G. W. Yeates

Linking above-ground and below-ground interactions: How plant responses to foliar herbivory influence soil organisms

Abstract Studies of the effects of above-ground herbivory on soil organisms and decomposer food webs, as well as the processes that they regulate, have largely concentrated on the effects of non-living inputs into the soil, such as dung, urine, body parts and litter. However, there is an increasing body of information which points to the importance of plant physiological responses to herbivory in regulating soil organisms and therefore, implicitly, key soil processes such as decomposition and nutrient mineralisation. In this review we identify the mechanisms by which foliar herbivory may indirectly affect the soil biota and associated below-ground processes through affecting plants, so as to better understand the nature of interactions which exist between above-ground and below-ground biota. We consider two broad pathways by which above-ground foliar herbivory may affect soil biotic communities. The first of these occurs through herbivore effects on patterns of root exudation and carbon allocation. These effects manifest themselves either as short-term changes in plant C allocation and root exudation or as long-term changes in root biomass and morphology. Evidence suggests that these mechanisms positively influence the size and activity of the soil biotic community and may alter the supply of nutrients in the rhizosphere for plant uptake and regrowth. The second of these involves herbivores influencing soil organisms through altering the quality of input of plant litter. Possible mechanisms by which this occurs are through herbivory enhancing nitrogen contents of root litter, through herbivory affecting production of secondary metabolites and concentrations of nutrients in foliage and thus in leaf litter and through selective foliar feeding causing shifts in plant community structure and thus the nature of litter input to the soil. While the effects of herbivory on soil organisms via plant responses may be extremely important, the directions of these effects are often unpredictable because several mechanisms are often involved and because of the inherently complex nature of soil food-web interactions; this creates obvious difficulties in developing general principles about how herbivory affects soil food-webs. Finally, it is apparent that very little is understood on how responses of soil organisms to herbivory affect those ecosystem-level processes regulated by the soil food-web (e.g. decomposition, nutrient mineralisation) and that such information is essential in developing a balanced understanding about how herbivory affects ecosystem function.

PLANT REMOVALS IN PERENNIAL GRASSLAND: VEGETATION DYNAMICS, DECOMPOSERS, SOIL BIODIVERSITY, AND ECOSYSTEM PROPERTIES

The consequences of permanent loss of species or species groups from plant communities are poorly understood, although there is increasing evidence that individual species effects are important in modifying ecosystem properties. We conducted a field experiment in a New Zealand perennial grassland ecosystem, creating artificial vegetation gaps and imposing manipulation treatments on the reestablishing vegetation. Treatments consisted of continual removal of different subsets or “functional groups” of the flora. We monitored vegetation and soil biotic and chemical properties over a 3-yr period. Plant competitive effects were clear: removal of the C3 grass Lolium perenne L. enhanced vegetative cover, biomass, and species richness of both the C4 grass and dicotyledonous weed functional groups and had either positive or negative effects on the legume Trifolium repens L., depending on season. Treatments significantly affected total plant cover and biomass; in particular, C4 grass removal reduced total plant biomass in summer, because no other species had appropriate phenology. Removal of C3 grasses reduced total root biomass and drastically enhanced overall shoot-to-root biomass ratios. Aboveground net primary productivity (NPP) was not strongly affected by any treatment, indicating strong compensatory effects between different functional components of the flora. Removing all plants often negatively affected three further trophic levels of the decomposer functional food web: microflora, microbe-feeding nematodes, and predaceous nematodes. However, as long as plants were present, we did not find strong effects of removal treatments, NPP, or plant biomass on these trophic groupings, which instead were most closely related to spatial variation in soil chemical properties across all trophic levels, soil N in particular. Larger decomposer organisms, i.e., Collembola and earthworms, were unresponsive to any factor other than removal of all plants, which reduced their populations. We also considered five functional components of the soil biota at finer taxonomic levels: three decomposer components (microflora, microbe-feeding nematodes, predaceous nematodes) and two herbivore groups (nematodes and arthropods). Taxa within these five groups responded to removal treatments, indicating that plant community composition has multitrophic effects at higher levels of taxonomic resolution. The principal ordination axes summarizing community-level data for different trophic groups in the soil food web were related to each other in several instances, but the plant ordination axes were only significantly related to those of the soil microfloral community. There were time lag effects, with ordination axes of soil-associated herbivorous arthropods and microbial-feeding nematodes being related to ordination axes representing plant community structure at earlier measurement dates. Taxonomic diversity of some soil organism groups was linked to plant removals or to plant diversity. For herbivorous arthropods, removal of C4 grasses enhanced diversity; there were negative correlations between plant and arthropod diversity, presumably because of negative influences of C4 species in the most diverse treatments. There was evidence of lag relationships between diversity of plants and that of the three decomposer groups, indicating multitrophic effects of altering plant diversity. Relatively small effects of plant removal on the decomposer food web were also apparent in soil processes regulated by this food web. Decomposition rates of substrates added to soils showed no relationship with treatment, and rates of CO2 evolution from the soil were only adversely affected when all plants were removed. Few plant functional-group effects on soil nutrient dynamics were identified. Although some treatments affected temporal variability (and thus stability) of soil biotic properties (particularly CO2 release) throughout the experiment, there was no evidence of destabilizing effects of plant removals. Our data provide evidence that permanent exclusion of plant species from the species pool can have important consequences for overall vegetation composition in addition to the direct effects of vegetation removal, and various potential effects on both the above- and belowground subsystems. The nature of many of these effects is driven by which plant species are lost from the system, which depends on the various attributes or traits of these species.

Nematodes as soil indicators: functional and biodiversity aspects

Since it has become appreciated that soil nematode assemblages are abundant, diverse and contribute to soil nutrient turnover, they have been increasingly used as indicators of soil condition. Use of nematodes as functional indicators relies on the allocation of nematodes to feeding groups and reproductive strategies; in both cases groupings are uncertain. Species within feeding groups vary in their food resources and response to environmental variables, as shown by the difficulties in managing plant-pathogenic nematodes. Therefore species-level discrimination is necessary to permit further advances in understanding the role of nematodes in soil processes and thus in ecosystem resilience. Analysis of published nematode lists shows that among the bacterial-feeding nematodes Cephalobidae are often the most abundant group in soils; Rhabditidae may increase following a resource pulse; in stressed, natural environments Plectidae may be important. To be comparable with other biota, nematode biodiversity assessment requires species-level identification. In many jurisdictions such identification will be difficult due to inadequate systematic knowledge of the nematode fauna.

INTRODUCED BROWSING MAMMALS IN NEW ZEALAND NATURAL FORESTS: ABOVEGROUND AND BELOWGROUND CONSEQUENCES

Forest dwelling browsing mammals, notably feral goats and deer, have been introduced to New Zealand over the past 220 years; prior to this such mammals were absent from New Zealand. The New Zealand forested landscape, therefore, presents an almost unique opportunity to determine the impacts of introduction of an entire functional group of alien animals to a habitat from which that group was previously absent. We sampled 30 long-term fenced exclosure plots in indigenous forests throughout New Zealand to evaluate community- and ecosystem-level impacts of introduced browsing mammals, emphasizing the decomposer subsystem. Browsing mammals often significantly altered plant community composition, reducing palatable broad-leaved species and promoting other less palatable types. Vegetation density in the browse layer was also usually reduced. Although there were some small but statis- tically significant effects of browsing on some measures of soil quality across the 30 locations, there were no consistent effects on components of the soil microfood web (com- prising microflora and nematodes, and spanning three consumer trophic levels); while there were clear multitrophic effects of browsing on this food web for several locations, com- parable numbers of locations showed stimulation and inhibition of biomasses or populations of food web components. In contrast, all microarthropod and macrofaunal groups were consistently adversely affected by browsing, irrespective of trophic position. Across the 30 locations, the magnitude of response of the dominant soil biotic groups to browsing mammals (and hence their resistance to browsers) was not correlated with the magnitude of vegetation response to browsing but was often strongly related to a range of other variables, including macroclimatic, soil nutrient, and tree stand properties. There were often strong significant effects of browsing mammals on species composition of the plant community, species composition of leaf litter in the litter layer, and composition of various litter-dwelling faunal groups. Across the 30 locations, the magnitude of browsing mammal effects on faunal community composition was often correlated with browser effects on litter layer leaf species composition but never with browser effects on plant community composition. Browsing mammals usually reduced browse layer plant diversity and often also altered habitat diversity in the litter layer and diversity of various soil faunal groups. Across the 30 locations, the magnitude of browser effects on diversity of only one faunal group, humus-dwelling nematodes, was correlated with browser effects on plant diversity. However, browser effects on diversity of diplopods and gastropods were correlated with browser effects on habitat diversity of the litter layer. Reasons for the lack of unidirectional relationships across locations between effects of browsers on vegetation community attri- butes and on soil invertebrate community attributes are discussed. Browsing mammals generally did not have strong effects on C mineralization but did significantly influence soil C and N storage on an areal basis for several locations. However the direction of these effects was idiosyncratic and presumably reflects different mechanisms by which browsers affect soil processes. While our study did not support hypotheses predicting consistent negative effects of browsing mammals on the decomposer subsystem through promotion of plant species with poorer litter quality, our results still show that the introduction of these mammals to New Zealand has caused far-ranging effects at both the community and ecosystem levels of resolution, with particularly adverse effects for indigenous plant com- munities and populations of most groups of litter-dwelling mesofauna and macrofauna.

The influence of nematodes on below-ground processes in grassland ecosystems

This review summarises recent information on beneficial roles that soil nematodes play in the cycling of carbon and other plant nutrients in grassland ecosystems. In particular, we focus on the role of the two dominant functional groups of nematodes, namely the microbial- and root-feeders, and how their activities may enhance soil ecosystem-level processes of nutrient cycling and, ultimately, plant productivity in managed and unmanaged grassland ecosystems. We report recent experiments which show that low amounts of root herbivory by nematodes can increase the allocation of photoassimilate carbon to roots, leading to increased root exudation and microbial activity in the rhizosphere. The effects of these interactions on soil nutrient cycling and plant productivity are discussed. Evidence is presented to show that the feeding activities of microbial-feeding nematodes can enhance nutrient mineralization and plant nutrient uptake in grasslands, but that these responses are highly species-specific and appear to be strongly regulated by higher trophic groups of fauna (top-down regulation). We recommend that future studies of the roles of nematodes in grasslands ecosystems should consider these more complex trophic interactions and also the effects of species diversity of nematodes on soil ecosystem-level processes.

Response of soil microbial biomass dynamics, activity and plant litter decomposition to agricultural intensification over a seven-year period

Soil microorganisms and the processes that they govern are essential for long-term sustainability of agricultural systems, but most studies on agricultural effects on the soil microflora are inherently short-term. We investigated the effects of three aspects of agricultural intensification, i.e. cultivation (disturbance), herbicide addition (modification of plant composition) and mulching (resource addition) on soil biological properties such as microbial biomass and activity over 7 yr in annual (maize) and perennial (asparagus) cropping systems. The mulching treatment had strong, usually positive effects on both substrate-induced respiration (SIR) and CO2–C release from chloroform-fumigated soil throughout the study. In the perennial crop, treatments allowing high weed biomass caused large increases in microbial biomass and respiration after yr 3, and in both sites microbial biomass was positively correlated with weed biomass and negatively with crop plant biomass. This latter effect appears due to the high decomposability of weed residues relative to those from crop plants. Microbial biomass was also enhanced in atrazine-treated plots in the annual crop but only during the final year, presumably due to beneficial effects of plot invasion by herbicide-tolerant weeds. Mulching often also enhanced the microbial metabolic quotient (qCO2), the bacteria-to-fungal biomass ratio and within-year temporal variability of the microbial biomass, all of which are indicative of greater turnover and instability of the microbial biomass. Other treatments generally had smaller effects on these properties, although in the perennial crop an intense summer drought in yr 4 caused a large elevation in the metabolic quotient in the herbicide-treated (low weed) plots relative to the other plots, suggesting that high quality weed residues have stabilising effects. Temporal variability across years of both SIR and CO2–C release from fumigated soil was greatest in the herbicide-treated plots in the perennial crop, suggesting that high weed biomass (producing easily degradable organic matter) has stabilising effects. Decomposition rates of added litter were partially consistent with the microbial biomass data, with the highest litter breakdown rates usually occurring in the mulched plots. Our study shows that soil biological properties such as microbial biomass and activity are not necessarily adversely affected by agricultural intensification and that consequences of intensification mainly depend upon practices which alter the quality and quantity of residue inputs. Further, our results underline the need for long,-term field experiments, and several of the effects we identified could only have been detected through an experiment of several years duration.

Impact of pasture contamination by copper, chromium, arsenic timber preservative on soil biological activity

Contamination of grazed pasture gave 0–5 cm soil contents of 19–835 mg kg-1 Cu, 47–739 mg kg-1 Cr, and 12–790 mg kg-1 As. Soil Cu, Cr, As contents were correlated and declined with depth to 30 cm. In plots with medium and high contamination buried cotton strips retained most of their original tensile strength, indicating repression of decomposition processes.Lumbricus rubellus andAporrectodea rosea were absent in plots with medium and high contamination; there was no evidence of heavy metal accumulation in earthworm tissue; soil bulk density was greater in the absence of lumbricids. Enchytraeids and nematodes were most abundant with low contamination. Nematode diversity was greater with low (0–5 cm) or medium (5–10 cm) contamination than in control plots or those with high contamination; the proportion of predators increased with contamination. Basal soil respiration was less sensitive than substrate-induced respiration to contamination. Although contamination reduced the nitrification rate, all mineral N was found as NOinf3sup- after 14 days. Sulphatase was the enzyme activity most sensitive to high contamination. Whereas contamination by 100 mg kg-1 of Cu, Cr, and As caused little depression of soil biological activity, there was some supperssion at 400 mg kg-1 and at 800 mg kg-1 normal processes were inhibited and herbage production was negligible. No single measurement adequately indicated the need for site remediation.

Responses of soil nematode populations, community structure, diversity and temporal variability to agricultural intensification over a seven-year period

Because soil nematode populations play a key role in regulating the turnover of microbial communities and respond to changes in environmental conditions, shifts in their abundance and composition can be useful indicators of soil conditions. In this study nematode communities and other ecosystem variables were investigated over 7 yr under an annual (Zea mays) and a perennial (Asparagus officinale) crop using three weed management practices (cultivation, herbicide application, mulching) which can be related to agricultural intensification. Crop productivity and soil conditions did not change significantly during the trial. All management practices influenced the nematode fauna but the greatest long-term effects were from sawdust mulching. In the mulched plots there was an initial flush of both total and bacterial-feeding nematodes but both subsequently declined, which was coincident with enhanced populations of top predatory nematodes. The apparent negative interaction between bacterial-feeding and predatory nematodes was also demonstrated through the former being significantly (P<0.001) negatively correlated with soil carbon, bacterial mass and weed biomass and the latter being positively correlated with the same variables. Herbicide use did not exert any consistent detrimental effects on nematode communities and the nematode fauna in the herbicide treated plots tended to have greater diversity (as indicated by the Shannon–Weiner index) than that in many of the other plots. The effects of cultivation varied, but under the perennial crop the greatest number of total and bacterial-feeding nematodes were commonly at 5–10 cm depth in cultivated plots. While most treatments had relatively little general effect on the composition of the nematode fauna over the study period, several important specific effects were only apparent after at least 3 yr. Thus to effectively evaluate the relative effects of different agricultural practices in the long-term it is necessary to sample until the ecosystem has achieved some degree of equilibrium rather than monitoring only initial cropping cycles.

Relationships between nematodes, soil microbial biomass and weed-management strategies in maize and asparagus cropping systems

Abstract Five weed-management strategies (sawdust mulching, repeated spring-summer cultivation, hand-hoeing, two herbicide treatments) were applied to asparagus and maize cropping systems near Hamilton, New Zealand. Assessments of 27 nematode populations on four sampling occasions over an entire cropping cycle are related to published microbial, arthropod and environmental data. Under asparagus cropping abundance of 11 nematode populations (at genus or family level) in 0–5 cm soil showed significant treatment effects on at least two sampling occasions; under maize 6 populations showed treatment effects. Overall, the most obvious trends were for some taxa of bacterial feeding nematodes to have their greatest abundances under different treatments. The ratio of bacterial feeding to fungal feeding nematodes varied significantly with time and treatment, and indicates shifts in trophic structure of the nematode fauna. Canonical correspondence analysis demonstrated that nematode populations were more strongly related to environmental factors at the prior sampling than those at the contemporary sampling time. Under asparagus cropping the sawdust mulch was the predominant factor affecting ordinations; bacterial and fungal feeding nematodes were most abundant or showed greatest treatment responses, but the increase in populations of predacious nematodes (Nygolaimus, Mononchidae, Aporcelaimidae) may be responsible for absence of marked increases in these other groups. Under maize, effects were similar but less significant. Helicotylenchus and Pratylenchus were present under the maize crop but not under the asparagus crop. The responses of nematode taxa to weed management practices were very variable but, given the range of life history strategies within trophic groups, responses follow a predictable pattern. Detailed correlation of management-induced changes in nematode populations and biological environmental factors is confounded by the effect of nematode feeding activity on the microbial populations. Overall, the results confirm the important influence of microfaunal grazing on microfloral populations and the cycling of plant nutrients in the soil.

Effects of agricultural intensification on soil-associated arthropod population dynamics, community structure, diversity and temporal variability over a seven-year period

Abstract While most studies focusing on the effects of agricultural intensification on soil biota are inherently short-term in nature, long-term (multiyear) studies are essential in assessing long-term temporal responses of soil biota to agronomic practices. We investigated the effects of three components of agricultural intensification, i.e. cultivation (disturbance), herbicide addition (modification of floristic composition) and mulching (resource addition) on soil-associated arthropods in an annual (maize) and a perennial (asparagus) cropping system over a 7 yr period. An additional treatment (hand-hoeing of weeds during the crop growing season) was used to represent minimal intensification. Many taxa of arthropods responded positively to mulching and to treatments which allowed high weed biomass in the non crop-production period, e.g. the hand-hoeing and cultivation treatments in the perennial crop. Herbicide treatments also facilitated high numbers of many taxa in the annual crop when this coincided with plot invasion by herbicide-tolerant weeds. Generally, arthropod taxa were positively correlated with weed biomass and negatively with crop plant biomass, probably because of the superior resource (litter) quality produced by the former. Ordination analyses indicated that arthropod community structure was often correlated with weed community structure. Mulching and allowing high weed biomass also promoted a high species richness of soil-associated Coleoptera, but coleopteran diversity was not related to weed species diversity. Analyses of temporal variability (inversely related to stability) of arthropod taxa across years revealed few treatment effects in the annual crop, but showed destabilising effects of weed reduction in the perennial crop. In the perennial crop, temporal variability was also positively correlated with crop biomass and negatively with weed biomass across plots. Our study shows that agricultural intensification is not consistently harmful to the soil fauna, that soil-associated arthropods are most responsive to management practices which affect the nature and quality of resource input, and that long-term experiments are essential for answering questions about how agricultural practices affect soil organisms against the natural backdrop of temporal variation.