Abstract

Biological pest control (i.e. 'biocontrol') agents can have direct and indirect non-target impacts, and predicting these effects (especially indirect impacts) remains a central challenge in biocontrol risk assessment. The analysis of ecological networks offers a promising approach to understanding the community-wide impacts of biocontrol agents (via direct and indirect interactions). Independently, species traits and phylogenies have been shown to successfully predict species interactions and network structure (alleviating the need to collect quantitative interaction data), but whether these approaches can be combined to predict indirect impacts of natural enemies remains untested. Whether predictions of interactions (i.e. direct effects) can be made equally well for generalists vs. specialists, abundant vs. less abundant species, and across different habitat types is also untested for consumer-prey interactions. Here, we used two machine-learning techniques (random forest and k-nearest neighbour; KNN) to test whether we could accurately predict empirically-observed quantitative host-parasitoid networks using trait and phylogenetic information. Then, we tested whether the accuracy of machine-learning-predicted interactions depended on the generality or abundance of the interacting partners, or on the source (habitat type) of the training data. Finally, we used these predicted networks to generate predictions of indirect effects via shared natural enemies (i.e. apparent competition), and tested these predictions against empirically observed indirect effects between hosts. We found that random-forest models predicted host-parasitoid pairwise interactions (which could be used to predict attack of non-target host species) more successfully than KNN. This predictive ability depended on the generality of the interacting partners for KNN models, and depended on species' abundances for both random-forest and KNN models, but did not depend on the source (habitat type) of data used to train the models. Further, although our machine-learning informed methods could significantly predict indirect effects, the explanatory power of our machine-learning models for indirect interactions was reasonably low. Combining machine-learning and network approaches provides a starting point for reducing risk in biocontrol introductions, and could be applied more generally to predicting species interactions such as impacts of invasive species.

Highlights

  • Growing public concern about the harmful health and environmental effects of pesticides [1, 2], combined with the rapid evolution of pest resistance to chemical control [3,4,5], mean that biocontrol agents are increasingly being advocated to suppress pests [6,7,8]

  • Can random forest and k-nearest neighbour (KNN) predict interaction frequencies and does this predictive ability vary with species’ generality and abundance, and whether the model was trained on data from the same vs. different habitat? To test the possibility that random-forest-predicted probability and KNN-predicted-frequency can predict observed interaction frequencies, and to compare the predictive ability of each random forest with that of its corresponding KNN model (‘native’, ‘plantation’, or ‘combined’), we fitted two Poisson generalised linear mixed effect models using observed interaction frequency as the response variable

  • For the less complex set of models, we found that random forest was more successful than KNN at predicting interaction frequencies

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Summary

Introduction

Growing public concern about the harmful health and environmental effects of pesticides [1, 2], combined with the rapid evolution of pest resistance to chemical control [3,4,5], mean that biocontrol agents are increasingly being advocated to suppress pests [6,7,8]. Biocontrol agents are often a more environmentally friendly means of suppressing pests than synthetic pesticides, they can have non-target effects on native species [9,10,11]. In addition to directly affecting individual non-target species (i.e. direct effects), biocontrol agents have the potential to affect communities through indirect effects (i.e. the effect of one species on another mediated by a third species) [14]. These indirect effects are more difficult to observe (or predict) because of the inherent difficulty in studying whole communities of interacting species and attributing causation to changes in potentially indirectly affected populations. Various tools (e.g. host range experiments) exist for assessing the potential direct effects of proposed biocontrol agents, to our knowledge, there are currently no methods available for quantifying and ranking potential non-target impacts of proposed biocontrol agents via indirect effects prior to their release [13], despite them being likely to be common [15, 16]

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