Dynamics of plant responses to combinations of air pollutants

The focus of this review is on how plants respond to combinations of multiple air pollutants. Global pollution trends, plant physiological responses and ecological perspectives in natural and agricultural systems are all discussed. In particular, we highlight the importance of studying sequential or simultaneous exposure of plants to pollutants, rather than exposure to individual pollutants in isolation, and explore how these responses may interfere with the way plants interact with their biotic community. Air pollutants can alter the normal physiology and metabolic functioning of plants. Here we describe how the phenotypic and molecular changes in response to multiple pollutants can differ compared to those elicited by single pollutants, and how different responses have been observed between plants in the field and in controlled laboratory conditions and between trees and crop plants. From an ecological perspective, we discuss how air pollution can result in greater susceptibility to biotic stressors and in direct or indirect effects on interactions with organisms that occupy higher trophic levels. Finally, we provide an overview of the potential uses of plants to mitigate air pollution, exploring the feasibility for pollution removal via the processes of bio‐accumulation and phytoremediation. We conclude by proposing some new directions for future research in the field.     

When do herbivores affect plant invasion? Evidence for the natural enemies and biotic resistance hypotheses

Two venerable hypotheses, widely cited as explanations for either the success or failure of introduced species in recipient communities, are the natural enemies hypothesis and the biotic resistance hypothesis. The natural enemies hypothesis posits that introduced organisms spread rapidly because they are liberated from their co‐evolved predators, pathogens and herbivores. The biotic resistance hypothesis asserts that introduced species often fail to invade communities because strong biotic interactions with native species hinder their establishment and spread. We reviewed the evidence for both of these hypotheses as they relate to the importance of non‐domesticated herbivores in affecting the success or failure of plant invasion.
To evaluate the natural enemies hypothesis, one must determine how commonly native herbivores have population‐level impacts on native plants. If native herbivores seldom limit native plant abundance, then there is little reason to think that introduced plants benefit from escape from these enemies. Studies of native herbivore‐native plant interactions reveal that plant life‐history greatly mediates the strength with which specialist herbivores suppress plant abundance. Relatively short‐lived plants that rely on current seed production for regeneration are most vulnerable to herbivory that reduces seed production. As such, these plants may gain the greatest advantage from escaping their specialist enemies in recipient communities. In contrast, native plants that are long lived or that possess long‐lived seedbanks may not be kept “in check” by native herbivores. For these species, escape from native enemies may have little to do with their success as exotics; they are abundant both where they are native and introduced.
Evidence for native herbivores providing biotic resistance to invasion by exotics is conflicting. Our review reveals that: 1) introduced plants can attract a diverse assemblage of native herbivores and that 2) native herbivores can reduce introduced plant growth, seed set and survival. However, the generality of these impacts is unclear, and evidence that herbivory actually limits or reduces introduced plant spread is scarce. The degree to which native herbivores provide biotic resistance to either exotic plant establishment or spread may be greatly determined by their functional and numerical responses to exotic plants, which we know little about. Generalist herbivores, through their direct effects on seed dispersal and their indirect effects in altering the outcome of native–non‐native plant competitive interactions, may have more of a facilitative than negative effect on exotic plant abundance.     

Volatile terpenes – mediators of plant-to-plant communication

Plants interact with other organisms employing volatile organic compounds (VOCs). The largest group of plant-released VOCs are terpenes, comprised of isoprene, monoterpenes, and sesquiterpenes. Mono- and sesquiterpenes are well-known communication compounds in plant–insect interactions, whereas the smallest, most commonly emitted terpene, isoprene, is rather assigned a function in combating abiotic stresses. Recently, it has become evident that different volatile terpenes also act as plant-to-plant signaling cues. Upon being perceived, specific volatile terpenes can sensitize distinct signaling pathways in receiver plant cells, which in turn trigger plant innate immune responses. This vastly extends the range of action of volatile terpenes, which not only protect plants from various biotic and abiotic stresses, but also convey information about environmental constraints within and between plants. As a result, plant–insect and plant–pathogen interactions, which are believed to influence each other through phytohormone crosstalk, are likely equally sensitive to reciprocal regulation via volatile terpene cues. Here, we review the current knowledge of terpenes as volatile semiochemicals and discuss why and how volatile terpenes make good signaling cues. We discuss how volatile terpenes may be perceived by plants, what are possible downstream signaling events in receiver plants, and how responses to different terpene cues might interact to orchestrate the net plant response to multiple stresses. Finally, we discuss how the signal can be further transmitted to the community level leading to a mutually beneficial community-scale response or distinct signaling with near kin.     

Plant metabolomics for plant chemical responses to belowground community change by climate change

General circulation models on global climate change predict increase in surface air temperature and changes in precipitation. Increases in air temperature (thus soil temperature) and altered precipitation are known to affect the species composition and function of soil microbial communities. Plant roots interact with diverse soil organisms such as bacteria, protozoa, fungi, nematodes, annelids and insects. Soil organisms show diverse interactions with plants (eg. competition, mutualism and parasitism) that may alter plant metabolism. Besides plant roots, various soil microbes such as bacteria and fungi can produce volatile organic compounds (VOCs), which can serve as infochemicals among soil organisms and plant roots. While the effects of climate change are likely to alter both soil communities and plant metabolism, it is equally probable that these changes will have cascading consequnces for grazers and subsequent food web components aboveground. Advances in plant metabolomics have made it possibile to track changes in plant metabolomes as they respond to biotic and abiotic environmental changes. Recent developments in analytical instrumentation and bioinformatics software have established metabolomics as an important research tool for studying ecological interactions between plants and other organisms. In this review, we will first summarize recent progress in plant metabolomics methodology and subsequently review recent studies of interactions between plants and soil organisms in relation to climate change issues.     

Temporal variation in plant-soil feedback controls succession

Soil abiotic and biotic factors play key roles in plant community dynamics. However, little is known about how soil biota influence vegetation changes over time. Here, we show that the effects of soil organisms may depend on both the successional development of ecosystems and on the successional position of the plants involved. In model systems of plants and soils from different successional stages, we observed negative plant–soil feedback for early-successional plant species, neutral feedback for mid-successional species, and positive feedback for late-successional species. The negative feedback of early-successional plants was independent of soil origin, while late-successional plants performed best in late- and worst in early-successional soil. Increased performance of the subordinate, late-successional plants resulted in enhanced plant community diversity. Observed feedback effects were more related to soil biota than to abiotic conditions. Our results show that temporal variations in plant–soil interactions profoundly contribute to plant community assemblage and ecosystem development.     

Indirect plant-mediated interactions among parasitoid larvae

Communities are riddled with indirect species interactions and these interactions can be modified by organisms that are parasitic or symbiotic with one of the indirectly interacting species. By inducing plant responses, herbivores are well known to alter the plant quality for subsequent feeders. The reduced performance of herbivores on induced plants cascades into effects on the performance of higher trophic level organisms such as parasitoids that develop inside herbivores. Parasitoids themselves may also, indirectly, interact with the host plant by affecting the behaviour and physiology of their herbivorous host. Here, we show that, through their herbivorous host, larvae of two parasitoid species differentially affect plant phenotypes leading to asymmetric interactions among parasitoid larvae developing in different hosts that feed on the same plant. Our results show that temporally separated parasitoid larvae are involved in indirect plant-mediated interactions by a network of trophic and non-trophic relationships.     

Florivores decrease pollinator visitation in a self-incompatible plant

Different biotic interactions may influence one another to produce complex patterns of direct and indirect effects, which together influence plant reproductive success. However, so far most studies on plant-animal interactions have focused on single interactions in isolation. In this study, we studied the effect of florivory by the weevil Cionus nigritarsis on pollinator visitation rate in the self-incompatible perennial herb Verbascum nigrum by combining observations of florivory and pollination in natural populations with records of pollinator visitation to plants with different levels of experimentally inflicted damage.Increasing levels of damage through either natural or simulated florivory resulted in fewer pollinator visits per plant and per flower. As expected, the magnitude of the indirect effect of florivory on pollinator visitation was proportional to the intensity of florivory. Our results indicate that biotic non-pollinating agents, such as florivores, may induce substantial changes in pollinator availability. Therefore, studies addressing different plant-animal interactions in parallel are necessary to better comprehend the factors influencing the reproductive performance and demography of flowering plants.     

Disease Interactions in a Shared Host Plant: Effects of Pre-Existing Viral Infection on Cucurbit Plant Defense Responses and Resistance to Bacterial Wilt Disease

Both biotic and abiotic stressors can elicit broad-spectrum plant resistance against subsequent pathogen challenges. However, we currently have little understanding of how such effects influence broader aspects of disease ecology and epidemiology in natural environments where plants interact with multiple antagonists simultaneously. In previous work, we have shown that healthy wild gourd plants (Cucurbita pepo ssp. texana) contract a fatal bacterial wilt infection (caused by Erwinia tracheiphila) at significantly higher rates than plants infected with Zucchini yellow mosaic virus (ZYMV). We recently reported evidence that this pattern is explained, at least in part, by reduced visitation of ZYMV-infected plants by the cucumber beetle vectors of E. tracheiphila. Here we examine whether ZYMV-infection may also directly elicit plant resistance to subsequent E. tracheiphila infection. In laboratory studies, we assayed the induction of key phytohormones (SA and JA) in single and mixed infections of these pathogens, as well as in response to the feeding of A. vittatum cucumber beetles on healthy and infected plants. We also tracked the incidence and progression of wilt disease symptoms in plants with prior ZYMV infections. Our results indicate that ZYMV-infection slightly delays the progression of wilt symptoms, but does not significantly reduce E. tracheiphila infection success. This observation supports the hypothesis that reduced rates of wilt disease in ZYMV-infected plants reflect reduced visitation by beetle vectors. We also documented consistently strong SA responses to ZYMV infection, but limited responses to E. tracheiphila in the absence of ZYMV, suggesting that the latter pathogen may effectively evade or suppress plant defenses, although we observed no evidence of antagonistic cross-talk between SA and JA signaling pathways. We did, however, document effects of E. tracheiphila on induced responses to herbivory that may influence host-plant quality for (and hence pathogen acquisition by) cucumber beetles.     

Disentangling how climate change can affect an aquatic food web by combining multiple experimental approaches

Predicting the biological effects of climate change presents major challenges due to the interplay of potential biotic and abiotic mechanisms. Climate change can create unexpected outcomes by altering species interactions, and uncertainty over the ability of species to develop in situ tolerance or track environmental change further hampers meaningful predictions. As multiple climatic variables shift in concert, their potential interactions further complicate ecosystem responses. Despite awareness of these complexities, we still lack controlled experiments that manipulate multiple climatic stressors, species interactions, and prior exposure of species to future climatic conditions. Particularly studies that address how changes in water availability interact with other climatic stressors to affect aquatic ecosystems are still rare. Using aquatic insect communities of Neotropical tank bromeliads, we combined controlled manipulations of drought length and species interactions with a space‐for‐time transplant (lower elevations represent future climate) and a common garden approach. Manipulating drought length and experiment elevation revealed that adverse effects of drought were amplified at the warmer location, highlighting the potential of climatic stressors to synergistically affect communities. Manipulating the presence of omnivorous tipulid larvae showed that negative interactions from tipulids, presumably from predation, arose under drought, and were stronger at the warmer location, stressing the importance of species interactions in mediating community responses to climate change. The common garden treatments revealed that prior community exposure to potential future climatic conditions did not affect the outcome. In this powerful experiment, we demonstrated how complexities arise from the interplay of biotic and abiotic mechanisms of climate change. We stress that single species can steer ecological outcomes, and suggest that focusing on such disproportionately influential species may improve attempts at making meaningful predictions of climate change impacts on food webs.     

Positive and negative biotic interactions and invasive Triadica sebifera tolerance to salinity: a cross‐continent comparative study

Exotic plant species may exhibit abiotic niche expansions that enable them to persist in a greater variety of habitat types in their introduced ranges than in their native ranges. This may reflect variation in limitation by different abiotic niche dimensions (realized niche shift) or phenotypic effects of biotic interactions that vary among ranges (realized niche expansion). Novel abiotic and biotic environments in the introduced range may also lead to genetic changes in exotic plant traits that enhance their abiotic stress tolerance (fundamental niche expansion). Here, we investigated how biotic interactions (aboveground herbivory and soil organisms) affect plant salinity tolerance using the invasive species Triadica sebifera from China (native range) and US (introduced range) populations grown in common gardens in both ranges. Simulated herbivory significantly reduced survival in saline treatments with reductions especially large at low salinity. Soil sterilization had a negative effect on survival at low salinity in China but had a positive effect on survival at low salinity in the US. Triadica survival and biomass were higher for US populations than for China populations, particularly in China but salinity tolerance did not depend on population origin. On average, arbuscular mycorrhizal (AM) colonization was higher for US populations, US soils and low salinity. These factors had a significant, positive, non‐additive interaction so that clipped seedlings from US populations in low saline US soils had high levels of AM colonization. Overall, our results show that phenotypic biotic interactions shape Triadica's salinity tolerance. Positive and negative biotic interactions together affected plant performance at intermediate stress levels. However, only aboveground damage consistently affected salinity tolerance, suggesting an important role for enemy release in expanding stress tolerance.     

Relative importance of competition and plant–soil feedback,their synergy,context dependency and implications for coexistence

Plants interact simultaneously with each other and with soil biota, yet the relative importance of competition vs. plant–soil feedback (PSF) on plant performance is poorly understood. Using a meta‐analysis of 38 published studies and 150 plant species, we show that effects of interspecific competition (either growing plants with a competitor or singly, or comparing inter‐ vs. intraspecific competition) and PSF (comparing home vs. away soil, live vs. sterile soil, or control vs. fungicide‐treated soil) depended on treatments but were predominantly negative, broadly comparable in magnitude, and additive or synergistic. Stronger competitors experienced more negative PSF than weaker competitors when controlling for density (inter‐ to intraspecific competition), suggesting that PSF could prevent competitive dominance and promote coexistence. When competition was measured against plants growing singly, the strength of competition overwhelmed PSF, indicating that the relative importance of PSF may depend not only on neighbour identity but also density. We evaluate how competition and PSFs might interact across resource gradients; PSF will likely strengthen competitive interactions in high resource environments and enhance facilitative interactions in low‐resource environments. Finally, we provide a framework for filling key knowledge gaps and advancing our understanding of how these biotic interactions influence community structure.     

Management of invasive plants through ecological resistance

Despite debates on the real impact of plant invasion on native biodiversity, there remain many situations where exotic invasive plants must be managed and habitats restored. Restoration practices that build on plant community assembly principles could be useful to delay or prevent re-invasion after control, but there are still few syntheses of the biodiversity theory, ecological mechanisms and experimental evidence relevant to invasive plant management, possibly delaying applications. To provide such a synthesis, we review current knowledge on three key determinants of invasion success: biotic resistance, abiotic constraints, and propagule pressure. We elaborate on the ecological mechanisms at play for each determinant and emphasize, using case studies, their relevance for invasive plant management and ecological restoration. We find evidence that restoring a plant cover can enhance invasion resistance, but the challenge for both research and field applications is to understand how multiple determinants interact in relation to species traits in the fields. Failure to recognize these interactions and their effect on community assembly processes may explain some of the mixed species responses observed. While we need control and restoration case studies with local species at different sites, the development of a coherent, dynamic and adaptive framework around biotic/ecological resistance will have to go beyond the idiosyncrasy of the many species and systems being tested. Emphasizing the functional diversity of the restored community seems a promising approach when facing potentially multiple invaders and/or fluctuating abiotic conditions.     

Contrasting effects of plant population size on florivory and pollination

Changes in plant population size, induced by various forms of habitat degradation, can affect the performance of plants by altering their interactions with other organisms such as pollinators and herbivores. However, studies on plant reproductive response to variation in population size that simultaneously consider different interactions are rare. In this study, we examined (1) how levels of pollinator visitation and florivory vary with population size of a self-incompatible herb, Verbascum nigrum (Scrophulariaceae), (2) the relative effect of these two interactions on host seed set, and (3) whether the intensity of florivory influences pollinator visitation rate. The intensity of florivory increased, whereas pollinator visitation rate decreased with host population size. Although average seed production was negatively affected by the intensity of florivory, seed production was independent of population size. The direct negative effect of florivores on plant seed set was indirectly enforced by their negative effect on pollinator visitation rate. Our results emphasize the complexity of responses of different plant–animal interactions to plant population size. However, interactions involving specialized organisms are likely to disrupt first as plant population size decreases.     

Coevolutionary Constraints? The Environment Alters Tripartite Interaction Traits in a Legume

Third party species, which interact with one or both partners of a pairwise species interaction, can shift the ecological costs and the evolutionary trajectory of the focal interaction. Shared genes that mediate a host's interactions with multiple partners have the potential to generate evolutionary constraints, making multi-player interactions critical to our understanding of the evolution of key interaction traits. Using a field quantitative genetics approach, we studied phenotypic and genetic correlations among legume traits for rhizobium and herbivore interactions in two light environments. Shifts in plant biomass allocation mediated negative phenotypic correlations between symbiotic nodule number and herbivory in the field, whereas positive genetic covariances suggested shared genetic pathways between nodulation and herbivory response. Trait variance-covariance (G) matrices were not equal in sun and shade, but nevertheless responses to independent and correlated selection are expected to be similar in both environments. Interactions between plants and aboveground antagonists might alter the evolutionary potential of traits mediating belowground mutualisms (and vice versa). Thus our understanding of legume-rhizobium genetics and coevolution may be incomplete without a grasp of how these networks overlap with other plant interactions.     

Climate change and invasion by intracontinental range-expanding exotic plants: the role of biotic interactions

Background and Aims

In this Botanical Briefing we describe how the interactions between plants and their biotic environment can change during range-expansion within a continent and how this may influence plant invasiveness.

Scope

We address how mechanisms explaining intercontinental plant invasions by exotics (such as release from enemies) may also apply to climate-warming-induced range-expanding exotics within the same continent. We focus on above-ground and below-ground interactions of plants, enemies and symbionts, on plant defences, and on nutrient cycling.

Conclusions

Range-expansion by plants may result in above-ground and below-ground enemy release. This enemy release can be due to the higher dispersal capacity of plants than of natural enemies. Moreover, lower-latitudinal plants can have higher defence levels than plants from temperate regions, making them better defended against herbivory. In a world that contains fewer enemies, exotic plants will experience less selection pressure to maintain high levels of defensive secondary metabolites. Range-expanders potentially affect ecosystem processes, such as nutrient cycling. These features are quite comparable with what is known of intercontinental invasive exotic plants. However, intracontinental range-expanding plants will have ongoing gene-flow between the newly established populations and the populations in the native range. This is a major difference from intercontinental invasive exotic plants, which become more severely disconnected from their source populations.     

Mycorrhizal-induced growth depression in plants

As plant mutualists, one would not expect arbuscular mycorrhizal fungi (AMF) to cause growth depression of their host plants. The mechanism responsible for negative effects of AMF is still debated and so here we review the possible abiotic and biotic reasons for AMF-induced growth depression in plants: 1) The Phytocentric explanations, include: a) AMF and non-mycotrophic plants, b) different growth stages of plants. 2) The Mycocentric explanations, include: a) Low effective AMF species, b) The existence of vesicles, c) Genetic variability of AMF, and d) Geographic origin of AMF. 3) Unbalanced C-for-nutrient-trade, involving both partners and 4) Indirect effects of other organisms. We note deficiencies in previous studies and suggest improvements in experimental designs such as the use of realistic mixtures of AM fungal species, and growing plants in mixtures in field situations, rather than single pot studies, with and without fungi. Determining whether and how AM fungi cheat on their hosts will enable a better understanding of their roles in natural communities and their use as biofertilizers in agriculture.     

Chemical interaction between undamaged plants--effects on herbivores and natural enemies

Most research on plant-plant chemical interactions has focussed on events following herbivore or pathogen attack. However, undamaged plants also interact chemically as a natural facet of their behaviour, and this may have consequences for insects that use the plants as hosts. In this review, the links between allelopathy and insect behaviour are outlined. Findings on how chemical interactions between different plant species and genotypes affect aphid herbivores and their natural enemies are reviewed, and the role of plant diversity and chemical interaction for trophic interactions in crops is discussed.     

Experimental manipulation of biotic and abiotic parameters changes the outcome of insect-plant interactions

Plants usually respond to environmental shifts with morpho-physiological adjustments, which trickles down to biotic interactions in the insect-plant system. We evaluate how Copaifera langsdorffii, a widespread tree species adapted to multiple ecosystems, responds to shifts in nutrient and water availability through experimental supplementation and how it affects its insect communities. We also evaluate how the presence of extrafloral nectaries (EFN) exudates modifies galling insect diversity and herbivory rates. Such experimental approach is scarce, as we simultaneously evaluate biotic and abiotic factors and cover the entire reproductive cycle of a species in natural environments, bringing important contributions to better understand how bottom-up factors drive species interactions and possibly community assembly. The experiment was set in an ironstone outcrop vegetation, where we deployed supplementation treatments in 80 plant individuals divided into the following field treatments: (T1 = Fertilizer, T2 = EFN simulation (Eppendorf tubes with a 20% sugar solution), T3 = fertilizer + EFN simulation, T4 = water spray, T5 = EFN control (microtube with water), and T6 = Control. We observed lower sclerophylly and greater leaf area in plant individuals that were supplemented with nutrients and water. Herbivory rates were lower and ant abundance was higher in plants with artificial EFNs available. While we did not observe variations in richness and abundance of galling insects, the patterns of co-occurrence of galls varied with the availability of resources (nesting space) in the plant. This study illustrates how variations in nutrient availability to plants modify interactions with insect communities. Ant-plant interactions can have a negative impact on general herbivory rates, however ants seem to have a more harmonious relationship with the galling insects.