How do belowground organisms influence plant-pollinator interactions?

Barber, Nicholas A.; Gorden, Nicole L. Soper

doi:10.1093/jpe/rtu012

Cited by 78 publications

(79 citation statements)

References 104 publications

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“…Soil arthropods are an abundant group of macro-invertebrates that can affect plants either directly, via root herbivory or indirectly, via decomposition of organic material. Although an increasing number of studies report on mechanisms through which root herbivory might impact aboveground plant-insect interactions (e.g., reviewed in Soler et al, 2012;Barber and Soper Gorden, 2014), most reviews remain inconclusive about the drivers behind the effects that are often observed. A metaanalysis showed that root herbivory by Diptera generally results in significantly negative effects on aboveground herbivores (Johnson et al, 2012), whereas herbivory by Coleoptera influences only aboveground Homoptera (positively) and herbivorous Hymenoptera (negatively), but has no significant effect on other groups.…”

Section: Soil Arthropodsmentioning

confidence: 99%

“…Soil arthropods often cause association-specific effects on their host plants, ranging from changes in flower number to flower size and nectar quality, which all may influence different types of pollinating insects (Barber and Soper Gorden, 2014). Likewise, there is no evident pattern for field studies ( Figure 2D, Supplementary Table 4).…”

Section: The Effect Of Root Herbivores On Aboveground Pollinatorsmentioning

confidence: 99%

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Effects of Soil Organisms on Aboveground Plant-Insect Interactions in the Field: Patterns, Mechanisms and the Role of Methodology

et al. 2018

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Soil biota-plant interactions play a dominant role in terrestrial ecosystems. Through nutrient mineralization and mutualistic or antagonistic interactions with plants soil biota can affect plant performance and physiology and via this affect plant-associated aboveground insects. There is a large body of work in this field that has already been synthesized in various review papers. However, most of the studies have been carried out under highly controlled laboratory or greenhouse conditions. Here, we review studies that manipulate soil organisms of four dominant taxa (i.e., bacteria, fungi, nematodes, and soil arthropods) in the field and assess the effects on the growth of plants and interactions with associated aboveground insects. We show that soil organisms play an important role in shaping plant-insect interactions in the field and that general patterns can be found for some taxa. Plant growth-promoting rhizobacteria generally have negative effects on herbivore performance or abundance, most likely through priming of defenses in the host plant. Addition of arbuscular mycorrhizal fungi (AMF) has positive effects on sap sucking herbivores, which is likely due to positive effects of AMF on nutrient levels in the phloem. The majority of AMF effects on chewers were neutral but when present, AMF effects were positive for specialist and negative for generalist chewing herbivores. AMF addition has negative effects on natural enemies in the field, suggesting that AMF may affect plant attractiveness for natural enemies, e.g., through volatile profiles. Alternatively, AMF may affect the quality of prey or host insects mediated by plant quality, which may in turn affect the performance and density of natural enemies. Nematodes negatively affect the performance of sap sucking herbivores (generally through phloem quality) but have no effect on chewing herbivores. For soil arthropods there are no clear patterns yet. We further show that the methodology used plays an important role in influencing the outcomes of field studies. Studies using potted plants in the field and studies that remove target soil taxa by means of pesticides are most likely to detect significant results. Lastly, we discuss suggestions for future research that could increase our understanding of soil biota-plant-insect interactions in the field.

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Section: Soil Arthropodsmentioning

confidence: 99%

Section: The Effect Of Root Herbivores On Aboveground Pollinatorsmentioning

confidence: 99%

Effects of Soil Organisms on Aboveground Plant-Insect Interactions in the Field: Patterns, Mechanisms and the Role of Methodology

et al. 2018

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“…For example, plants widely associate with arbuscular mycorrhizal fungi (AMF), which can enhance nutrient absorption (Brundrett and Tedersoo 2018) and induce systemic expression of proteins and genes involved in defense in root and foliar tissues (Liu et al 2007, Campos-Soriano et al 2010. To date, no study has examined the effect of AMF on floral secondary chemistry, other than floral volatiles (Becklin et al 2011), although there is evidence that AMF can increase or decrease pollinator attraction via changes in floral display (Barber and Soper Gordon 2015). Moreover, because plant benefit from AMF depends on the relative availability of soil nitrogen and phosphorus (Johnson 2010), and soil nutrients can shape nectar secondary chemistry (Adler et al 2006), AMF and nutrients may interactively influence defense expression, including in floral tissue.…”

Section: Introductionmentioning

confidence: 99%

From plant fungi to bee parasites: mycorrhizae and soil nutrients shape floral chemistry and bee pathogens

Davis

Aguirre

Barber

et al. 2019

Ecology

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Bee populations have experienced declines in recent years, due in part to increased disease incidence. Multiple factors influence bee-pathogen interactions, including nectar and pollen quality and secondary metabolites. However, we lack an understanding of how plant interactions with their environment shape bee diet quality. We examined how plant interactions with the belowground environment alter floral rewards and, in turn, bee-pathogen interactions. Soil-dwelling mycorrhizal fungi are considered plant mutualists, although the outcome of the relationship depends on environmental conditions such as nutrients. In a 2 9 2 factorial design, we asked whether mycorrhizal fungi and nutrients affect concentrations of nectar and pollen alkaloids (anabasine and nicotine) previously shown to reduce infection by the gut pathogen Crithidia in the native bumble bee Bombus impatiens. To ask how plant interactions affect this common bee pathogen, we fed pollen and nectar from our treatment plants, and from a wildflower pollen control with artificial nectar, to bees infected with Crithidia. Mycorrhizal fungi and fertilizer both influenced flowering phenology and floral chemistry. While we found no anabasine or nicotine in nectar, high fertilizer increased anabasine and nicotine in pollen. Arbuscular mycorrhizal fungi (AMF) decreased nicotine concentrations, but the reduction due to AMF was stronger in high than low-nutrient conditions. AMF and nutrients also had interactive effects on bee pathogens via changes in nectar and pollen. High fertilizer reduced Crithidia cell counts relative to low fertilizer in AMF plants, but increased Crithidia in non-AMF plants. These results did not correspond with effects of fertilizer and AMF on pollen alkaloid concentrations, suggesting that other components of pollen or nectar were affected by treatments and shaped pathogen counts. Our results indicate that soil biotic and abiotic environment can alter bee-pathogen interactions via changes in floral rewards, and underscore the importance of integrative studies to predict disease dynamics and ecological outcomes.

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“…Root herbivory can modify floral characteristics, altering interactions with pollinators (Poveda et al . , ; Barber & Soper Gorden ), and foliage traits, affecting herbivores, pathogens and parasitoids (Blossey & Hunt‐Joshi ; Soler et al . , ).…”

Section: Introductionmentioning

confidence: 99%

“…Plant–pollinator interactions illustrate this challenge. Although herbivory frequently affects floral traits (Adler ; Theis, Kesler & Adler ; Barber & Soper Gorden ) and pollinator behaviour (Strauss, Conner & Rush ; Lehtila & Strauss ; Barber, Adler & Bernardo ; Kessler, Halitschke & Poveda ; Barber et al . ), changes in pollinator visitation alone do not demonstrate that altered pollination services are the cause of reduced plant fitness.…”

Section: Introductionmentioning

confidence: 99%

Root herbivory indirectly affects above‐ and below‐ground community members and directly reduces plant performance

et al. 2015

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Summary There is a widespread recognition that above‐ and below‐ground organisms are linked through their interactions with host plants that span terrestrial subsystems. In addition to direct effects on plants, soil organisms such as root herbivores can indirectly alter interactions between plants and other community members, with potentially important effects on plant growth and fitness. We manipulated root herbivory by Acalymma vittatum in Cucumis sativus to determine indirect effects on arbuscular mycorrhizal fungi, leaf herbivory, the leaf pathogen downy mildew and pollinators. We also manipulated pollen receipt by plants to determine whether root herbivory reduced plant reproduction through changes in pollinator visitation. Overall, root herbivory had strong net negative effects on plant growth and fitness, with 34% reductions in both leaf and fruit production by high root damage levels relative to control, despite reduced infection by downy mildew. High root herbivory also reduced floral visitation by 39%, apparently due to lower flower production, as flower size and scent were unaffected. Above‐ground herbivory was not affected by root herbivores. Although root herbivory reduced pollinator visits, pollen receipt manipulations had no effect on fruit set, indicating that reduced pollinator service did not affect plant reproduction. Synthesis. Root herbivory had indirect effects on a range of community members, including mutualists and antagonists both above‐ and below‐ground. Although reduced pathogen infection associated with root herbivory would be expected to benefit plants, root herbivory had an overall strong negative effect on plant growth and reproduction, indicating that direct negative effects over‐rode any potential indirect benefits.

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How do belowground organisms influence plant-pollinator interactions?

Cited by 78 publications

References 104 publications

Effects of Soil Organisms on Aboveground Plant-Insect Interactions in the Field: Patterns, Mechanisms and the Role of Methodology

Effects of Soil Organisms on Aboveground Plant-Insect Interactions in the Field: Patterns, Mechanisms and the Role of Methodology

From plant fungi to bee parasites: mycorrhizae and soil nutrients shape floral chemistry and bee pathogens

Root herbivory indirectly affects above‐ and below‐ground community members and directly reduces plant performance

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