Combined effects of warming and drought on plant biomass depend on plant woodiness and community type: a meta-analysis.

Global warming and precipitation extremes (drought or increased precipitation) strongly affect plant primary production and thereby terrestrial ecosystem functioning. Recent syntheses show that combined effects of warming and precipitation extremes on plant biomass are generally additive, while individual experiments often show interactive effects, indicating that combined effects are more negative or positive than expected based on the effects of single factors. Here, we examined whether variation in biomass responses to single and combined effects of warming and precipitation extremes can be explained by plant growth form and community type. We performed a meta-analysis of 37 studies, which experimentally crossed warming and precipitation treatments, to test whether biomass responses to combined effects of warming and precipitation extremes depended on plant woodiness and community type (monocultures versus mixtures). Our results confirmed that the effects of warming and precipitation extremes were overall additive. However, combined effects of warming and drought on above- and belowground biomass were less negative in woody- than in herbaceous plant systems and more negative in plant mixtures than in monocultures. We further show that drought effects on plant biomass were more negative in greenhouse, than in field studies, suggesting that greenhouse experiments may overstate drought effects in the field. Our results highlight the importance of plant system characteristics to better understand plant responses to climate change

Combined effects of warming and drought on plant biomass depend on plant woodiness and community type: a meta-analysis

Global warming and precipitation extremes (drought or increased precipitation) strongly affect plant primary production and thereby terrestrial ecosystem functioning. Recent syntheses show that combined effects of warming and precipitation extremes on plant biomass are generally additive, while individual experiments often show interactive effects, indicating that combined effects are more negative or positive than expected based on the effects of single factors. Here, we examined whether variation in biomass responses to single and combined effects of warming and precipitation extremes can be explained by plant growth form and community type. We performed a meta-analysis of 37 studies, which experimentally crossed warming and precipitation treatments, to test whether biomass responses to combined effects of warming and precipitation extremes depended on plant woodiness and community type (monocultures versus mixtures). Our results confirmed that the effects of warming and precipitation extremes were overall additive. However, combined effects of warming and drought on above- and belowground biomass were less negative in woody- than in herbaceous plant systems and more negative in plant mixtures than in monocultures. We further show that drought effects on plant biomass were more negative in greenhouse, than in field studies, suggesting that greenhouse experiments may overstate drought effects in the field. Our results highlight the importance of plant system characteristics to better understand plant responses to climate change

Impact of trophic ecologies on the whereabouts of nematodes in soil

Soil life is highly diverse, and ecologically intricate due to myriad of biotic interactions that take place. Terrestrial nematodes have a high potential to serve as an effective and policy-relevant indicator group for ecosystem functioning and soil biodiversity. The work described in this thesis contributed to the robust mapping of nematode communities at scales relevant in both agronomic and environmental contexts. The overarching aim of the work described in this thesis was to contribute to a sound exploration of the potential of nematode communities as an indicator group for the biological condition of soils. Therefore, the distributions of a wide range of nematode taxa were studied, within and between trophic groups and in soils conditioned by various plant species and/or farming systems. In Chapter 2 nematode taxon-specific qPCR assays were used to pinpoint responses of nematode communities to invasive plant species Solidago gigantea in two invaded ecosystems: semi-natural grasslands and riparian floodplains. Nematode communities and fungal biomass were examined in adjacent invaded and uninvaded patches. The dominant presence of the invasive plant causes a decrease of plant species-richness and diversity, and an about twofold increase of fungal biomass. Only the density of a single group of fungivorous nematodes (Aphelenchoididea) increased, whereas the densities of two other, phylogenetically distinct lineages of fungivorous nematodes, Aphelenchidae and Diphtherophoridae, were unaffected by the local increase in fungal biomass. Apparently S. gigantea induces a local asymmetric boost of the fungal community, and only Aphelenchoididae were able to benefit from this change induced by the invasive plant. In Chapter 3 the outcome is shown of a test whether farming system effects are mirrored in compositional changes in nematode communities. The long-term impact of three farming systems (conventional, integrated and organic) on nematode communities was investigated at the Vredepeel, an experimental farm in the southeastern part of The Netherlands. The results showed that organic farming causes specific shifts in nematode community composition, exceeding the usually large crop-related assemblage shifts. Strongest effects were observed for the (putative) bacterivore Prismatolaimus, which was relatively common in organic fields and nearly absent in conventional and integrated farming. A reverse effect was observed for Pristionchus; this necromenic bacterivore and facultative predator made up about 7 – 21% of the total nematode community in integrated and conventional farming, whereas it was nearly absent from organic fields. The observed farming system effects suggest that specific nematode taxa might be indicative for the impact of farming practices on soil biota. Knowledge of spatial distribution patterns of soil organisms with distinct trophic preferences will contribute to our understanding of factors that maintain and regulate soil biodiversity, and is essential information to design soil sampling strategies with predictable accuracies. Chapter 4 deals with microscale patchiness of 45 nematode taxa (at family, genus or species-level) in arable fields and semi-natural grasslands, on marine clay, river clay or sandy soils. Contrary to our expectations, an increase of the number of cores per composite sample above 3, did not result in more accurate detection for any of the taxa under investigation (range of number of cores per composite sample: 3, 6, 12 or 24). Neither system nor soil type did influence microscale distribution. The insights in the spatial distribution of nematodes at microscale presented here, sheds light on the impact of trophic preferences on the spatial distribution of individual nematode taxa, and will allow for the design of statistically sound soil sampling strategies. Chapter 5 shows belowground distribution patterns of 48 nematode taxa in 12 visually homogeneous fields (each 100 x 100 m) on three soil types (marine clay, river clay and sand) and two land-use types (arable and natural grasslands) across the Netherlands. Over 35,000 nematode-taxon specific qPCR assays allowed us to quantitative analyse nematode taxa at family, genus or species level in over 1,200 soil samples. A sampling scheme was optimized for Bayesian geostatistical analysis (Integrated nested Laplace approximations; INLA). Multivariate analysis show soil type and land-use related differences in the nematode community composition, which underline the effects of environmental filtering and niche partitioning of nematodes. All individual nematode taxa together show a wide range of degrees of spatial variabilities were found (expressed by the range-parameter and the spatial variance parameter (s2spatial). No general effects were detected of soil characteristics or nematode traits (cp-value, trophic group, weight) on the spatial distribution parameters. The relatively high percentages of unexplained spatial variability – 92.5% of the variation for the range-parameter and 74% for spatial variance (s2spatial) – point at a major role of stochasticity for variability of nematode densities within fields. This study adds empirical evidence that distribution patterns of terrestrial nematodes, in areas without noticeable gradients, are driven by neutral / stochastic processes, within the boundaries set by the environment. In the final Chapter 6, I discuss the opportunities and challenges of the use of molecular tools in soil ecological research, the impact of trophic preferences on the whereabouts of nematodes, the use of nematode communities as indicator for soil condition and how this might be developed and applied to facilitate more sustainable ecosystem management

Soil predator loss alters aboveground stoichiometry in a native but not in a related range-expanding plant when exposed to periodic heat waves

Increasing frequency and magnitude of climatic extremes, such as heat waves are expected to enhance abiotic stresses on ecological communities. It has been proposed that ecological communities in disturbed habitats may be most sensitive to climatic extremes, as disturbance may reduce density and diversity of higher trophic level organisms like predators. However, there is little experimental evidence that climatic extremes indeed have stronger impact on functioning of such trophically downgraded ecosystems. Here, we experimentally examine how removal of predators from soil communities affects plant performance under periodic heat waves. We used a native plant species, and a congeneric native that is currently expanding its range because of climate change. We used soil nematode communities as the model system, as these are most abundant soil animals and their communities are trophically diverse. Predatory nematodes were manually removed from intact soil nematode communities (mainly the adults as some juveniles are impossible to manually remove) to create a trophically downgraded soil. Intact nematode communities and communities with reduced predatory nematodes were added separately to soils that were planted with either the native Centaurea jacea or the range-expanding congener Centaurea stoebe. Half the experimental units were exposed periodically to experimental heat waves of 10 °C above the control temperature. Our results show that the C: N and C: N: P ratio of plant shoots in predator-reduced soils became lower when exposed to periodic heat waves, however, only in the native plant C. jacea. The decrease in C: N ratio corresponded with increase of an herbivorous nematode in trophically intact soils of C. jacea independent of warming, whereas this relationships disappeared in warmed and predator-reduced soils. Our results accordingly highlight that periodic heat waves may affect stoichiometry of certain plant species by altering trophic interactions in predator-reduced soils.</p

Data from: Feeding preference as a main determinant of microscale patchiness among terrestrial nematodes

Soil biota are responsible for essential ecosystem services such as carbon storage, nutrient cycling and water retention. However, assessment of the condition of soil biota is hampered by an overwhelming level of diversity. With representatives in all trophic levels of the food web, nematode communities can be used as bio-indicators. Accurate assessment of nematode assemblages requires insight in the distribution of specimens with distinct food preferences. With the availability of taxon-specific quantitative-PCR assays, distribution patterns of multiple nematode groups can be investigated simultaneously. Here, microscale patchiness of 45 nematode taxa was studied on 12 sampling sites (each with four adjacent microplots) located on arable fields or semi-natural grasslands (‘system’), and on marine-, river clay or sandy soils (‘soil type’). From each microplot five composite samples were collected. Contrary to our expectations, an increase of the number of cores per composite sample did not result in more accurate measurements, and apparently the levels of microscale patchiness of the taxa are low compared to what has been reported for oligophagous plant-parasites. System and soil type did not affect microscale distribution. To investigate the level of patchiness in more detail, detection probability (DP) and variability of abundances were calculated. Common and widespread bacterivorous and fungivorous taxa had DP ≥ 90%, confirming low level of microscale patchiness. With DPs of 40-70%, predators and most omnivores showed degrees of local clustering. An overview of mean variabilities of abundances is presented that offers insight in how feeding preferences impact the microscale distribution both between and within trophic groups

Organic farming practices result in compositional shifts in nematode communities that exceed crop-related changes

Intensification of conventional agriculture has resulted in a decline of soil ecosystem functioning. Organic agriculture intends to manage soil biota in a manner that is more geared towards adequate cycling of nutrients with minimal losses. Ecological interpretation of agricultural practices-induced shifts in primary decomposers, bacteria and fungi, is non-trivial due to their enormous biodiversity. Bacterivorous and fungivorous nematodes feed selectively on these microorganisms, and we intended to test whether farming system effects are mirrored in compositional changes in nematode communities. Therefore, we analysed the impact of three farming systems, conventional (ConMin), integrated (ConSlu) and organic (Organic), on nematode communities in the southeastern part of The Netherlands on a sandy soil with 3–5% organic matter. Effects of each farming system were assessed for four different crops (barley, maize, pea or potato) by a series of taxon-specific quantitative PCRs (qPCR). Changes in community structure analysed by nonmetric multidimensional scaling (NMDS) showed that organic farming resulted in specific shifts in nematode community composition exceeding crop-related assemblage shifts. Three out of thirteen quantified nematode taxa showed significant farming system effects. Strongest effects were observed for the (putative) bacterivore Prismatolaimus, which was relatively common in Organic fields and nearly absent in ConMin and ConSlu fields. A reverse effect was observed for Pristionchus; this necromenic bacterivore and facultative predator made up about 21% and 7% of the total nematode community in respectively ConMin and ConSlu fields, whereas it was nearly absent from Organic fields. The observed farming system effects suggest that specific nematode taxa might be indicative for the impact of farming practices on soil biota

The differential impact of a native and a non-native ragwort species (Senecioneae) on the first and second trophic level of the rhizosphere food web

Whereas the impact of exotic plant species on above-ground biota is relatively well-documented, far less is known about the effects of non-indigenous plants on the first and second trophic level of the rhizosphere food web. Here, rhizosphere communities of the invasive narrow-leaved ragwort Senecio inaequidens and the native tansy ragwort Jacobaea vulgaris, co-occurring in three semi-natural habitats are compared. For both species, two life stages were taken into consideration. Quantitative PCR assays for the analyses of bacterial and fungal communities at a high taxonomic level were optimized, and it was investigated whether changes in the primary decomposer community were translated in alterations in bacterivorous and fungivorous nematode communities. In contrast to J. vulgaris, small but significant reductions were observed for Actinobacteria and Bacteroidetes (both p < 0.05) in case of the invasive S. inaequidens. More pronounced changes were detected for the overall nematode community density, and, more specifically, for the bacterivorous genus Anaplectus and the family Monhysteridae (both p < 0.05), as well as the necromenic Pristionchus (p < 0.001). At high taxonomic level, no differences were observed in fungal rhizosphere communities between native and non-native ragwort species. The impact of plant developmental stages on rhizosphere biota was prominent. The overall bacterial and fungal biomasses, as well as a remarkably consistent set of constituents (Actinobacteria, α- and β-Proteobacteria and Bacteroidetes) were negatively affected by plant stage for both ragwort species. Although later developmental stages of plants generally coincided with lower levels for individual nematode taxa, densities of the fungivorous genera Diphtherophora and Tylolaimophorus remain unaltered. Hence, even at a high taxonomic level, differential effects of native and non-native ragwort could be pinpointed. However, plant developmental stage has a more prominent impact and this impact was similar in nature for both native and non-native ragwort species

Data from: The differential impact of a native and a non-native ragwort species (Senecioneae) on the first and second trophic level of the rhizosphere food web

Whereas the impact of exotic plant species on above-ground biota is relatively well-documented, far less is known about the effects of non-indigenous plants on the first and second trophic level of the rhizosphere food web. Here, rhizosphere communities of the invasive narrow-leaved ragwort Senecio inaequidens and the native tansy ragwort Jacobaea vulgaris, co-occurring in three semi-natural habitats are compared. For both species, two life stages were taken into consideration. Quantitative PCR assays for the analyses of bacterial and fungal communities at a high taxonomic level were optimized, and it was investigated whether changes in the primary decomposer community were translated in alterations in bacterivorous and fungivorous nematode communities. In contrast to J. vulgaris, small but significant reductions were observed for Actinobacteria and Bacteroidetes (both p < 0.05) in case of the invasive S. inaequidens. More pronounced changes were detected for the overall nematode community density, and, more specifically, for the bacterivorous genus Anaplectus and the family Monhysteridae (both p < 0.05), as well as the necromenic Pristionchus (p < 0.001). At high taxonomic level, no differences were observed in fungal rhizosphere communities between native and non-native ragwort species. The impact of plant developmental stages on rhizosphere biota was prominent. The overall bacterial and fungal biomasses, as well as a remarkably consistent set of constituents (Actinobacteria, α- and β-Proteobacteria and Bacteroidetes) were negatively affected by plant stage for both ragwort species. Although later developmental stages of plants generally coincided with lower levels for individual nematode taxa, densities of the fungivorous genera Diphtherophora and Tylolaimophorus remain unaltered. Hence, even at a high taxonomic level, differential effects of native and non-native ragwort could be pinpointed. However, plant developmental stage has a more prominent impact and this impact was similar in nature for both native and non-native ragwort species

Spatial distribution of soil nematodes relates to soil organic matter and life strategy

Soils are among the most biodiverse and densely inhabited environments on our planet. However, there is little understanding of spatial distribution patterns of belowground biota, and this hampers progress in understanding species interactions in belowground communities. We investigated the spatial distribution of nematodes, which are highly abundant and diverse metazoans in most soil ecosystems. To gain insight into nematode patchiness, we mapped distribution patterns in twelve apparently homogeneous agricultural fields (100 m × 100 m each) with equal representation of three soil textures (marine clay, river clay and sandy soil). Quantitative PCRs were used to measure the abundances of 48 distinct nematode taxa in ≈1200 plots. Multivariate analysis showed that within this selection of sites, soil texture more strongly affected soil nematode communities than land management. Geostatistical analysis of nematode distributions revealed both taxon-specific and field-specific patchiness. The average geostatistical range (indicating patch diameter) of 48 nematode taxa in these fields was 36 m, and related to soil organic matter. Soil organic matter content affected the spatial variance (indicating within-field variation of densities) in a life-strategy dependent manner. The r-strategists (fast-growing bacterivores and fungivores) showed a positive correlation between organic matter content and spatial variance, whereas most K-strategists (slow-growing omnivores and carnivores) showed a negative correlation. Hence, the combination of two parameters, soil organic matter content and a general life-strategy characterisation, can be used to explain the spatial distribution of nematodes at field scale.</p