Responses of soil biota and nitrogen availability to an invasive plant under aboveground herbivory

Plant and Soil - Recently, much attention has been paid to the plant-mediated effects of aboveground herbivory on soil ecosystems. However, studies about the herbivore-induced effects of invasive...     

Sequential effects of root and foliar herbivory on aboveground and belowground induced plant defense responses and insect performance

Plants are often simultaneously or sequentially attacked by multiple herbivores and changes in host plants induced by one herbivore can influence the performance of other herbivores. We examined how sequential feeding on the plant Plantago lanceolata by the aboveground herbivore Spodoptera exigua and the belowground herbivore Agriotes lineatus influences plant defense and the performance of both insects. Belowground herbivory caused a reduction in the food consumption by the aboveground herbivore independent of whether it was initiated before, at the same time, or after that of the aboveground herbivore. By contrast, aboveground herbivory did not significantly affect belowground herbivore performance, but significantly reduced the performance of later arriving aboveground conspecifics. Interestingly, belowground herbivores negated negative effects of aboveground herbivores on consumption efficiency of their later arriving conspecifics, but only if the belowground herbivores were introduced simultaneously with the early arriving aboveground herbivores. Aboveground–belowground interactions could only partly be explained by induced changes in an important class of defense compounds, iridoid glycosides (IGs). Belowground herbivory caused a reduction in IGs in roots without affecting shoot levels, while aboveground herbivory increased IG levels in roots in the short term (4 days) but only in the shoots in the longer term (17 days). We conclude that the sequence of aboveground and belowground herbivory is important in interactions between aboveground and belowground herbivores and that knowledge on the timing of exposure is essential to predict outcomes of aboveground–belowground interactions.     

Plant responses to variable timing of aboveground clipping and belowground herbivory depend on plant age

Aims Plants use different types of responses such as tolerance and induced defense to mitigate the effects of herbivores. The direction and magnitude of both these plant responses can vary with plant age. However, most studies have focused on aboveground herbivory, whereas important feeding occurs belowground. Here, we tested the hypothesis that plant tolerance and defense following shoot damage or root herbivory depends on plant age.     

Effects of aboveground herbivory on plants with long-term belowground biomass storage

Plant tolerance to herbivory is contingent on multiple traits and adaptive mechanisms, which makes it a complex response with ecological implications. In plants with long-term belowground storage, allocation of biomass to inaccessible parts belowground in response to folivory is a well-recognized tolerance mechanism. In temperate regions, spring growth from buried rootstock is common among winter deciduous plants and is often followed by regrowth after defoliation, both of which draws resources from the stored reserves. We developed a mathematical model to analyze this tolerance response in a winter deciduous plant with long-term belowground biomass when it is defoliated by a specialist insect folivore. The model explores how three closely associated traits—(1) belowground biomass allocation to roots, (2) spring utilization of stored reserves, and (3) post-defoliation regrowth capacity—modulate the persistence and dynamics of the plant and herbivore populations. Model results show that allocation to belowground storage is not only a critical component of tolerance but also influences the herbivore population dynamics in ways that depend on how and when plant biomass is allocated and used. Low belowground biomass allocation and high storage utilization combined with poor photosynthetic growth caused extirpation of the plant population by the defoliating insects. Stable coexistence of the plant at low biomass along with its specialist insect required a moderate amount of post-herbivory belowground allocation. High values of belowground biomass allocation, storage utilization, and photosynthetic growth resulted in sustained cycles of the herbivore and plant populations. Interestingly, utilization of stored reserves had conflicting influence on above and belowground biomass, and strongly affected herbivore population dynamics. Our model thus highlights the complexity of tolerance response when it involves multiple traits and mechanisms as evinced by winter deciduous plants. We close by discussing the implications of our findings for the contributions of defoliating insects to biocontrol programs.     

Herbivore effects on above- and belowground plant production and soil nitrogen availability in the Trans-Himalayan shrub-steppes

Large mammalian herbivores may have positive, neutral, or negative effects on annual net aboveground plant production (NAP) in different ecosystems, depending on their indirect effects on availability of key nutrients such as soil N. In comparison, less is known about the corresponding influence of grazers, and nutrient dynamics, over annual net belowground plant production (NBP). In natural multi-species plant communities, it remains uncertain how grazing influences relative allocation in the above- and belowground compartments in relation to its effects on plant nutrients. We evaluated grazer impacts on NAP, NBP, and relative investment in the above- and belowground compartments, alongside their indirect effects on soil N availability in the multiple-use Trans-Himalayan grazing ecosystem with native grazers and livestock. Data show that a prevailing grazing intensity of 51% increases NAP (+61%), but reduces NBP (−35%). Grazing also reduced C:N ratio in shoots (−16%) and litter (−50%), but not in roots, and these changes coincided with increased plant-available inorganic soil N (+23%). Areas used by livestock and native grazers showed qualitatively similar responses since NAP was promoted, and NBP was reduced, in both cases. The preferential investment in the aboveground fraction, at the expense of the belowground fraction, was correlated positively with grazing intensity and with improvement in litter quality. These results are consistent with hypothesized herbivore-mediated positive feedbacks between soil nutrients and relative investment in above- and belowground compartments. Since potentially overlapping mechanisms, such as N mineralization rate, plant N uptake, compositional turnover, and soil microbial activity, may contribute towards these feedbacks, further studies may be able to discern their respective contributions.     

Indirect effects of deer herbivory on local nitrogen availability in a coastal dune ecosystem

Herbivores can have indirect effects on local nutrient availability if their direct effects on plants lead to changes in the amount or chemical composition of litter reaching the soil surface. Using two exclosure experiments, we evaluated this possibility for black-tailed deer ( Odocoileus hemionus columbianus ) feeding on silver bush lupine ( Lupinus chamissonis ) in a coastal dune system in northern California. Our first experiment assessed the effects of deer herbivory on 360 lupines that were tracked from newly germinated seedlings in 1996 and 1997 until 2000, when most surviving individuals had reached reproductive age. Results from this experiment showed that browsing by deer significantly reduced growth rates and seed production of lupines and delayed the onset of reproductive maturity. Although deer had no effect on the density of litter accumulating underneath shrubs (g m⁻²), browsing significantly decreased C:N ratios of leaf tissue, due primarily to increased nitrogen content of leaves. Deer browsing also caused significantly increased net nitrogen mineralization rates in the soil under shrubs, although pools of ammonium and nitrate were uninfluenced. The second experiment examined 72 established bush lupines from 1997 to 2000, and showed that deer browsing significantly decreased seed production but had no effect on shrub growth. We also detected trends for browsed shrubs to have reduced pools of ammonium and nitrate underneath their canopies, although no such patterns emerged for nitrogen mineralization rates. Collectively, these data suggest that changes in litter quality, more so than litter quantity, contributed to the indirect effects of deer herbivory on local nitrogen dynamics. We hypothesize that deer browsing induced chemical changes in lupine plant tissue, which increased the nitrogen content of litter reaching the soil surface and subsequently increased rates of nitrogen mineralization.     

Emerging role of roots in plant responses to aboveground insect herbivory

Plants have evolved complex biochemical mechanisms to counter threats from insect herbivory. Recent research has revealed an important role of roots in plant responses to above ground herbivory (AGH). The involvement of roots is integral to plant resistance and tolerance mechanisms. Roots not only play an active role in plant defenses by acting as sites for biosynthesis of various toxins and but also contribute to tolerance by storing photoassimilates to enable future regrowth. The interaction of roots with beneficial soil‐borne microorganisms also influences the outcome of the interaction between plant and insect herbivores. Shoot‐to‐root communication signals are critical for plant response to AGH. A better understanding of the role of roots in plant response to AGH is essential in order to develop a comprehensive picture of plant‐insect interactions. Here, we summarize the current status of research on the role of roots in plant response to AGH and also discuss possible signals involved in shoot‐to‐root communication.     

Palatability, decomposition and insect herbivory: patterns in a successional old-field plant community

We tested the hypothesis that selective feeding by insect herbivores in an old‐field plant community induces a shift of community structure towards less palatable plant species with lower leaf and litter tissue quality and may therefore affect nutrient cycling. Leaf palatability of 20 herbaceous plant species which are common during the early successional stages of an old‐field plant community was assayed using the generalist herbivores Deroceras reticulatum (Mollusca: Agriolomacidae) and Acheta domesticus (Ensifera: Gryllidae). Palatability was positively correlated with nitrogen content, specific leaf area and water content of leaves and negatively correlated with leaf carbon content and leaf C/N‐ratio. Specific decomposition rates were assessed in a litter bag experiment. Decomposition was positively correlated with nitrogen content of litter, specific leaf area and water content of living leaves and negatively correlated with leaf C/N‐ratio. When using phylogentically independent contrasts the correlations between palatability and decomposition versus leaf and litter traits remained significant (except for specific leaf area) and may therefore reflect functional relationships. As palatability and decomposition show similar correlations to leaf and litter traits, the correlation between leaf palatability and litter decomposition rate was also significant, and this held even in a phylogenetically controlled analysis. This correlation highlights the possible effects of invertebrate herbivory on resource dynamics. In a two‐year experiment we reduced the density of above‐ground and below‐ground insect herbivores in an early successional old‐field community in a two‐factorial design by insecticide application. The palatability ranking of plants showed no relationship with the specific change of cover abundance of plants due to the reduction of above‐ or below‐ground herbivory. Thus, changes in the dominance structure as well as potentially associated changes in the resource dynamics are not the result of differences in palatability between plant species. This highlights fundamental differences between the effects of insect herbivory on ecosystems and published results from vertebrate‐grazing systems.     

Separate effects of human visitation and touch on plant growth and herbivory in an old-field community

Although animal scientists have long been aware that methods used to measure an experimental system can affect the subject of measurement, similar confounding effects of commonly used field methods have only recently been acknowledged by plant ecologists. Here we demonstrate significant effects of weekly visitation (walking up to a focal plant) and handling (taking morphological measures) on plant growth and herbivory in an old-field community. Of the three species examined, Apocynum cannabinum was the most severely affected by our treatments. For Apocynum, weekly visitations resulted in a positive relationship between initial and final size, which did not occur in the unvisited plants. Visitation also increased leaf herbivory, resulting in a reduced leaf:stem biomass ratio. Handling the plants nearly doubled the proportion of individuals with a stem borer emergence hole. Growth of the other species in this study, Potentilla recta and Erigeron philadelphicus, was altered by either visitation or visitation plus handling. Visiting plants in order to observe them and touching them as one would when making morphological measurements can have important biological consequences. We suggest that plant ecologists treat repeated entry into a natural system as a research method, subject to the same scrutiny and justification as all other experimental methods.     

Sources of variation in plant responses to belowground insect herbivory: a meta-analysis

Growing interest in belowground herbivory and the remarkable diversity of the accumulated information on this topic inspired us to quantitatively explore the variation in the outcomes of individual studies. We conducted a meta-analysis of 85 experimental studies reporting the effects of root-feeding insect herbivores (36 species) on plants (75 species). On average, belowground herbivory led to a 36.3% loss of root biomass, which was accompanied by a reduction in aboveground growth (-16.3%), photosynthesis (-11.7%) and reproduction (-15.5%). The effects of root herbivory on aboveground plant characteristics were significant in agricultural and biological control studies, but not in studies of natural systems. Experiments conducted in controlled environments yielded larger effects on plants than field experiments, and infestation experiments resulted in more severe effects than removal studies employing natural levels of herbivory. Simulated root herbivory led to greater aboveground growth reductions than similar root loss imposed by insect feeding. External root chewers caused stronger detrimental effects than sap feeders or root borers; specialist herbivores imposed milder adverse effects on plants than generalists. Woody plants suffered from root herbivory more than herbaceous plants, although root loss was similar in these two groups. Evergreen woody plants responded to root herbivory more strongly than deciduous woody plants, and grasses suffered from root herbivory more than herbs. Environmental factors such as drought, poor nutrient supply, among-plant competition, and aboveground herbivory increased the adverse effects of root damage on plants in an additive manner. In general, plant tolerance to root herbivores is lower than tolerance to defoliating aboveground herbivores.     

Positive and negative impacts of insect frass quality on soil nitrogen availability and plant growth

Frass deposition to soil is an important pathway by which herbivorous insects impact decomposition and soil nutrient availability. However, little is known about how frass quality influences ecosystem properties. Here, we examined the effects of frass quality on the decomposition process, soil nitrogen (N) availability, and plant growth, using frass of Mamestra brassicae (L.) that fed on fertilized or unfertilized Brassica rapa L. var. perviridis Bailey. The frass quality was largely dependent on the host plant quality. Frass excreted by larvae that fed on the fertilized plants had higher N than that of larvae that fed on the unfertilized plants. The decomposition rate of the frass did not differ between N-rich and N-poor frass, except during the early decomposition period. The inorganic N concentration decreased during decomposition in both frass types. However, difference in the initial inorganic N concentration led to different consequences regarding soil N availability. Furthermore, addition of frass to the soil differently influenced the growth of B. rapa plants depending on the frass quality: plant biomass was increased by N-rich frass addition but decreased by N-poor frass addition, compared to the biomass without frass addition. These results indicate that frass quality is an important factor in determining the impact of herbivorous insects on nutrient dynamics, and that frass positively or negatively influences soil N availability and plant growth, depending on its quality.     

Differential effects of two dominant plant species on community structure and invasibility in an old-field ecosystem

Aims In this study, we examined the effects of Solidago altissima (hereafter Solidago) and two species in the genus Verbesina, Verbesina virginica and Verbesina occidentalis (hereafter Verbesina), on the structure of an old-field plant community and establishment by an invasive plant species, Lespedeza cuneata (hereafter Lespedeza).Methods We removed Solidago, Verbesina and both Solidago and Verbesina from 4-m 2 plots in an intact old-field community during two growing seasons. We then quantified the effects of these removals on richness, evenness, diversity and composition of the subdominant plant community. We also measured the total aboveground biomass and the aboveground biomass of the subdominant community. To assess how these removals affected establishment by Lespedeza, we planted 20 seeds in each plot and tracked seedling emergence and survival for one growing season.Important findings Subdominant community evenness and Shannon diversity were higher in plots from which Solidago and Verbesina were removed relative to control plots. However, there were no effects of dominant species removal on species richness or composition of the subdominant community. Total aboveground biomass was not affected by dominant species removal, suggesting that the community of subdominant species exhibited compensation. In fact, subdominant community biomass was greater when Solidago, but not Verbesina, was removed. Light availability was also greater in plots where Solidago was removed relative to control plots throughout the growing season. In addition, removal of dominant species, in particular Solidago, indirectly reduced the emergence, but not survival, of Lespedeza seedlings by directly promoting subdominant community biomass. Taken together, our results suggest that dominant old-field plant species affect subdominant community structure and indirectly promote establishment by Lespedeza .     

Interactive effects of fertilization and disturbance on community structure and resource availability in an old-field plant community

Summary The interactive effects of fertilization and disturbance on plant community structure and resource availability were studied by supplying four levels of nitrogen and applying four intensities of tilling to a 30 year old field in a factorial design for 2 year. Live above-ground biomass, root biomass, and litter generally increased with nitrogen supply and decreased with disturbance. Species composition varied significantly, with annuals increasing with both nitrogen and disturbance, but with perennials unaffected by nitrogen and decreased by disturbance. Species diversity decreased with disturbance, but decreased with nitrogen only in undisturbed vegetation. Root: shoot ratios decreased with added nitrogen, leaf allocation decreased with disturbance, and flowering allocation increased. Surprisingly, stem allocation was unaffected by disturbance. This result reflected a shift from vertical stems to horizontal stems as disturbance increased. Resource measurements suggested that the vegetation responded to interactions between the treatments as well as to direct treatment effects. Variation in light penetration was reduced by fertilization in undisturbed vegetation but not in tilled plots; variability was not directly affected by disturbance. The availability of nitrogen, the limiting soil nutrient, increased with fertilization but was not significantly affected by disturbance. In contrast, the ratio of ammonium to nitrate was significantly reduced by disturbance but unaffected by supply rates, suggesting that nitrogen may have had different effects under different disturbance regimes, even though its total availability was constant. While many community responses to fertilization and disturbance conformed to those reported earlier, resource and allocation measurements indicated that their interactions are not always predictable from their separate effects.     

Plant silicon effects on insect feeding dynamics are influenced by plant nitrogen availability

Although there is growing evidence that silicon (Si)‐based plant defenses effectively reduce both the palatability and digestibility of leaves, and thus impact nutrient assimilation by insect herbivores, much less is known about how this is affected by extrinsic and intrinsic factors. For example, do herbivores exhibit compensatory feeding on poor‐quality diets with Si or are Si defenses less effective in agroecosystems where high N availability increases plant quality? To investigate the interactive effects of N and Si on insect feeding, we conducted insect performance and compensatory feeding bioassays using maize, Zea mays L. (Poaceae), and the true armyworm, Pseudeletia unipuncta Haworth (Lepidoptera: Noctuidae). In the performance assay, the addition of Si alone resulted in increased larval mortality compared with the controls, likely because early instars with poorly developed mandibles could not feed effectively. However, larvae fed on plants treated with both Si and N survived better than on plants treated with Si only, although pupal mass did not differ between treatments. In our compensatory assay, Si addition reduced maize consumption, but increased both armyworm approximate digestibility and N assimilation efficiency, suggesting that enhanced post‐ingestion feeding physiology, rather than compensatory food intake, could have accounted for the lack of Si effects on pupal weight. Overall, our results demonstrate that, similar to other chemical and mechanical defenses, the effectiveness of plant Si defense is influenced by plant nutrient status and consumer compensatory ability.     

The effects of biomass removal and N additions on microbial N transformations and biomass at different vegetation types in an old-field ecosystem in northern China

There is an increasing demand for the sustainable management of old-field communities in northern China, which have developed on abandoned cropland on formerly converted natural steppe sites, to regain forage yield, biodiversity, and soil fertility. In thus study we examined how two management options—clipping and nitrogen (N) addition—may affect net >microbial N mineralization (ammonification?+?nitrification), microbial biomass carbon (MBC), microbial biomass nitrogen (MBN), and microbial respirations (MR) in grass dominated, herb dominated, and grass-herb mixed patches in an old-field community in northern China.Topsoil (0–10 cm) net N mineralization rate was 177% and 69% higher in mixed grass and herb patches (patch B) as compared to unmixed grass (patch A) or herb (patch C) patches, respectively. Topsoil MBN was significantly different among the three patches with the highest value for soils taken from umixed grass patches. However, patches with mixed grass and herb or herb dominated patches had 12% higher microbial respiration (MR) than unmixed grass patch. Clipping and N addition had no effects on net N mineralization or MBC, but both treatments decreased MBN and MR and increased the ratio between microbial biomass C and microbial biomass N (MBC/MBN) in the growing season. Incubation of soil cores under optimal water and temperature conditions in the laboratory showed that the response of microbial N transformations in soils under different vegetation patches to experimental N addition and clipping was limited by soil water availability. Our results strongly highlight the need to further study the importance of belowground C supply as a control of microbial N cycling processes. It also suggests that during the restoration process of degenerated croplands N cycling rates are stimulated, but that the magnitude of this stimulation is modulated by plant community composition of the old-fields.     

Carbon and nitrogen cycling during old-field succession: Constraints on plant and microbial biomass

Soil C and N dynamics were studied in a sequence of old fields of increasing age to determine how these biogeochemical cycles change during secondary succession. In addition, three different late-successional forests were studied to represent possible "steady state" conditions. Surface soil samples collected from the fields and forests were analyzed for total C, H₂O-soluble C, total N, potential net N mineralization, potential net nitrification, and microbial biomass. Above-and belowground plant biomass was estimated within each of the old field sites.Temporal changes in soil organic C, total N and total plant biomass were best described by a gamma function [y =at ^b e ^ctd +f] whereas a simple exponential model [y =a(l – e^–bt ) + c] provided the best fit to changes in H₂O-soluble C, C:N ratio, microbial C, and microbial N. Potential N mineralization and nitrification linearly increased with field age; however, rates were variable among the fields. Microbial biomass was highly correlated to soil C and N pools and well correlated to the standing crop of plant biomass. In turn, plant biomass was highly correlated to pools and rates of N cycling.Patterns of C and N cycling within the old field sites were different from those in a northern hardwood forest and a xeric oak forest; however, nutrient dynamics within an oak savanna were similar to those found in a 60-yr old field. Results suggest that patterns in C and N cycling within the old-field chronosequence were predictable and highly correlated to the accrual of plant and microbial biomass.     

Top predator control of plant biodiversity and productivity in an old-field ecosystem

Abstract Predators can have strong indirect effects on plants by altering the way herbivores impact plants. Yet, many current evaluations of plant species diversity and ecosystem function ignore the effects of predators and focus directly on the plant trophic level. This report presents results of a 3‐year field experiment in a temperate old‐field ecosystem that excluded either predators, or predators and herbivores and evaluated the consequence of those manipulations on plant species diversity (richness and evenness) and plant productivity. Sustained predator and predator and herbivore exclusion resulted in lower plant species evenness and higher plant biomass production than control field plots representing the intact natural ecosystem. Predators had this diversity‐enhancing effect on plants by causing herbivores to suppress the abundance of a competitively dominant plant species that offered herbivores a refuge from predation risk.     

气候因子通过土壤微生物生物量氮促进青藏高原高寒草地地上生态系统功能

近年来, 在人类活动和气候变化的影响下, 物种多样性丧失趋势不断加剧, 对生态系统功能带来严重后果。目前, 关于生态系统功能的研究, 忽略了土壤和微生物碳氮养分循环过程对地上生态系统功能(AEF)的重要驱动作用, 而土壤碳氮要素和微生物的任何变化都有可能改变地下群落对生态系统功能的维持作用。该研究旨在探究高寒草地AEF的主要控制因子, 以及其关键要素对AEF的作用机理。2015年7-8月, 对青藏高原地区115个样点进行了草地群落和土壤属性等要素样带调查; 综合植物地上生物量, 叶片碳、氮和磷含量等参数计算AEF值, 分析地下土壤有机碳含量、全氮含量、生物量等关键要素对AEF值的影响。结合取样点年降水量和年平均气温, 深入探讨影响AEF的主要控制因子和作用机理。结果表明降水对AEF有较大影响, 而气温影响相对较低。年降水量、土壤微生物生物量碳含量和干旱指数对AEF值的相对重要性贡献较高(重要值分别为21.1%、10.9%和10.1%), 控制青藏高原高寒草地AEF值的关键是土壤因子。在气候因子对土壤养分和微生物的作用下, 土壤微生物生物量氮含量在调控高寒草地AEF值方面发挥重要作用。     

Comparing intra- and inter-specific effects on litter decomposition in an old-field ecosystem

Plant species can differ in the quantity and quality of leaf litter they produce, and many studies have examined whether plant species diversity affects leaf-litter decomposition and nutrient release. A growing number of studies have indicated that intra-specific variation within plant species can also affect key ecosystem processes. However, the relative importance of intra- versus inter-specific variation for the functioning of ecosystems remains poorly known. Here, we investigate the effects of intra-specific variation in a dominant old-field plant species, tall goldenrod (Solidago altissima), and inter-specific variation among goldenrod species on litter quality, decomposition, and nitrogen (N) release. We found that the nutrient concentration of leaf litter varied among genotypes, which translated into ～50% difference in decomposition rates. Variation among other goldenrod species in decomposition rate was more than twice that of genetic variation within S. altissima. Furthermore, by manipulating litterbags to contain 1, 3, 6, or 9 genotypes, we found that S. altissima genotype identity had much stronger effects than did genotypic diversity on leaf-litter quality, decomposition, and N release. Taken together, these results suggest that the order of ecological importance for controlling leaf-litter decomposition and N release dynamics is plant species identity?genotype identity>genotypic diversity.