Exploring multitrophic interactions in oilseed rape fields reveals the prevailing role of Carabidae

Abstract

In cropped fields, birds are often at the highest position in the food chain, feeding on pest arthropods and their intermediate predators in a process known as intraguild predation. The net effects of bird predation on phytophagous insect populations (feeding on plants) are difficult to predict without comprehensively describing prey-predator communities and their complex interplay. We sampled bird and arthropod communities in 30 oilseed rape fields in the spring of 2019 and 2020 in France. To assess the top-down control of arthropods by birds, we used a vertebrate exclusion experiment. Using a taxonomic and functional trait-based approach, we determined the direct and indirect influences of birds on arthropod predators and phytophagous insect populations in arable crops. We observed a negative relationship between the abundance of Carabidae and phytophagous insects but not with the other predator group suggesting the key role of Carabidae on phytophagous insects in agroecosystem. We found no statistical evidence of intraguild predation from birds toward intermediate predators. Despite the lack of overall effect of predator functional diversity on their prey, we highlighted the negative relationship between the functional complementarity (through functional evenness) of Carabidae and the abundance of phytophagous insects. This result suggests that functional complementarity between Carabidae species could help to reduce phytophagous insect populations. We analyzed the effect of agricultural practices on these multitrophic interactions, showing that pesticide intensity only had detrimental effects on Carabidae abundance, while the frequency of tillage did not affect the studied communities. Complementary indices used to depict communities are helpful to better understand the mechanisms underlying trophic relationships.

Keywords: avian predation; biological control; food web; functional diversity; trophic‐level interactions.

FIGURE 1

Design of the bird exclusion experiment, photograph of a bird exclusion cage in an oilseed rape field in late February and photograph of a Western Yellow Wagtail (Motacilla flava) on oilseed rape

FIGURE 2

Hypothetical food web relationship using structural equation models in oilseed rape crop. (a) taxonomic approach based on abundance; (b) trophic approach with community trophic index (CTI); (c) functional approach based on functional diversity (FD) indices with Rao's quadratic entropy (RaoQ), functional evenness (Feve), or functional dissimilarities (Fdis) depending on the model

FIGURE 3

Boxplots of the number of arthropods with and without birds. “Other predators” corresponds to the sum of Staphylinidae, Opiliones, and Chilopoda abundances. “All phytophagous insects” include Thysanoptera, Cicadomorpha, Curculionidae, Nitidulidae, and Chrysomelidae. “Alternative prey” includes Collembola and Acari

FIGURE 4

Structural equation modeling showing direct and indirect relationships between (a) the abundance of predators and phytophagous arthropods (model 1 in a‐1 and 2 in a‐2; Table 1), (b) the mean trophic level of predators (model 4; Table 1), and (c) the functional diversity (RaoQ) and functional evenness (Feve) of predators on the one hand and the abundance of phytophagous arthropods on the other (model 6 in c‐1 and 8 in c‐2; Table 1). Black and grey lines indicate positive and negative relationships, respectively. Solid lines represent significant relationships (p < .05) and dotted lines represent trends (0.05 < p < .10). We reported standardized estimates (with “*” for significant relationships and “.” for trends) for each arrow and marginal R ² (R ² m). Other predators correspond to the sum of abundances of Staphylinidae, Opiliones, and Chilopoda individuals. Phytophagous insects include Thysanoptera, Cicadomorpha, Curculionidae, Nitidulidae, and Chrysomelidae. Pesticide is the treatment frequency index