weed competition (Winter et al., 2018). However, both farmers and society at large are increasingly aware of the need to move from high-input agriculture towards more environmentally sound and sustainable farming practices. Glyphosate, the most widely used herbicide in agriculture (Benbrook, 2016), represents an emblematic example of the need to change a chemistry-based agricultural paradigm dominant since the 1950s (Pimentel, 1996). In 2017, over 1.3 million Europeans signed a petition calling for a ban on this herbicide. Concern over human and environmental exposure to pesticides has led several European countries such as Germany, France, Italy, Austria and Greece to plan a complete ban on Glyphosate in the coming years. This growing awareness of the need for successful ecological change in agriculture offers an opportunity to rethink vegetation management and to move towards more sustainable and biodiversity-friendly farming practices. This is particularly relevant in vineyards, a perennial crop system with a high pesticide consumption (Butault et al., 2011).

More sustainable vineyard practices like wider use of vegetated inter-rows remain limited by various constraints, such as potential competition for water, particularly in water-limited regions of the Mediterranean (Celette et al., 2009; Ruiz-Colmenero et al., 2011). However, vegetation cover can directly and indirectly provide several ecosystem services to wine and grape production when managed appropriately (Garcia et al., 2018; Winter et al., 2018). Vegetation cover in vineyards can enhance biological activity (Quecedo et al., 2012; Buchholz et al., 2017), water infiltration (García-Díaz et al., 2017) and organic matter availability (Ruiz-Colmenero et al., 2011). Maintaining vegetation cover improves soil stabilisation because organic matter stabilises aggregates, and root systems protect the soil (Ruiz-Colmenero et al., 2011). Vegetation cover can also favour beneficial organisms associated with grapevines (Altieri and Letourneau, 1982; Sáenz-Romo et al., 2019b) and supports higher levels of biodiversity (Altieri et al., 2005; Wilson et al., 2017b).

Pest regulation has been identified as another important ecosystem service enhanced by the presence of inter-row vegetation. The pest regulation service has commonly been linked to the abundance of natural enemies, such as generalist predators and parasitoids (Costello and Daane, 1999; Sharley et al., 2008; Hoffmann et al., 2017; Sáenz-Romo et al., 2019b). Predators are typically larger than their prey and, unlike parasitoids, they require more than one prey individual during their development. Generalist predators that feed on a variety of prey, such as leafhoppers, flies and caterpillars, are commonly considered to be poorly effective in pest regulation because their numbers are not sufficient to deal with pest population dynamics (Miñarro et al., 2005). However, generalist predator efficiency may be higher if their abundances are high before the pest invades (Symondson et al., 2002). In the case of such early arrival, they may hamper or even prevent pest invasion.

In vineyards, spiders and predatory beetles, such as Carabidae and Staphylinidae, are among the largest generalist predator groups feeding on pests (Thomson and Hoffmann, 2013; Pfingstmann et al., 2019; Sáenz-Romo et al., 2019b). To a lesser degree, lacewings, hoverflies and thrips have been recorded as vineyard predators (Costello and Daane, 1999; Hoffmann et al., 2017; Loni et al., 2017). Although ants are known to favour aphids and coccids through mutualistic interactions (exchanging honeydew for protection, Mansour et al. (2012); Beltrà et al. (2017)), they may also act as predators of insect pests (Offenberg, 2015). All these taxa play a significant role in crop pest regulation (Symondson et al., 2002) and have been shown to be promoted by vegetation cover in vineyards (Thomson and Hoffmann, 2009; Sáenz-Romo et al., 2019a). Vegetation may also facilitate grapevine access to ground-dwelling predators (Frank et al., 2007; Irvin et al., 2016).

In general, the abundance of natural enemies is higher in more diverse ecosystems because vegetation cover provides both additional habitat and food (Nicholls et al., 2000). However, there have been few attempts to document how vegetation cover enhances predation. The relationship between predation and vegetation cover has been explored in several recent studies, but with contrasting results. While Rusch et al. (2017) did not record any direct influence of local vegetation management on pest predation, both native and introduced vegetation cover were found to increase sentinel egg predation in other studies (Danne et al., 2010; Hoffmann et al., 2017). Further investigations are required to improve our understanding of vegetation management effects on both generalist predator abundance and their predatory activity.

Although vegetation cover may help increase generalist predator abundances, predators must move from the inter-row to the grapevine to affect pest insect control. In the present study, we evaluated the abundance of generalist arthropod predators and the related predation function in Mediterranean organic vineyards under three different inter-row management systems. Our predation survey was performed both throughout the day and at night’s end, to analyse the effects of vegetation cover, plant species richness and diversity on predators and on the attack on sentinel prey. We addressed the following research questions: (1) Do generalist predator abundance and final predation increase with vegetation cover? (2) Do the effects on predator numbers and final predation depend on vegetation characteristics (plant species richness, percentage of vegetation cover and its variance, beta diversity (Bray-Curtis index)? (3) Are these effects limited to predation in the inter-row, or is there a spill-over effect to grapevine plants? (4) What are the major predator groups attacking sentinel prey?

Section snippets

Study sites and design

This study was conducted in south-eastern France, between the southern slopes of the Luberon mountains and the Durance river. The landscape is dominated by medium-sized vineyards (0.7 +/- 0.5 ha) and the degree of urbanisation is low. In this region, winegrowers most often keep bare soil from mid-spring to autumn rains. This is the most widely adopted practice. In permanently vegetated vineyards, the vegetation is mowed or laid down before summer. The southern Luberon area has a Mediterranean

Vegetation cover

We recorded 91 plant species in the 0/2 vineyards, predominantly annuals. Lolium rigidum (annual), Convolvulus arvensis (perennial) and Avena sterilis (annual) were the dominant species in the quadrats, with a mean cover of 5.4 %, 1.8 % and 1.7 %, respectively. In the 1/2 vineyards, 115 plant species were sampled, with the dominant species Lolium rigidum, Bromus hordeaceus and Vicia sativa covering 9.2 %, 3.5 % and 3.3 % of the quadrats, respectively. We identified 114 plant species in the 2/2

Discussion

This study reveals a clear positive effect of inter-row vegetation on the predation dynamics and final predation of sentinel prey. Although this effect was more pronounced on the ground, a spill-over from the vegetated inter-rows to the grapevines was observed. We also demonstrate for the first time in temperate perennial crops the predominant role of ants as potential natural enemies of pest insects. Our findings provide valuable insights into the strong functional role that vegetation plays

Authors contribution

C.B., O.B. and C.M. conceived the ideas and designed the experiment; C.B., O.B. and A.B. collected the data; C.B. O.B. and A.M. analysed the data, C.B. and O.B. led the writing of the manuscript. All authors contributed critically to the drafts and gave final approval for publication.

This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.

Declaration of Competing Interest

The authors report no declarations of interest.

Acknowledgements

We want to express our gratitude to the cooperative of Marennon and all the farmers for authorising us to access to their vineyards and for their interest in the project. Thanks to Daniel Pavon, Emile Melloul, Elza Boniffacy, Pauline Mathieu and Romain Septidi-Lenfant for valuable help during the fieldwork.

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