Above‐ and belowground insect herbivores mediate the impact of nitrogen eutrophication on the soil food web in a grassland ecosystem

Insect herbivores are important drivers of ecosystem processes in grasslands, and can mediate the grassland's response to environmental change. For example, recent evidence shows that above‐ and belowground herbivory, individually and in combination, can modify how a plant community responds to nitrogen (N) eutrophication, an important driver of global change. However, knowledge about how such effects extend to the associated soil food web is lacking. In a mesocosm experiment, we investigated how communities of soil nematodes – an abundant and functionally important group of soil organisms – responded to above‐ and belowground insect herbivory at contrasting N levels. We found that the strongest influence of above‐ and belowground herbivory on the nematode community appeared at elevated N. The abundance of root‐feeding nematodes increased when either above‐ or belowground insect herbivores were present at elevated N, but when applied together the two herbivore types cancelled out one another's effect. Additionally, at elevated N aboveground herbivory increased the abundance of fungal‐feeders relative to bacterial‐feeders, which indicates changes in decomposition pathways induced by N and herbivory. Belowground herbivory increased the abundance of omnivorous nematodes. The shifts in both the herbivorous and detrital parts of the soil food web demonstrate that above‐ and belowground herbivory does not only mediate the response of the plant community to N eutrophication, but in extension also the soil food web sustained by the plant community. We conclude that feedbacks between effects of above‐ and belowground herbivory mediate the response of the grassland ecosystem to N eutrophication.     

The effects of insects,nutrients, and plant invasion on community structure and function above‐ and belowground

Soil nutrient availability, invasive plants, and insect presence can directly alter ecosystem structure and function, but less is known about how these factors may interact. In this 6‐year study in an old‐field ecosystem, we manipulated insect abundance (reduced and control), the propagule pressure of an invasive nitrogen‐fixing plant (propagules added and control), and soil nutrient availability (nitrogen added, nitrogen reduced and control) in a fully crossed, completely randomized plot design. We found that nutrient amendment and, occasionally, insect abundance interacted with the propagule pressure of an invasive plant to alter above‐ and belowground structure and function at our site. Not surprisingly, nutrient amendment had a direct effect on aboveground biomass and soil nutrient mineralization. The introduction of invasive nitrogen‐fixing plant propagules interacted with nutrient amendment and insect presence to alter soil bacterial abundance and the activity of the microbial community. While the larger‐scale, longer‐term bulk measurements such as biomass production and nutrient mineralization responded to the direct effects of our treatments, the shorter‐term and dynamic microbial communities tended to respond to interactions among our treatments. Our results indicate that soil nutrients, invasive plants, and insect herbivores determine both above‐ and belowground responses, but whether such effects are independent versus interdependent varies with scale.     

Responses of Plant Community Composition and Biomass Production to Warming and Nitrogen Deposition in a Temperate Meadow Ecosystem

Climate change has profound influences on plant community composition and ecosystem functions. However, its effects on plant community composition and biomass production are not well understood. A four-year field experiment was conducted to examine the effects of warming, nitrogen (N) addition, and their interactions on plant community composition and biomass production in a temperate meadow ecosystem in northeast China. Experimental warming had no significant effect on plant species richness, evenness, and diversity, while N addition highly reduced the species richness and diversity. Warming tended to reduce the importance value of graminoid species but increased the value of forbs, while N addition had the opposite effect. Warming tended to increase the belowground biomass, but had an opposite tendency to decrease the aboveground biomass. The influences of warming on aboveground production were dependent upon precipitation. Experimental warming had little effect on aboveground biomass in the years with higher precipitation, but significantly suppressed aboveground biomass in dry years. Our results suggest that warming had indirect effects on plant production via its effect on the water availability. Nitrogen addition significantly increased above- and below-ground production, suggesting that N is one of the most important limiting factors determining plant productivity in the studied meadow steppe. Significant interactive effects of warming plus N addition on belowground biomass were also detected. Our observations revealed that environmental changes (warming and N deposition) play significant roles in regulating plant community composition and biomass production in temperate meadow steppe ecosystem in northeast China.     

Putting the ‘upstairs–downstairs’ into ecosystem service: What can aboveground–belowground ecology tell us?

Interactions between spatially-separated aboveground and belowground biota exert important influences on the functioning of terrestrial ecosystems. Plant root exudates and litter inputs affect root-associated and decomposer sub-communities, which, in turn, regulate nutrient availability and plant growth. Ecosystem services theoretically attributed to specific functional components of aboveground or belowground biota are, therefore, influenced by indirect (plant-mediated) interactions with the wider community. Some recent studies have considered aboveground–belowground interactions in a climate change context, with implications for altered ecosystem service provision. This review is a conceptual discussion of the mechanisms by which aboveground–belowground interactions affect specific ecosystem services: control of herbivores by natural enemies, insect pollination and nutrient mineralization by soil decomposers. While some mechanisms are well-characterized, others are poorly understood. Reducing root and shoot herbivory, in addition to the direct plant benefit, indirectly promotes antagonism of the spatially-separate herbivore by its natural enemies. Soil decomposers and mycorrhizal fungi can increase shoot herbivore performance such that control by natural enemies is weakened, or initiate bottom-up trophic cascades which strengthen antagonism of shoot herbivores. Aboveground herbivory generally stimulates nutrient cycling by decomposers. Root herbivory and mycorrhizal association both appear to increase floral attractiveness to insect pollinators. Mechanisms reflect alterations to plant growth, nutritional quality and chemical defenses. Climate change has considerable potential to alter aboveground–belowground interactions, with largely unexplored implications for biological control, pollination and soil nutrient cycling.     

Above- and belowground responses to nitrogen addition in a Chihuahuan Desert grassland

Increased available soil nitrogen can increase biomass, lower species richness, alter soil chemistry and modify community structure in herbaceous ecosystems worldwide. Although increased nitrogen availability typically increases aboveground production and decreases species richness in mesic systems, the impacts of nitrogen additions on semiarid ecosystems remain unclear. To determine how a semiarid grassland responds to increased nitrogen availability, we examined plant community structure and above- and belowground net primary production in response to long-term nitrogen addition in a desert grassland in central New Mexico, USA. Plots were fertilized annually (10 g N m⁻²) since 1995 and NPP measured from 2004 to 2009. Differences in aboveground NPP between fertilized and control treatments occurred in 2004 following a prescribed fire and in 2006 when precipitation was double the long-term average during the summer monsoon. Presumably, nitrogen only became limiting once drought stress was alleviated. Belowground NPP was also related to precipitation, and greatest root growth occurred the year following the wettest summer, decreasing gradually thereafter. Belowground production was unrelated to aboveground production within years and unrelated to nitrogen enrichment. Species richness changed between years in response to seasonal precipitation variability, but was not altered by nitrogen addition. Community structure did respond to nitrogen fertilization primarily through increased abundance of two dominant perennial grasses. These results were contrary to most nitrogen addition studies that find increased biomass and decreased species richness with nitrogen fertilization. Therefore, factors other than nitrogen deposition, such as fire or drought, may play a stronger role in shaping semiarid grassland communities than soil fertility.     

短期氮素添加和模拟放牧对青藏高原高寒草甸生态系统呼吸的影响

氮沉降和放牧是影响草地碳循环过程的重要环境因子,但很少有研究探讨这些因子交互作用对生态系统呼吸的影响。在西藏高原高寒草甸地区开展了外源氮素添加与刈割模拟放牧实验,测定了其对植物生物量分配、土壤微生物碳氮和生态系统呼吸的影响。结果表明:氮素添加显著促进生态系统呼吸,而模拟放牧对其无显著影响,且降低了氮素添加的刺激作用。氮素添加通过提高微生物氮含量和土壤微生物代谢活性,促进植物地上生产,从而增加生态系统的碳排放;而模拟放牧降低了微生物碳含量,且降低了氮素添加的作用,促进根系的补偿性生长,降低了氮素添加对生态系统碳排放的刺激作用。这表明,放牧压力的存在会抑制氮沉降对高寒草甸生态系统碳排放的促进作用,同时外源氮输入也会缓解放牧压力对高寒草甸生态系统生产的负面影响。     

Legacy effects of aboveground-belowground interactions

Root herbivory can greatly affect the performance of aboveground insects via changes in plant chemistry. These interactions have been studied extensively in experiments where aboveground and belowground insects were feeding on the same plant. However, little is known about how aboveground and belowground organisms interact when they feed on plant individuals that grow after each other in the same soil. We show that feeding by aboveground and belowground insect herbivores on ragwort (Jacobaea vulgaris) plants exert unique soil legacy effects, via herbivore-induced changes in the composition of soil fungi. These changes in the soil biota induced by aboveground and belowground herbivores of preceding plants greatly influenced the pyrrolizidine alkaloid content, biomass and aboveground multitrophic interactions of succeeding plants. We conclude that plant-mediated interactions between aboveground and belowground insects are also important when they do not feed simultaneously on the same plant.     

Above- and belowground insect herbivores differentially affect soil nematode communities in species-rich plant communities

Interactions between above‐ and belowground invertebrate herbivores alter plant diversity, however, little is known on how these effects may influence higher trophic level organisms belowground. Here we explore whether above‐ and belowground invertebrate herbivores which alter plant community diversity and biomass, in turn affect soil nematode communities. We test the hypotheses that insect herbivores 1) alter soil nematode diversity, 2) stimulate bacterial‐feeding and 3) reduce plant‐feeding nematode abundances. In a full factorial outdoor mesocosm experiment we introduced grasshoppers (aboveground herbivores), wireworms (belowground herbivores) and a diverse soil nematode community to species‐rich model plant communities. After two years, insect herbivore effects on nematode diversity and on abundance of herbivorous, bacterivorous, fungivorous and omni‐carnivorous nematodes were evaluated in relation to plant community composition. Wireworms did not affect nematode diversity despite enhanced plant diversity, while grasshoppers, which did not affect plant diversity, reduced nematode diversity. Although grasshoppers and wireworms caused contrasting shifts in plant species dominance, they did not affect abundances of decomposer nematodes at any trophic level. Primary consumer nematodes were, however, strongly promoted by wireworms, while community root biomass was not altered by the insect herbivores. Overall, interaction effects of wireworms and grasshoppers on the soil nematodes were not observed, and we found no support for bottom‐up control of the nematodes. However, our results show that above‐ and belowground insect herbivores may facilitate root‐feeding rather than decomposer nematodes and that this facilitation appears to be driven by shifts in plant species composition. Moreover, the addition of nematodes strongly suppressed shoot biomass of several forb species and reduced grasshopper abundance. Thus, our results suggest that nematode feedback effects on plant community composition, due to plant and herbivore parasitism, may strongly depend on the presence of insect herbivores.     

Insect herbivore effects on resource allocation to shoots and roots in <Emphasis Type="Italic">Lespedeza capitata</Emphasis>

Aboveground and belowground processes in plants are intimately linked because the resources that must be divided among growth, maintenance, and development of essential structures are finite. To determine how aboveground insect herbivory affects root-system size, morphology, interactions with soil biota, and temporal patterns in the development of root systems, we grew the legume Lespedeza capitata in sunken pots in a restored prairie in south-central Kansas. The plants were manipulated in a factorial experiment that involved reduction of natural herbivory with insecticide and age of plant at harvest (2, 4, or 6 months). Herbivory reduced the aboveground sizes of plants throughout the growing season but did not affect their belowground size or root-system branching ratio. Further, the failure of aboveground insect herbivory to affect density of nitrogen-fixing nodules on L. capitata roots suggests that plants did not shift allocation of carbon to compensate for naturally occurring levels of folivory. We suggest that conservation of root-system structure or low rates of change in root-system structure in response to aboveground insect herbivory may be an adaptive strategy in environments with scarce soil resources, for example near species’ xeric range limits.     

Granivory reduces biomass and lignin concentrations of plant tissue during grassland assembly

Small mammals can influence grassland assembly by selecting against palatable plants – the community can become dominated by the plants they avoid. This predation-based selection could have indirect effects on community biomass and tissue quality, especially given how untasty plants may have higher concentrations of recalcitrant carbon compounds including lignin. We tested small mammal effects on biomass and tissue quality of roots and shoots in a two-year-old 18 ha restored tallgrass prairie with established zones of high and low plant predation. We focused on the three dominant herbaceous functional groups of tallgrass prairie (perennial forbs, C₃ and C₄ grasses), and targeted the early stages of assembly given that plant predation by small animals can unfold quickly and is difficult to subsequently quantify. We predicted rodent predation to create communities with reduced biomass but an increased abundance of lignin-rich plants; we only observed the former. Rodents reduced aboveground biomass by 46% but preferentially targeted lignin-rich plants, with the latter result explained by the predominance of granivory over herbivory – there was no opportunity for selection based on tissue palatability. Based strictly on aboveground biomass, we estimated small mammals reduced standing stocks of recalcitrant carbon by 65 kg ha⁻¹, with reductions in belowground stocks almost certainly higher given that root:shoot ratios averaged 21:1. Given that the quantity and quality of plant production can affect ecosystem functions including decomposition and the regulation of soil carbon stocks, our work suggests that non-random plant predation may substantially affect rates of soil carbon accumulation in the early stages of grassland development.     

青藏高原高寒草甸植物群落生物量对氮、磷添加的响应

青藏高原正经历着明显的温暖化过程, 由此引起的土壤温度的升高促进了土壤中微生物的活性, 同时青藏高原东缘地区大气氮沉降十分明显, 并呈逐年增加的趋势, 这些环境变化均促使土壤中可利用营养元素增加, 因此深入了解青藏高原高寒草甸植物生物量对可利用营养元素增加的响应, 是准确预测未来全球变化背景下青藏高原高寒草甸碳循环过程的重要基础。该研究基于在青藏高原高寒草甸连续4年(2009-2012年)氮、磷添加后对不同功能群植物地上生物量、群落地上和地下生物量的测定, 探讨高寒草甸生态系统碳输入对氮、磷添加的响应。结果表明: (1)氮、磷添加均极显著增加了禾草的地上绝对生物量及其在群落总生物量中所占的比例, 同时均显著降低了杂类草在群落总生物量中的比例, 此外磷添加极显著降低了莎草地上绝对生物量及其在群落总生物量中所占的比例。(2)氮、磷添加均显著促进了青藏高原高寒草甸的地上生物量增加, 分别增加了24%和52%。(3)氮添加对高寒草甸地下生物量无显著影响, 而磷添加后地下生物量有增加的趋势。(4)氮添加对高寒草甸植物总生物量无显著影响, 而磷添加后植物总生物量显著增加。研究表明, 氮、磷添加可缓解青藏高原高寒草甸植物生长的营养限制, 促进植物地上部分的生长, 然而高寒草甸植物的生长极有可能更受土壤中可利用磷含量的限制。     

Resource manipulation effects on net primary production,biomass allocation and rain-use efficiency of two semiarid grassland sites in Inner Mongolia,China

Productivity of semiarid grasslands is affected by soil water and nutrient availability, with water controlling net primary production under dry conditions and soil nutrients constraining biomass production under wet conditions. In order to investigate limitations on plants by the response of root–shoot biomass allocation to water and nitrogen (N) availability, a field experiment, on restoration plots with rainfed, unfertilized control plots, fertilized plots receiving N (25 kg urea-N ha⁻¹) and water (irrigation simulating a wet season), was conducted at two sites with different grazing histories: moderate (MG) and heavy (HG) grazing. Irrigation and N addition had no effect on belowground biomass. Irrigation increased aboveground (ANPP) and belowground net primary production (BNPP) and rain-use efficiency based on ANPP (RUE_ANPP), whereas N addition on rainfed plots had no effect on any of the measured parameters. N fertilizer application on irrigated plots increased ANPP and RUE_ANPP and reduced the root fraction (RF: root dry matter/total dry matter), resulting in smaller N effects on total net primary production (NPP) and rain-use efficiency based on NPP. This suggests that BNPP should be included in evaluating ecosystem responses to resource availability from the whole-plant perspective. N effects on all measured parameters were similar on both sites. However, site HG responded to irrigation with higher ANPP and a lower RF when compared to site MG, indicating that species composition had a pronounced effect on carbon allocation pattern due to below- and aboveground niche complementarity.     

13C and 15N in microarthropods reveal little response of Douglas-fir ecosystems to climate change

Understanding ecosystem carbon (C) and nitrogen (N) cycling under global change requires experiments maintaining natural interactions among soil structure, soil communities, nutrient availability, and plant growth. In model Douglas-fir ecosystems maintained for five growing seasons, elevated temperature and carbon dioxide (CO₂) increased photosynthesis and increased C storage belowground but not aboveground. We hypothesized that interactions between N cycling and C fluxes through two main groups of microbes, mycorrhizal fungi (symbiotic with plants) and saprotrophic fungi (free-living), mediated ecosystem C storage. To quantify proportions of mycorrhizal and saprotrophic fungi, we measured stable isotopes in fungivorous microarthropods that efficiently censused the fungal community. Fungivorous microarthropods consumed on average 35% mycorrhizal fungi and 65% saprotrophic fungi. Elevated temperature decreased C flux through mycorrhizal fungi by 7%, whereas elevated CO₂ increased it by 4%. The dietary proportion of mycorrhizal fungi correlated across treatments with total plant biomass (n= 4, r²= 0.96, P= 0.021), but not with root biomass. This suggests that belowground allocation increased with increasing plant biomass, but that mycorrhizal fungi were stronger sinks for recent photosynthate than roots. Low N content of needles (0.8–1.1%) and A horizon soil (0.11%) coupled with high C : N ratios of A horizon soil (25–26) and litter (36–48) indicated severe N limitation. Elevated temperature treatments increased the saprotrophic decomposition of litter and lowered litter C : N ratios. Because of low N availability of this litter, its decomposition presumably increased N immobilization belowground, thereby restricting soil N availability for both mycorrhizal fungi and plant growth. Although increased photosynthesis with elevated CO₂ increased allocation of C to ectomycorrhizal fungi, it did not benefit plant N status. Most N for plants and soil storage was derived from litter decomposition. N sequestration by mycorrhizal fungi and limited N release during litter decomposition by saprotrophic fungi restricted N supply to plants, thereby constraining plant growth response to the different treatments.     

Trade-offs in plant responses to herbivory influence trophic routes of production in a freshwater wetland

Responses of aquatic macrophytes to leaf herbivory may differ from those documented for terrestrial plants, in part, because the potential to maximize growth following herbivory may be limited by the stress of being rooted in flooded, anaerobic sediments. Herbivory on aquatic macrophytes may have ecosystem consequences by altering the allocation of nutrients and production of biomass within individual plants and changing the quality and quantity of aboveground biomass available to consumers or decomposers. To test the effects of leaf herbivory on plant growth and production, herbivory of a dominant macrophyte, Nymphaea odorata, by chrysomelid beetles and crambid moths was controlled during a 2-year field experiment. Plants exposed to herbivory maintained, or tended to increase, biomass and aboveground net primary production relative to controls, which resulted in 1.5 times more aboveground primary production entering the detrital pathway of the wetland. In a complementary greenhouse experiment, the effects of simulated leaf herbivory on total plant responses, including biomass and nutrient allocation, were investigated. Plants in the greenhouse responded to moderate herbivory by maintaining aboveground biomass relative to controls, but this response occurred at the expense of belowground growth. Results of these studies suggest that N. odorata may tolerate moderate levels of herbivory by reallocating biomass and resources aboveground, which in turn influences the quantity, quality and fate of organic matter available to herbivores and decomposers.     

Plant invasion alters nitrogen cycling by modifying the soil nitrifying community

Plant invasions have dramatic aboveground effects on plant community composition, but their belowground effects remain largely uncharacterized. Soil microorganisms directly interact with plants and mediate many nutrient transformations in soil. We hypothesized that belowground changes to the soil microbial community provide a mechanistic link between exotic plant invasion and changes to ecosystem nutrient cycling. To examine this possible link, monocultures and mixtures of exotic and native species were maintained for 4 years in a California grassland. Gross rates of nitrogen (N) mineralization and nitrification were quantified with ¹⁵N pool dilution and soil microbial communities were characterized with DNA‐based methods. Exotic grasses doubled gross nitrification rates, in part by increasing the abundance and changing the composition of ammonia‐oxidizing bacteria in soil. These changes may translate into altered ecosystem N budgets after invasion. Altered soil microbial communities and their resulting effects on ecosystem processes may be an invisible legacy of exotic plant invasions.     

Aggravated phosphorus limitation on biomass production under increasing nitrogen loading: a meta‐analysis

Nitrogen (N) and phosphorus (P), either individually or in combination, have been demonstrated to limit biomass production in terrestrial ecosystems. Field studies have been extensively synthesized to assess global patterns of N impacts on terrestrial ecosystem processes. However, to our knowledge, no synthesis has been done so far to reveal global patterns of P impacts on terrestrial ecosystems, especially under different nitrogen (N) levels. Here, we conducted a meta‐analysis of impacts of P addition, either alone or with N addition, on aboveground (AGB) and belowground biomass production (BGB), plant and soil P concentrations, and N : P ratio in terrestrial ecosystems. Overall, our meta‐analysis quantitatively confirmed existing notions: (i) colimitation of N and P on biomass production and (ii) more P limitation in tropical forest than other ecosystems. More importantly, our analysis revealed new findings: (i) P limitation on biomass production was aggravated by N enrichment and (ii) plant P concentration was a better indicator of P limitation than soil P availability. Specifically, P addition increased AGB and BGB by 34% and 13%, respectively. The effect size of P addition on biomass production was larger in tropical forest than grassland, wetland, and tundra and varied with P fertilizer forms, P addition rates, or experimental durations. The P‐induced increase in biomass production and plant P concentration was larger under elevated than ambient N. Our findings suggest that the global limitation of P on biomass production will become severer under increasing N fertilizer and deposition in the future.     

Interactions among plants,bacteria, and fungi reduce extracellular enzyme activities under long‐term N fertilization

Atmospheric nitrogen (N) deposition has enhanced soil carbon (C) stocks in temperate forests. Most research has posited that these soil C gains are driven primarily by shifts in fungal community composition with elevated N leading to declines in lignin degrading Basidiomycetes. Recent research, however, suggests that plants and soil microbes are dynamically intertwined, whereby plants send C subsidies to rhizosphere microbes to enhance enzyme production and the mobilization of N. Thus, under elevated N, trees may reduce belowground C allocation leading to cascading impacts on the ability of microbes to degrade soil organic matter through a shift in microbial species and/or a change in plant–microbe interactions. The objective of this study was to determine the extent to which couplings among plant, fungal, and bacterial responses to N fertilization alter the activity of enzymes that are the primary agents of soil decomposition. We measured fungal and bacterial community composition, root–microbial interactions, and extracellular enzyme activity in the rhizosphere, bulk, and organic horizon of soils sampled from a long‐term (>25 years), whole‐watershed, N fertilization experiment at the Fernow Experimental Forest in West Virginia, USA. We observed significant declines in plant C investment to fine root biomass (24.7%), root morphology, and arbuscular mycorrhizal (AM) colonization (55.9%). Moreover, we found that declines in extracellular enzyme activity were significantly correlated with a shift in bacterial community composition, but not fungal community composition. This bacterial community shift was also correlated with reduced AM fungal colonization indicating that declines in plant investment belowground drive the response of bacterial community structure and function to N fertilization. Collectively, we find that enzyme activity responses to N fertilization are not solely driven by fungi, but instead reflect a whole ecosystem response, whereby declines in the strength of belowground C investment to gain N cascade through the soil environment.     

Additive Effects of Warming and Increased Nitrogen Deposition in a Temperate Old Field: Plant Productivity and the Importance of Winter

Both climate warming and atmospheric nitrogen (N) deposition are predicted to alter plant productivity and species composition over the next century. However, the extent to which their effects may interact is unclear. For example, over winter, the effects of warming on soil freezing dynamics may promote ecosystem N losses, thereby limiting increases in productivity in response to warming, yet these losses may be compensated for by increased N deposition. We measured plant production and species composition in response to warming (winter-only or year-round) and N addition in a temperate old field. We used shoot allometric relationships to estimate aboveground production non-destructively and sampled root biomass destructively throughout two growing seasons. We also used spectral data (normalized difference vegetation index—NDVI) to examine the treatment effects on the timing of plant green-up and senescence. In 2007, which featured an exceptionally dry summer, there were no treatment effects on plant growth. However, in 2008, warming (both winter-only and year-round) and N addition combined approximately doubled aboveground productivity, and these effects were additive. Warming increased root biomass, but no N effect was evident. Conversely, N addition increased NDVI, but NDVI was unresponsive to warming. Overall, our results do not support the hypothesis that warming-induced changes to soil freezing dynamics limit plant productivity in our system. On the contrary, they demonstrate that winter warming alone can increase primary productivity to the same extent as year-round warming, and that this effect may interact very strongly with interannual variation in precipitation.     

Intermediate herbivory intensity of an aboveground pest promotes soil labile resources and microbial biomass via modifying rice growth

Background and Aims

The importance of aboveground herbivores for modifying belowground ecosystems has prompted numerous studies; however, studies can be biased by context dependent conditions which lead to extremely inconsistent results. So far, the impacts of herbivory intensity by important rice pests on rice paddy soil ecosystems are lacking. The aim of this study was to test the hypothesis that intermediate herbivory intensity of the brown planthopper (Nilaparvata lugens Stål) could promote soil labile resources and microbial biomass, while high intensity would show a reverse pattern, by mediating rice plant growth. This study will also help the development of integrative pest management.

Methods

Four hopper infestation density treatments (0, 4, 8 and 12 nymphs per rice plant) and two infestation duration treatments (9 and 15 days after N. lugens infestation, DAI 9 and DAI 15) were established in a glasshouse experiment. Soil and plant were sampled destructively from four replicates and analysed for soil labile resources availability, soil microbial biomass and plant performance, respectively.

Results

The infestation density significantly affected both shoot and root mass of rice (P?<?0.05), soil dissolved organic carbon (DOC) and nitrogen (DON), and microbial biomass carbon (MBC) and nitrogen (MBN), and the effects were further enhanced by prolonged infestation duration. Compared to the control (CK) without N. lugens, plant dry mass, DOC, DON, MBC and MBN increased under low (LD) and moderate hopper densities (MD) but decreased under high density (HD) on DAI 9. Moreover, the LD treatment exerted the most promotional effects on DAI 15. Rice root to shoot ratio generally increased in treatments subjected to herbivory. The labile resources and microbial biomass showed close relationships with both shoot and root mass across treatments, in particular with root mass on DAI 15. Such a trend indicated that the shift of photosynthate allocation to belowground contributed to changes of soil resource availability and microbial biomass.

Conclusions

Intermediate herbivory intensity showed positive effects on rice seedling performance and, further, promoted soil labile resource availability and microbial biomass. The importance of extrapolating temporal and spatial scale, i.e. from the short-term greenhouse experiment to an entire rice growing season in the field, was highlighted.     

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.