Abstract

Simple SummaryMismatched distributions between biological control agents and their host plants occur for a variety of reasons but are often linked to climate, specifically differences in their low-temperature tolerances. How to measure and use low-temperature tolerances of control agents to inform agent prioritization, selection for redistribution, or predict efficacy is vitally important, but has not been previously synthesized in a single source. We discuss causes of climate mismatches between agents and target weeds, the traditional and non-traditional approaches that could be used to decrease the degree of mismatch and improve control, and regulatory issues to consider when taking such approaches. We also discuss the variety of cold tolerance metrics, their measurement and ecological value, and the types of modeling that can be carried out to improve predictions about potential distributions of agents. We also briefly touch on molecular bases for cold tolerance and opportunities for improving cold tolerance of agents using modern molecular tools.Many weed biological control programs suffer from large-scale spatial variation in success due to restricted distributions or abundances of agents in temperate climates. For some of the world’s worst aquatic weeds, agents are established but overwintering conditions limit their survival in higher latitudes or elevations. The resulting need is for new or improved site- or region-specific biological control tools. Here, we review this challenge with a focus on low-temperature limitations of agents and propose a roadmap for improving success. Investigations across spatial scales, from global (e.g., foreign exploration), to local (selective breeding), to individual organisms (molecular modification), are discussed. A combination of traditional (foreign) and non-traditional (introduced range) exploration may lead to the discovery and development of better-adapted agent genotypes. A multivariate approach using ecologically relevant metrics to quantify and compare cold tolerance among agent populations is likely required. These data can be used to inform environmental niche modeling combined with mechanistic modeling of species’ fundamental climate niches and life histories to predict where, when, and at what abundance agents will occur. Finally, synthetic and systems biology approaches in conjunction with advanced modern genomics, gene silencing and gene editing technologies may be used to identify and alter the expression of genes enhancing cold tolerance, but this technology in the context of weed biological control has not been fully explored.

Highlights

  • Management of invasive plants with biological control agents has the potential to be a cost-effective tool with long-lasting ecological and economic benefits

  • Kriticos and Brunel [39] found that the native potential distribution of P. crassipes under historical and future climate scenarios was smaller than predicted by environmental niche modelling

  • The sustainable, cost-savings benefits of biological control programs may be offset by the occurrence of climate mismatches between agents and target weeds in the introduced range

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Summary

Introduction

Management of invasive plants with biological control agents has the potential to be a cost-effective tool with long-lasting ecological and economic benefits. The influence of geographic variation on the outcome of biological control programs is often related to the differential responses of agents and target weeds to biotic or abiotic factors, of which precipitation and/or temperature seem to be the most critical [8]. These differential responses may lead to cases where agent and host climate envelopes, and distributions, do not overlap completely (Figure 1b–d). Biological control programs for these invaders have resulted in regional success but agents are often more limited in their distribution than their target weeds [9,10,11,12].

Why Does Climate Mismatch Occur?
Inadequate Exploration
Climate Niche Shifts and Expansions
Traditional Approaches
Non-Traditional Approaches
Cold Tolerance Metrics and Their Application
Measures of Failure
Measures of Performance
Predicting Distributions of Agents and Hosts
Mechanistic Modelling
Fitted Process-Based Models
Non-Classical Biological Control
Molecular Mechanisms Underlying Cold Tolerance
Enhancing Cold Hardiness
Regulatory Considerations
Findings
Conclusions and Recommendations
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