Abstract. Research investigating interactions between aboveground (AG) and belowground (BG) herbivores has been central to characterizing AG-BG linkages in terrestrial ecosystems, with many of these interactions forming the basis of complex food webs spanning the two subsystems. Despite the growing literature on the effects of AG and BG herbivores on each other, underlying patterns have been difficult to identify due to a high degree of context dependency. In this study, we present the first quantitative meta-analysis of AG and BG herbivore interactions. Previous global predictions, specifically that BG herbivores normally promoted AG herbivore performance and AG herbivores normally reduced BG herbivore performance, were not supported. Instead, the meta-analysis identified four factors that determined the outcome of AG-BG interactions. (1) Sequence of herbivore arrival on host plants was important, with BG herbivores promoting AG herbivore performance only when introduced to the plant simultaneously, whereas AG herbivores had negative effects on BG herbivores only when introduced first. (2) AG herbivores negatively affected BG herbivore survival but tended to increase population growth rates. (3) AG herbivores negatively affected BG herbivore performance on annual plants, but not on perennials, and these effects were observed more consistently in laboratory than field studies. (4) The type of herbivore was also important, with BG insect herbivores belonging to the order Diptera (i.e., true flies) having the strongest negative effects on AG herbivores. Coleoptera (i.e., beetles) species were the most widely investigated BG herbivores and had positive impacts on AG Homoptera (e.g., aphids), but negative effects on AG Hymenoptera (e.g., sawflies). The strongest negative outcomes for BG herbivores were seen when the AG herbivore was a Coleoptera species. We found no evidence for publication bias in AG-BG herbivore interaction literature and conclude that several biological and experimental factors are important for predicting the outcome of AG-BG herbivore interactions. The sequence of herbivore arrival on the host plant was among the most influential.
Photosynthetic pathway is an important cause of growth rate variation between species such that the enhanced carbon uptake of C4 species leads to faster growth than their C3 counterparts. Leaf traits that promote rapid resource acquisition may further enhance the growth capacity of C4 species. However, how root economic traits interact with leaf traits, and the different growth strategies adopted by plants with C3 and C4 photosynthetic pathways is unclear. Plant economic traits could interact with, or act independently of, photosynthetic pathway in influencing growth rate, or C3 and C4 species could segregate out along a common growth rate–trait relationship. We measured leaf and root traits on 100+ grass species grown from seeds in a controlled, common environment to compare with relative growth rates (RGR) during the initial phase of rapid growth, controlling for phylogeny and allometric effects. Photosynthetic pathway acts independently to leaf and root functional traits in causing fast growth. Using C4 photosynthesis, plants can achieve faster growth than their C3 counterparts (by an average 0.04 g g−1 day−1) for a given suite of functional trait values, with lower investments of leaf and root nitrogen. Leaf and root traits had an additive effect on RGR, with plants achieving fast growth by possessing resource‐acquisitive leaf traits (high specific leaf area and low leaf dry matter content) or root traits (high specific root length and area, and low root diameter), but having both leads to an even faster growth rate (by up to 0.06 g g−1 day−1). C4 photosynthesis can provide a greater relative increase in RGR for plants with a ‘slow’ ecological strategy than in those with fast growth. However, above‐ground and below‐ground strategies are not coordinated so that species can have any combination of ‘slow’ or ‘fast’ leaf and root traits. Synthesis. C4 photosynthesis increases growth rate for a given combination of economic traits, and significantly alters plant nitrogen economy in the leaves and roots. However, leaf and root economic traits act independently to further enhance growth. The fast growth of C4 grasses promotes a competitive advantage under hot, sunny conditions.
Predicted changes to the Earth’s climate are likely to affect above–belowground interactions. Our understanding is limited, however, by past focus on two-species aboveground interactions mostly ignoring belowground influences. Despite their importance to ecosystem processes, there remains a dearth of empirical evidence showing how climate change will affect above–belowground interactions. The responses of above- and belowground organisms to climate change are likely to differ given the fundamentally different niches they inhabit. Yet there are few studies that address the biological and ecological reactions of belowground herbivores to environmental conditions in current and future climates. Even fewer studies investigate the consequences of climate change for above–belowground interactions between herbivores and other organisms; those that do provide no evidence of a directed response. This paper highlights the importance of considering the belowground fauna when making predictions on the effects of climate change on plant-mediated interspecific interactions.
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