Conserving Species-Rich Predator Assemblages Strengthens Natural Pest Control in a Climate Warming Context
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Agricultural and Forest Entomology (2016), DOI: 10.1111/afe.12180 Conserving species-rich predator assemblages strengthens natural pest control in a climate warming context ∗†‡ ∗† Robin Drieu and Adrien Rusch ∗INRA, ISVV, UMR 1065 Santé et Agroécologie du Vignoble, F-33883, 71 rue Edouard Bourlaux, Villenave d’Ornon, France, †INRA UMR 1065 Santé et Agroécologie du Vignoble, Bordeaux Sciences Agro, Université de Bordeaux, F-33883, 71 rue Edouard Bourlaux, Villenave d’Ornon, France and ‡Centre International D’études Supérieures en Sciences Agronomiques, Montpellier SupAgro, Place Pierre Viala, 34060, Montpellier, France Abstract 1 Recent evidence has shown that a consideration of multiple drivers is important if we want to understand how ecosystem functioning will respond to global change. 2 In the present study, we used a substitutive approach to examine how two major components of global change, warming and predator diversity, affect the top-down control of two phytophagous insect pests. Predator assemblages were created using a substitutive design to give three single-species treatments (low diversity) and one three-species treatment (high diversity) under two temperature treatments (current seasonal temperature and an increase of +3∘C over current temperatures). 3 The results obtained indicate a shift from substitutive to complementarity effects among predatory species with experimental warming. Experimental warming revealed complementarity between the predatory species in diverse assemblages because higher predation rates on both prey species were found in the high diversity treatment compared with what was expected based on low diversity treatments at the same temperature. 4 Our analyses of prey selectivity provided evidence that resource-niche partitioning is involved in the emergence of functional complementarity under warming. The present study highlights the importance of maintaining diverse predator assemblages if we want to increase natural pest control services in agroecosystems and reduce dependence on agrochemicals in a climate change context. Keywords Agroecosystems, biodiversity, biodiversity-ecosystem functioning, climate change, food web, grapevine, multiple predator, trophic cascade. Introduction Changes in abiotic conditions such as temperature affect the strength of trophic interactions that play critical roles in the func- The effects of global environmental changes are predicted to tioning of terrestrial ecosystems (Schmitz, 2003; Barton et al., become more important in the future, such as increases in tem- 2009; Barton & Ives, 2014). Temperature affects seasonal phe- perature and atmospheric CO , as well as losses of biodiver- 2 nology, metabolic rate or the behaviour of arthropod predators, sity or biological invasions that are triggered and maintained by with potential important consequences related to the top-down human activities (Tylianakis et al., 2008). Several studies have control of herbivores and primary producers (Schmitz & Bar- revealed that global environmental changes can affect the geo- ton, 2014). Moreover, empirical studies have reported that direct graphical distribution and community composition of plant and effects of predators on herbivores may be reduced at elevated animal communities (Tylianakis et al., 2008; Sarmento et al., 2010; Walther, 2010; Harley, 2011). These modifications are pre- temperatures (Barton, 2010; Laws & Joern, 2013) and also dicted to alter direct and indirect interactions among species that cascading effects related to invertebrate predators on plant and therefore ecosystem functioning (Tylianakis et al., 2008). communities can be magnified at elevated temperatures (Bar- However, the empirical evidence related to such effects remains ton & Schmitz, 2009; Barton et al., 2009). Furthermore, labo- limited (Dossena et al., 2012; Barton & Ives, 2014). ratory and modelling studies have found higher feeding rates and short-term per capita interaction strength between predators Correspondence: Adrien Rusch. Tel.: +33 557122643; e-mail: and their prey at higher temperature, suggesting a higher level [email protected] of top-down control at higher temperatures (Rall et al., 2010; © 2016 The Royal Entomological Society 2 R. Drieu and A. Rusch Vucic-Pestic et al., 2011). This variability of outcomes suggests a of predatory species will occur in the ambient temperature high context-dependency of trophic interaction responses to ele- treatment because the complementary habitat domain limited vated temperature, where some interactions are magnified under interspecific interactions between predators. We expected that warming, whereas others are weakened. Moreover, because the warming effect on predators and prey will affect the feeding species differ greatly in their thermal tolerance and because niche of predators and modify the emergent effects of multiple increased temperatures affect foraging, consumption and diges- assemblages on predation rates from the substitutable effect to tion, as well as growth rates of both predators and prey, warming either risk reducing or risk enhancement for the prey. We also is assumed to potentially alter the relative strengths of top-down expected higher predation rates by individual predatory species and bottom-up effects in an ecosystem (Hoekman, 2010). in the elevated temperature treatment compared with ambient Both diversity and community composition of predators can temperature as a result of accelerated metabolism. influence the magnitude of top-down control in different ways. First, a large body of work related to biodiversity and ecosys- tem functioning suggests that a higher predator diversity leads to an increase in overall predation rates caused by niche par- Materials and methods titioning, facilitation or a higher probability of having efficient Study system predators included in the community as the number of species increases (Letourneau et al., 2009; Cardinale et al., 2012). Sec- We selected grapevine (Vitis vinifera) to test our hypothe- ond, empirical evidence indicates that increasing predator diver- ses for several reasons. First, various pests attack vineyards sity may lead to various effects on the extent of top-down con- resulting in very intensive pesticide treatments; approximately trol. Studies have found reduced top-down control as a result of 20% of the phytochemicals sprayed in agriculture in France, negative interactions among predators such as intraguild preda- measured in tons, are used to treat vineyards (Aubertot et al., tion (Martin et al., 2013). Other studies have reported a similar 2006). Moreover, this perennial crop hosts a large number of level of top-down control at a different level of predator diversity different pest species and grows in areas that are expected caused by the balance between positive and negative interactions to experience climate change in the near future with impor- (Straub et al., 2008; Letourneau et al., 2009). Finally, recent stud- tant consequences for crop production and biodiversity (Han- ies have demonstrated that important functional traits, such as nah et al., 2013). Reducing agrochemical use at the same hunting-mode, relative body size or habitat domain of predator time as maintaining yield and preserving biodiversity in those and prey, are good predictors of the rate of top-down control of agroecosystems will therefore be a major applied challenge in herbivores by their natural enemies (Schmitz, 2008; Schneider the near future. et al., 2012; Rusch et al., 2015). Our experiment used two common leafhopper (Hemiptera: Biodiversity loss is a major component of global change Cicadellidae) species that infest vines: the green leafhopper (Hooper et al., 2012). Declines in biodiversity over time have Empoasca vitis (Gothe) and the Flavescence dorée leafhopper been observed for many different communities, including nat- Scaphoideus titanus (Ball). These two leafhoppers can cause ural enemies of crop pests because of changes in climate, land severe damage to grapevine. Empoasca vitis feeds by punctur- use or farming practices (Robinson & Sutherland, 2002; Thomas ing phloem vessels of the leaves leading to obstruction of the et al., 2004). However, the way that predator diversity will affect vessels and leaf necrosis, thereby resulting in a reduced pho- top-down control in agroecosystems remains poorly understood tosynthetic rate and delayed fruit maturity (Chuche & Thiéry, (Letourneau et al., 2009). There is increasing concern that stud- 2014). Scaphoideus titanus is the only known vector of Flaves- ies investigating the consequences of individual components of cence dorée, a phytoplasma-borne disease, one of the most global change may not reflect their synergistic or antagonistic severe and damaging diseases in European vineyards; this dis- joint effects in real ecosystems or ecological communities (Did- ease causes major economic losses (Chuche & Thiéry, 2014). ham et al., 2007; Tylianakis et al., 2008; Hoover et al., 2012; These two leafhopper species are found at the same time Rosenblatt & Schmitz, 2014). Complex interactions between period on vines but usually occur at different phenological multiple drivers of global change provide an important reason stages (adult and larva). Both species are mainly active at night for considering more than one driver if we are to understand how (from 18.00 to 08.00 h) and stay on the leaves during the day ecosystem functioning will respond to global change. (Lessio & Alma, 2004). In the present study, we examined how