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From a conservation biological control perspective, the attention of agroecologists has increasingly focused on the relationship between arthropod predator diversity and pest suppression. Numerous studies have provided consistent evidence that arthropod predators can effectively suppress populations of crop pests (Symondson et al., 2002; Snyder et al., 2005). However, the understanding of how and whether pest regulation is enhanced by changes in predator diversity remains limited (Straub et al., 2008).
Theory suggests that there are a variety of mechanisms by which changes in predator diversity could enhance prey suppression (Sih et al., 1998; Ives et al., 2005) and strengthen the top-down biological pest control. The sampling (Huston, 1997), or positive selection (Loreau, 2000) effect refers to the probability that a diverse predator community will include key species with unusually high consumption rates. Therefore, the performance of the predator community with regard to prey suppression may be driven primarily by whether these best-performing species are present. Changes in predator diversity can enhance prey suppression also through complementary resource use (Tilman et al., 1997; Loreau, 2000). Different predator species often consume different prey species (Duffy, 2002) or different life-history stages of a single prey species (Wilby et al., 2005). Such complementarity in resource use suggests that the effect of predators is additive if the prey mortality that results from the combined action of different species is equal to the summed mortality caused by each predator species on its own (Snyder et al., 2005).
In addition to its positive effect on prey suppression enhancement, changes in predator diversity sometimes leads to increasing intra-guild predation among predator species, which reduces their collective effect on prey suppression (Straub et al., 2008; Letourneau et al., 2009). The effects of changes in predator diversity on prey suppression could also be neutral. This occurs when multiple predators have ‘redundant’ or ‘compensatory’ effects, i.e. their combined effects are the average of the corresponding single-species effect (Sokol-Hessner & Schmitz, 2002; Schmitz, 2007). Thus, the removal of one species is compensated by increases in the prey consumption by another species (Navarrete & Menge, 1996; Otto et al., 2008). This effect is encompassed in the insurance hypothesis (Tilman, 1996), which states that redundancy stabilises the aggregate predation rates in the face of environmental changes (Wellnitz & Poff, 2001).
In spite of the growing number of studies investigating how changes in predator diversity could enhance prey suppression, little has been done to examine the effects of variation in predator traits (functional diversity) that mediate such mechanisms. Previous research on the effects of predator diversity on prey suppression have focused almost exclusively on predator species richness, whereas biodiversity-ecosystem function studies suggest that functional diversity rather than richness per se drives ecological processes, such as prey suppression (Schmitz, 2007, 2009; Bruno & Cardianale, 2008). Predator body size is considered to be a key functional trait determining the strength and type of species interactions (Delclos & Rudolf, 2011; Rudolf, 2012) and, therefore, how predator diversity affects prey suppression (Brose, 2010; Rudolf, 2012). This attribute influences the habitat choice, prey size, range of prey, and consumption rate of the predator (Cohen et al., 1993). Predator size also determines the individual body mass and the biomass of a population as a whole (Woodward et al., 2010). Predator size variation can enhance prey suppression through an increase in the average body size that increases the per capita consumption rates of predators (Rudolf, 2012). Mechanisms such as complementary resource use could apply similarly to the ecological effects of body size variation among predator species (Woodward & Hildrew, 2002; Rudolf, 2012). Indeed, increasing the size range of predators has the potential to increase resource partitioning in terms of prey size (Woodward & Hildrew, 2002) and, therefore, enhance prey suppression through niche complementarity (Rudolf, 2012). The presence of different-sized species within a predator population could, however, lead to increasing the negative interferences between the predators (e.g. intra-guild predation). These antagonistic interactions should decrease the strength of top-down prey control (Delclos & Rudolf, 2011; Rudolf, 2012).
Given their cosmopolitan distribution, their polyphagy, and their taxonomic and functional diversity, ground beetles are especially suitable organisms for both ecological and entomological studies. Ground beetles are an important component of the ground-dwelling fauna of most of the world's terrestrial environments. They are predators of many invertebrate pests in agricultural ecosystems, such as aphids (Schmidt et al., 2004) and slugs (Mair & Port, 2001; Oberholzer & Frank, 2003). Thus, they may be potential biological control agents. With more than 40 000 described species, ground beetles are likely to have greater levels of diversity in traits associated with prey capture and consumption. Although superficially most ground beetle species seem to have a similar body shape, there are species-specific differences and the morphological particularities of each species reflect the special demands of its niche (Loreau, 1983; Bauer et al., 1998; Kromp, 1999). Ground beetles show considerable variation in their size. This trait diversity may lead to complementary resource use.
The objective of the present study was to determine how changes in the body size diversity of ground beetles influence prey suppression. To accomplish this objective and using a functional group approach, we have created ground beetle assemblages according to three levels of size diversity: low, medium, and high. Three species groups of a different size (large, medium, and small) were used as units of diversity in creating assemblages. Comparing prey suppression between the created assemblages enabled us to test whether increasing the ground beetles' body size diversity enhances prey suppression through a complementary resource use or through a sampling effect of the best performing size group of species. In addition, we used the variation in the species composition of the created assemblages to test if there is (or not) an additive effect among species of the best performing size group.
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Partitioning the effects of ground beetle size diversity in our study revealed that prey suppression by ground beetles depends on their functional identity rather than on functional diversity, with one group of species (large beetles) contributing more to prey suppression than the other groups. Indeed, in the assemblages containing at least one large ground beetle species, prey suppression was significantly greater than in assemblages without large ground beetles. Such relationships between predator size diversity and prey suppression is common in a variety of systems and taxa (Radloff & Du Toit, 2004; Bruno et al., 2005, 2006; Arenas et al., 2006; Philpott et al., 2009; Valdivia et al., 2009; Rudolf, 2012; Toscano & Griffen, 2012). An identity effect for large ground beetles found in our study is in agreement with the hypothesis given by Rudolf (2012) to explain the ecological effects of variation in predator body size on prey suppression, and according to which this variation can increase prey suppression through increases in the average size that increases the per capita consumption rates of predators. As for other organisms (Reiss et al., 2011), large ground beetles most likely have higher mass-specific metabolic rates, higher energy demands, and higher ingestion rates than small species.
The neutral effect of increasing ground beetle size diversity was not surprising given that there was no partitioning of resource between small, medium, and large species. Although we showed distinct patterns in prey consumption, the different-sized ground beetles did not occupy distinct trophic niches. The results revealed an increase in the amount and range of prey consumed with increasing ground beetle body size; small ground beetles showed low prey consumption and did not attack adult slugs, whereas large ground beetles showed maximum prey suppression and demonstrated an ability to consume all of the prey species. Neutral effects of predators' diversity on prey suppression are often expected to occur when increasing the diversity within a predator population increases the potential for intra-guild predation as well as for negative behavioural interference (Letourneau et al., 2009). For example, in the presence of a large predator, small ones often alter their activity rates or habitat use, which also reduces their foraging rates that indirectly alter prey suppression (Prasad & Snyder, 2006; Crumrine, 2010; Rudolf, 2012). In our case, such negative interactions could not be responsible for the neutral effect of the increasing ground beetle size diversity on prey suppression. All of the ground beetles were alive at the end of the experiment, indicating that there was no intra-guild predation. Additionally, we expect that large ground beetles in the more diverse assemblages did not reduce or only slightly reduced the foraging rates of the small ground beetle species, as the prey suppression was low even when these small species were present alone (Assemblage 1, Fig. 1).
Excluding negative interactions to explain the neutral effect of increasing the ground beetle size diversity effect on prey suppression does not exclude that it is the absence of intra-guild predation among the large ground beetle species (best performing predators in our study) that may leads to the evident identity effect of this species group rather than ground beetles size diversity per se. Indeed, in the absence of negative interferences among species that overlap in resource use, there would be no advantage of resource use differentiation and no significant difference between predator diversity treatments (Snyder & Ives, 2003). At least two explanations can account for the absence of intra-guild predation and ground beetles' functional diversity effect in our study.
Predator to prey ratio
It may be possible that the ratio of predators to prey in our experiment was too low (i.e. the prey offered were sufficient enough) for antagonistic interactions to occur among the ground beetles. Most of the studies that have examined the effects of prey density on the outcome of predator–predator interactions have found that lower prey density increases intra-guild predation, whereas higher prey density results in synergetic interactions (Lucas et al., 1998; Kajita et al., 2000; Hindayana et al., 2001; Burgio et al., 2002; de Clercq et al., 2003; Nóia et al., 2008). Werling et al. (2012) showed that combining two functionally distinct predators increased the predation of Colorado potato beetle only when the larval density of this insect pest was low. However, Griffin et al. (2008) found that functionally diverse communities of crab species showed greater prey consumption only when the predator density was high. This observation has also been reported in other previous studies (Griffin et al., 2008; Takizawa & Snyder, 2011), in which reducing the intra-specific density of predators reduced the resource overlap and interference and, therefore, had a greater effect on prey suppression.
Our experiment may not have lasted long enough to detect the positive indirect effects on prey suppression that may result from interferences among ground beetle species of the same group. As shown above, intra-guild predation occurrence usually involves a lower prey density. The short time scales of our experiment could have been insufficient for prey density to be reduced by the ground beetle consumption and then to reach the ‘critical threshold’ that trigger intra-guild predation. Previous studies suggested that intra-guild predation requires prey density changes, which may take some time to manifest (Rosenheim, 2001)
While we found evidence for a functional identity effect, there was no species identity effect, as prey suppression in the assemblages where the three large ground beetles occurred separately was not different. Additionally, the effects of these three ground beetle species on prey suppression seems to be non-additive but redundant in the sense that there was no difference in prey suppression between the assemblages in which two species were present together and those in which each species was present separately. The redundant effects of the large ground beetle species suggest that they occupy similar trophic niches, have overlapping resources, and interfere with each other. Indeed, when such effects occurred, they were often related to competition for food among predators that alter the behaviours of the predators. They were also related to intra-guild predation that often occurs between certain life history stages, such as adults preying on juveniles, or when one of the predators is an intermediate predator (often because of its small size) and is vulnerable to predation by the top predator (Rosenheim, 1998; Finke & Denno, 2002; Crumrine & Crowley, 2003; Lang, 2003; Griffen & Byers, 2006). Because all of the ground beetles were recovered at the end of our experiment, we suggest that inter-specific competition for food, and not intra-guild predation, was responsible for the non-additive effect among the three large ground beetle species. However, we have no evidence that this behavioural interference existed in our experiment. A similar non-additive effect of multiple predators was observed in a system composed of three spider species preying upon the grasshopper Melanoplus femurrubrum (De Geer) (Sokol-hessner & Schmitz, 2002). The spiders had different hunting modes and occupied complementary habitats, but their combined effects were equivalent to the average of the corresponding single-species effect. The authors concluded that the species effects of the three spiders were substitutable and that it is reasonable to aggregate them into a single functional unit. The same results were also found by Woodcock and Heard (2011). Similar effects of the three large ground beetles in our experiment validate the fact that they have been treated as a single functional group and suggest that the effect of ground beetles on prey suppression should depend on the presence of large ground beetles, independent of their species identity.
Although predators of the same guild could have a non-additive (redundant) effect, increasing their number could increases prey suppression through a resource use complementarity (Powell et al., 2006). Moreover, species that appear functionally redundant under some environmental conditions are functionally diverse when environmental conditions change (Naeem & Li, 1997). This effect is encompassed in the ‘insurance hypothesis’, which states that maintaining different predators that perform better or worse in particular environments provides functional compensation and reliable pest suppression in spite of changing conditions (Loreau et al., 2003). Also, it has been suggested that if predator communities contain functionally redundant species, key aspects of community and ecosystem processes may remain unchanged by the changes in species' compositions as long as each broad functional group retains at least one functionally competent species (Morin, 1995). This suggestion is consistent with the results found in the present study. Indeed, there were no differences in prey suppression between the assemblages that included at least one large ground beetle species, except assemblage in which the three large species occurred together (A3) and in which prey suppression was more important than in two other assemblages (A7 and A8).
This study found that increasing the size diversity of ground beetles had no effect on the strength of prey suppression. Instead, prey suppression was strongly strengthened by the presence of large ground beetles (irrespective of their species identity). Based on these results and given that large ground beetles are vulnerable to environmental disturbances (Ribera et al., 2001; Kotze & O'Hara, 2003) and predation (Kaspari & Joern, 1993; Brose, 2003), we suggest that conservation biological control strategies should promote the presence of large carabids. These strategies should, however, be established without being in conflict with the global objectives of biodiversity conservation. Redundancy among species should also be considered in conservation biological control strategies. Indeed, given that the local and global extinctions are more likely for species occupying higher trophic levels than for species at lower trophic levels within food webs (Petchey et al., 1999), it is always important to maintain redundancy both among and within local communities because species that are redundant in their effects will not necessarily have the same responses to environmental change (Wellnitz & Poff, 2001). Thus, this redundancy could provide insurance against loss or degradation of the biological pest suppression (Walker, 1991)