Theory on trophic interactions predicts that predators increase plant biomass by feeding on herbivores, an indirect interaction called a trophic cascade. Theory also predicts that predators feeding on predators, or intraguild predation, will weaken trophic cascades. Although past syntheses have confirmed cascading effects of terrestrial arthropod predators, we lack a comprehensive analysis for vertebrate insectivores-which by virtue of their body size and feeding habits are often top predators in these systems-and of how intraguild predation mediates trophic cascade strength. We report here on a meta-analysis of 113 experiments documenting the effects of insectivorous birds, bats, or lizards on predaceous arthropods, herbivorous arthropods, and plants. Although vertebrate insectivores fed as intraguild predators, strongly reducing predaceous arthropods (38%), they nevertheless suppressed herbivores (39%), indirectly reduced plant damage (40%), and increased plant biomass (14%). Furthermore, effects of vertebrate insectivores on predatory and herbivorous arthropods were positively correlated. Effects were strongest on arthropods and plants in communities with abundant predaceous arthropods and strong intraguild predation, but weak in communities depauperate in arthropod predators and intraguild predation. The naturally occurring ratio of arthropod predators relative to herbivores varied tremendously among the studied communities, and the skew to predators increased with site primary productivity and in trees relative to shrubs. Although intraguild predation among arthropod predators has been shown to weaken herbivore suppression, we find this paradigm does not extend to vertebrate insectivores in these communities. Instead, vertebrate intraguild predation is associated with strengthened trophic cascades, and insectivores function as dominant predators in terrestrial plant-arthropod communities.bottom-up and top-down control | intraguild predation | meta-analysis | trophic cascade | vertebrate predator exclusion R esearch demonstrates that predators, by feeding on herbivores, can increase plant biomass via the indirect interaction commonly labeled a trophic cascade (1). In recent years, metaanalyses have quantified trophic cascades separately in terrestrial (2, 3) and aquatic systems (4, 5) and in multiple habitats together to compare the strength of trophic cascades among ecosystem types (6). Although the strengths of trophic cascades vary across ecosystem types, explanations for the significant residual variation within ecosystems remain enigmatic (6-8).Vertebrate insectivores such as birds, bats, and lizards often feed as top predators on terrestrial arthropod communities, but based upon current theory it is unclear whether their effects should cascade down to affect plant biomass. Because of their large body size relative to arthropod prey, vertebrate insectivores can consume both predatory and herbivorous arthropods (9, 10). As a consequence, vertebrate insectivores may feed as so-called intraguild predators ...
Abstract. Herbivores affect plants through direct effects, such as tissue damage, and through indirect effects that alter species interactions. Interactions may be positive or negative, so indirect effects have the potential to enhance or lessen the net impacts of herbivores. Despite the ubiquity of these interactions, the indirect pathways are considerably less understood than the direct effects of herbivores, and multiple indirect pathways are rarely studied simultaneously. We placed herbivore effects in a comprehensive community context by studying how herbivory influences plant interactions with antagonists and mutualists both aboveground and belowground. We manipulated early-season aboveground herbivore damage to Cucumis sativus (cucumber, Cucurbitaceae) and measured interactions with subsequent aboveground herbivores, root-feeding herbivores, pollinators, and arbuscular mycorrhizal fungi (AMF). We quantified plant growth and reproduction and used an enhanced pollination treatment to determine if plants were pollen limited. Increased herbivory reduced interactions with both antagonists and mutualists. Plants with high levels of early herbivory were significantly less likely to suffer leaf damage later in the summer and tended to be less attacked by root herbivores. Herbivory also reduced pollinator visitation, likely due to fewer and smaller flowers, and reduced AMF colonization. The net effect of herbivory on plant growth and reproduction was strongly negative, but lower fruit and seed production were not due to reduced pollinator visits, because reproduction was not pollen limited. Although herbivores influenced interactions between plants and other organisms, these effects appear to be weaker than the direct negative effects of early-season tissue loss.
Plants experience unique challenges due to simultaneous life in two spheres, above- and belowground. Interactions with other organisms on one side of the soil surface may have impacts that extend across this boundary. Although our understanding of plant-herbivore interactions is derived largely from studies of leaf herbivory, belowground root herbivores may affect plant fitness directly or by altering interactions with other organisms, such as pollinators. In this study, we investigated the effects of leaf herbivory, root herbivory, and pollination on plant growth, subsequent leaf herbivory, flower production, pollinator attraction, and reproduction in cucumber (Cucumis sativus). We manipulated leaf and root herbivory with striped cucumber beetle (Acalymma vittatum) adults and larvae, respectively, and manipulated pollination with supplemental pollen. Both enhanced leaf and root herbivory reduced plant growth, and leaf herbivory reduced subsequent leaf damage. Plants with enhanced root herbivory produced 35% fewer female flowers, while leaf herbivory had no effect on flower production. While leaf herbivory reduced the time that honey bees spent probing flowers by 29%, probing times on root-damaged plants were over twice as long as those on control plants. Root herbivory increased pollen limitation for seed production in spite of increased honey bee preference for plants with root damage. Leaf damage and hand-pollination treatments had no effect on fruit production, but plants with enhanced root damage produced 38% fewer fruits that were 25% lighter than those on control plants. Despite the positive effect of belowground damage on honey bee visitation, root herbivory had a stronger negative effect on plant reproduction than leaf herbivory. These results demonstrate that the often-overlooked effects of belowground herbivores may have profound effects on plant performance.
Abstract. Insectivorous birds reduce arthropod abundances and their damage to plants in some, but not all, studies where predation by birds has been assessed. The variation in bird effects may be due to characteristics such as plant productivity or quality, habitat complexity, and/or species diversity of predator and prey assemblages. Since agroforestry systems vary in such characteristics, these systems provide a good starting point for understanding when and where we can expect predation by birds to be important. We analyze data from bird exclosure studies in forests and agroforestry systems to ask whether birds consistently reduce their arthropod prey base and whether bird predation differs between forests and agroforestry systems. Further, we focus on agroforestry systems to ask whether the magnitude of bird predation (1) differs between canopy trees and understory plants, (2) differs when migratory birds are present or absent, and (3) correlates with bird abundance and diversity. We found that, across all studies, birds reduce all arthropods, herbivores, carnivores, and plant damage. We observed no difference in the magnitude of bird effects between agroforestry systems and forests despite simplified habitat structure and plant diversity in agroforests. Within agroforestry systems, bird reduction of arthropods was greater in the canopy than the crop layer. Top-down effects of bird predation were especially strong during censuses when migratory birds were present in agroforestry systems. Importantly, the diversity of the predator assemblage correlated with the magnitude of predator effects; where the diversity of birds, especially migratory birds, was greater, birds reduced arthropod densities to a greater extent. We outline potential mechanisms for relationships between bird predator, insect prey, and habitat characteristics, and we suggest future studies using tropical agroforests as a model system to further test these areas of ecological theory.
An important stabilizing mechanism in most diversity stability models is the insurance hypothesis, which involves correlation/covariance relationships among species. These models require that species do not fluctuate synchronously over time: that is, the correlation between pairs of species does not equal 1.0. However, the strength of this stabilizing mechanism increases as correlations decline away from 1.0, especially as they become more negative and also as the summed covariance across all species pairs becomes more negative. We evaluated the importance of the insurance hypothesis as a stabilizing mechanism by examining a variety of terrestrial assemblages using long-term data from the Global Population Dynamics Database, the Breeding Bird Survey, and a long-term site in southeastern Arizona, USA. We identified co-occurring assemblages of species and calculated the Spearman rank correlations of all pairs of species and the summed covariance of the entire assemblage. We found that, in most assemblages, positive correlations were two to three times more common than negative and that the magnitude of the positive correlations tended to be stronger than the negative correlations. For all but three assemblages, the summed covariance was positive. Data from larger spatial scales tended to exhibit more positive correlations, but even at the smallest spatial scales, positive correlations outnumbered negative. We suggest that species often covary positively because coexisting species respond similarly to fluctuations in their resource base driven by climatic fluctuations. As such, our review suggests that the insurance hypothesis may not be a strong mechanism stabilizing fluctuations in natural terrestrial communities.
While an extensive literature exists on the negative effects of invasive species, little is known about their facilitative effects on native species, particularly the role of invasives as trophic subsidies to native predators. The invasive gypsy moth (Lymantria dispar) undergoes periodic outbreaks during which it represents a super-abundant food source for predators capable of consuming it, particularly native cuckoos (Coccyzus erythropthalmus and C. americanus). We examined how gypsy moth outbreaks affect the abundance and distribution of cuckoos using the North American Breeding Bird Survey and 29 years of U.S. Forest Service gypsy moth defoliation records. Abundances of both Black-billed and Yellow-billed Cuckoos were significantly above average during outbreaks, but populations were average or below average in preceding and subsequent years, suggesting that cuckoos are immigrating to defoliations during outbreak years. Spatial analyses showed that cuckoo abundances approximately 40-150 km outside of defoliation areas were significantly below average, and these under-occupied breeding areas extended in all four compass directions around outbreaks. This result supports the idea that cuckoos locate gypsy moth outbreaks during a post-migratory nomadic phase. By shifting the annual distribution of cuckoos, gypsy moths may be shifting the trophic impact of cuckoos across large distances, which could affect native insect herbivores and plants.
Summary Ecosystem restoration is an important tool for mitigating biodiversity loss and recovering critical ecosystem services to humanity, but restoration rarely takes into account the evolutionary attributes of the community being restored. Phylogenetic diversity (PD) represents a potentially valuable measure of restoration success because it can correlate with functional trait diversity that drives ecosystem function. However, PD patterns in restored communities are rarely assessed. We surveyed plant communities in restored tallgrass prairies 2–19 years old and calculated two PD measures, SESMNTD and SESMPD, of the communities and seed mixture applied to sites. We also identified high‐threat exotic species present in each site to determine whether PD of the seed mixture applied was related to resistance against invasion. We show that PD in North American tallgrass prairie restorations, as measured by both SESMNTD and SESMPD, is maintained over time even as richness declines. Neither the resulting community PD nor invasion by high‐threat exotic species was affected by PD of the seed mixture used in site restoration. Thus, simply maximizing PD of seed mixtures without considering the particular component species is unlikely to help achieve restoration goals. Synthesis and applications. These results suggest that species losses over time are not biased towards species with or without close relatives in the community. If phylogenetic diversity (PD) reflects functional trait diversity in communities, then local declines in species richness may not necessarily mean the loss of ecosystem function in restoration projects. However, PD of restored communities may be limited by low establishment rates for most species. Conservation practitioners should consider PD with careful planning to maintain overall community diversity and potentially maximize ecosystem function and services in restorations. This perspective will require a deeper understanding of the relationships between phylogenetic relatedness and traits associated with competition and fitness.
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