T. Martijn Bezemer

Plant-soil feedbacks: The past, the present and future challenges

Summary Plant–soil feedbacks is becoming an important concept for explaining vegetation dynamics, the invasiveness of introduced exotic species in new habitats and how terrestrial ecosystems respond to global land use and climate change. Using a new conceptual model, we show how critical alterations in plant–soil feedback interactions can change the assemblage of plant communities. We highlight recent advances, define terms and identify future challenges in this area of research and discuss how variations in strengths and directions of plant–soil feedbacks can explain succession, invasion, response to climate warming and diversity-productivity relationships. While there has been a rapid increase in understanding the biological, chemical and physical mechanisms and their interdependencies underlying plant–soil feedback interactions, further progress is to be expected from applying new experimental techniques and technologies, linking empirical studies to modelling and field-based studies that can include plant–soil feedback interactions on longer time scales that also include long-term processes such as litter decomposition and mineralization. Significant progress has also been made in analysing consequences of plant–soil feedbacks for biodiversity-functioning relationships, plant fitness and selection. To further integrate plant–soil feedbacks into ecological theory, it will be important to determine where and how observed patterns may be generalized, and how they may influence evolution. Synthesis. Gaining a greater understanding of plant–soil feedbacks and underlying mechanisms is improving our ability to predict consequences of these interactions for plant community composition and productivity under a variety of conditions. Future research will enable better prediction and mitigation of the consequences of human-induced global changes, improve efforts of restoration and conservation and promote sustainable provision of ecosystem services in a rapidly changing world.

Soil invertebrate fauna enhances grassland succession and diversity

One of the most important areas in ecology is to elucidate the factors that drive succession in ecosystems and thus influence the diversity of species in natural vegetation. Significant mechanisms in this process are known to be resource limitation and the effects of aboveground vertebrate herbivores. More recently, symbiotic and pathogenic soil microbes have been shown to exert a profound effect on the composition of vegetation and changes therein. However, the influence of invertebrate soil fauna on succession has so far received little attention. Here we report that invertebrate soil fauna might enhance both secondary succession and local plant species diversity. Soil fauna from a series of secondary grassland succession stages selectively suppress early successional dominant plant species, thereby enhancing the relative abundance of subordinate species and also that of species from later succession stages. Soil fauna from the mid-succession stage had the strongest effect. Our results clearly show that soil fauna strongly affects the composition of natural vegetation and we suggest that this knowledge might improve the restoration and conservation of plant species diversity.

Plant-Insect Herbivore Interactions in Elevated Atmospheric CO 2 : Quantitative Analyses and Guild Effects

Interactions between insect herbivores and plants grown under conditions of ambient and elevated CO 2 were investigated by analysing data on 43 herbivores, representing 61 plant-hcrbivore interactions. Changes in herbivore performance in enhanced CO 2 environments were correlated with changes in the quality of the host plants. measured as nitrogen content. water content, carbohydrate content and secondary plant compounds. The data were analysed to determine whether CO 2 mediated effects on insect performance differed between feeding guilds (leaf-chewers. leaf miners, phloem-feeders (root and shoot), xylem-feeders, whole-cell-feeders and seed-caters) or instar stage. Host-plant quality changed in elevated CO 2 ; leaf nitrogen content decreased, on average. by 15% while carbohydrates increased by 47% and secondary plant compounds (phenolics) by 31%. Water content did not change. Of the variables measured changes in nitrogen and carbohydrate levels only were found to be correlated with changes in food consumption. No differences were found in CO 2 -mediated herbivore responses on woody plant compared with non-woody plants. Insects from different feeding guilds respond to CO 2 mediated changes in host-plant quality in various ways. Leaf-chewer generally seem able to compensate for the decreased nitrogen levels in the plant tissues by increasing their food consumption (by 30%) and with no adverse effects on pupal weights. Leaf-miners only slightly increase their food consumption. The negative effect on pupal weight suggests that their population dynamics may change over several generations. Limited data on seed-eaters suggest that enhanced CO 2 conditions have no effect on these insects. Phloem-feeders and whole-cell-feeders are the only insects to show a positive CO 2 response. Population sizes generally increased in elevated CO 2 and development time of phloem-feeders was reduced by 17%. Early instar larvae are restricted more by CO 2 enhancement than late instars. Although changes in food consumption are similar. changes in development times are much more pronounced in young instars (18% vs 6%).

Successful range-expanding plants experience less above-ground and below-ground enemy impact

Many species are currently moving to higher latitudes and altitudes. However, little is known about the factors that influence the future performance of range-expanding species in their new habitats. Here we show that range-expanding plant species from a riverine area were better defended against shoot and root enemies than were related native plant species growing in the same area. We grew fifteen plant species with and without non-coevolved polyphagous locusts and cosmopolitan, polyphagous aphids. Contrary to our expectations, the locusts performed more poorly on the range-expanding plant species than on the congeneric native plant species, whereas the aphids showed no difference. The shoot herbivores reduced the biomass of the native plants more than they did that of the congeneric range expanders. Also, the range-expanding plants developed fewer pathogenic effects in their root-zone soil than did the related native species. Current predictions forecast biodiversity loss due to limitations in the ability of species to adjust to climate warming conditions in their range. Our results strongly suggest that the plants that shift ranges towards higher latitudes and altitudes may include potential invaders, as the successful range expanders may experience less control by above-ground or below-ground enemies than the natives.

Interactions between aboveground and belowground induced responses against phytophages

Abstract Since their discovery about thirty years ago, induced plant responses have mainly been studied in interactions of plants with aboveground (AG) pathogens, herbivores and their natural enemies. Many induced responses, however, are known to be systemic and thus it is likely that responses induced by AG phytophages affect belowground (BG) phytophages feeding on the same plant, and vice versa . The awareness that interactions between AG and BG phytophages may be an important aspect in the evolution of induced responses came only recently and little research has been done to date. In this review we first summarise ecological studies that show how AG phytophages may affect BG phytophages, and vice versa . Then we focus on mechanisms governing interactions between AG and BG induced responses, such as cross-talk between signals. We chose the genus Nicotiana and the family Brassicaceae as two examples of plant groups that have been well studied for their induced responses both AG and BG – but not in concert – and explore how interactions between AG and BG induced compounds may link multitrophic interactions associated with these plants. We propose that future research on AG and BG interactions should focus on: 1). Identification of compounds and signalling pathways involved in AG and BG induced responses and analysis of their interaction mechanisms, 2). Evaluation of how induced responses affect interactions between BG and AG phytophages and their natural enemies, 3). Evaluation of the effects of AG and BG phytophages -in combination with their natural enemies- on plant fitness to identify keystone interactions that are driving the natural selection for induced responses in plants. Seit ihrer Entdeckung vor ca. dreisig Jahren werden induzierte pflanzliche Antworten der Pflanzen zumeist mit solchen Pathogenen, Herbivoren und deren naturlichen Feinden untersucht, die an oberirdischen Pflanzenteilen zu finden sind. Viele induzierte Antworten der Pflanzen konnen aber systemisch sein. Daher ist es wahrscheinlich, dass pflanzliche Antworten, die durch oberirdische Organismen induziert werden, auch solche Phytophagen beeinflussen, die unterirdisch an der Pflanze fressen, und umgekehrt. Das Bewustsein darum, dass Interaktionen zwischen ober- und unterirdischen Phytophagen ein wichtiger Aspekt in der Evolution von induzierten pflanzlichen Abwehrreaktionen sein konnen, kam erst in neuerer Zeit auf. Deshalb gibt es bisher wenig Forschung auf diesem Gebiet. In diesem Uberblick werden zunachst die Studien zusammengefasst, die den Einfluss oberirdischer Phytophager auf die unterirdischen Phytophagen zeigen und umgekehrt. Weiterhin wird auf die Mechanismen fokussiert, die Interaktionen zwischen ober- und unterirdisch fressenden Phytophagen steuern, wie z.B. Wechselwirkungen zwischen Signalen. Die Gattung Nicotiana und die Familie Brassicaceae werden als Modellpflanzen ausgewahlt, an denen die induzierte Abwehr gegen entweder oberirdische oder unterirdische Phytophage – aber nicht gegen beide gleichzeitig – bereits gut untersucht wurde. Es wird analysiert, wie Interaktionen zwischen ober- und unterirdisch induzierten Verbindungen mit multitrophischen Interaktionen dieser Pflanzen in Zusammenhang stehen. Es werden Vorschlage unterbreitet, worauf zukunftige Forschung an ober- und unterirdisch induzierten Interaktionen fokussieren sollte: (1) Identifizierung der Verbindungen und der Signalwege, die bei ober- und unterirdischer Induktion von Bedeutung sind und Analyse der Interaktionsmechanismen, (2) Untersuchung der Frage, wie induzierte Reaktionen der Pflanze sich auf Interaktionen zwischen ober- und unterirdischen Phytophagen und deren naturlichen Feinden auswirken, (3) Analyse der Auswirkungen der Effekte von ober- und unterirdisch fressenden Phytophagen unter Berucksichtigung auch ihrer naturlichen Feinde auf die pflanzliche Fitness, um solche Schlusselinteraktionen zu identifizieren, die entscheidend sind fur die Selektion der induzierten pflanzlichen Reaktion auf Angriffe durch Phytophage.

Long-term effects of elevated CO2 and temperature on populations of the peach potato aphid Myzus persicae and its parasitoid Aphidius matricariae

Abstract Model terrestrial ecosystems were set-up in the Ecotron controlled environment facility. The effects of elevated CO2 (ambient + 200 mol/mol) and temperature (ambient + 2.0°C) on plant chemistry, the abundance of the peach potato aphid Myzus persicae, and on the performance of one of its parasitoids Aphidius matricariae, were studied. Total above-ground plant biomass at the end of the experiment was not affected by elevated atmospheric CO2, nor were foliar nitrogen and carbon concentrations. Elevated temperature decreased final plant biomass while leaf nitrogen concentrations increased. Aphid abundance was enhanced by both the␣CO2 and temperature treatment. Parasitism rates remained unchanged in elevated CO2, but showed an increasing trend in conditions of elevated temperature. Our results suggest that M. persicae, an important pest of many crops, might increase its abundance under conditions of climate change.

The way forward in biochar research: targeting trade-offs between the potential wins

Biochar application to soil is currently widely advocated for a variety of reasons related to sustainability. Typically, soil amelioration with biochar is presented as a multiple‐‘win’ strategy, although it is also associated with potential risks such as environmental contamination. The most often claimed benefits of biochar (i.e. the ‘wins’) include (i) carbon sequestration; (ii) soil fertility enhancement; (iii) biofuel/bioenergy production; (iv) pollutant immobilization; and (v) waste disposal. However, the vast majority of studies ignore possible trade‐offs between them. For example, there is an obvious trade‐off between maximizing biofuel production and maximizing biochar production. Also, relatively little attention has been paid to mechanisms, as opposed to systems impacts, behind observed biochar effects, often leaving open the question as to whether they reflect truly unique properties of biochar as opposed to being simply the short‐term consequences of a fertilization or liming effect. Here, we provide an outline for the future of soil biochar research. We first identify possible trade‐offs between the potential benefits. Second, to be able to better understand and quantify these trade‐offs, we propose guidelines for robust experimental design and selection of appropriate controls that allow both mechanistic and systems assessment of biochar effects and trade‐offs between the wins. Third, we offer a conceptual framework to guide future experiments and suggest guidelines for the standardized reporting of biochar experiments to allow effective between‐site comparisons to quantify trade‐offs. Such a mechanistic and systems framework is required to allow effective comparisons between experiments, across scales and locations, to guide policy and recommendations concerning biochar application to soil.

Impact of foliar herbivory on the development of a root-feeding insect and its parasitoid

The majority of studies exploring interactions between above- and below-ground biota have been focused on the effects of root-associated organisms on foliar herbivorous insects. This study examined the effects of foliar herbivory by Pieris brassicae L. (Lepidoptera: Pieridae) on the performance of the root herbivore Delia radicum L. (Diptera: Anthomyiidae) and its parasitoid Trybliographa rapae (Westwood) (Hymenoptera: Figitidae), mediated through a shared host plant Brassica nigra L. (Brassicaceae). In the presence of foliar herbivory, the survival of D. radicum and T. rapae decreased significantly by more than 50%. In addition, newly emerged adults of both root herbivores and parasitoids were significantly smaller on plants that had been exposed to foliar herbivory than on control plants. To determine what factor(s) may have accounted for the observed results, we examined the effects of foliar herbivory on root quantity and quality. No significant differences in root biomass were found between plants with and without shoot herbivore damage. Moreover, concentrations of nitrogen in root tissues were also unaffected by shoot damage by P. brassicae larvae. However, higher levels of indole glucosinolates were measured in roots of plants exposed to foliar herbivory, suggesting that the development of the root herbivore and its parasitoid may be, at least partly, negatively affected by increased levels of these allelochemicals in root tissues. Our results show that foliar herbivores can affect the development not only of root-feeding insects but also their natural enemies. We argue that such indirect interactions between above- and below-ground biota may play an important role in the structuring and functioning of communities.

Development of the solitary endoparasitoid Microplitis demolitor: host quality does not increase with host age and size

Abstract.  1. Many studies examining the relationship between host size, an index of host quality, and parasitoid fitness use development time and/or adult parasitoid size as currencies of fitness, while ignoring pre‐adult mortality. Because the physiological suitability of the host may vary in different stages, sizes, or ages of hosts, a misleading picture of host quality may therefore be obtained in cases where fitness is based on only one or two developmental traits.

Climate vs. soil factors in local adaptation of two common plant species

Evolutionary theory suggests that divergent natural selection in heterogeneous environments can result in locally adapted plant genotypes. To understand local adaptation it is important to study the ecological factors responsible for divergent selection. At a continental scale, variation in climate can be important while at a local scale soil properties could also play a role. We designed an experiment aimed to disentangle the role of climate and (abiotic and biotic) soil properties in local adaptation of two common plant species. A grass (Holcus lanatus) and a legume (Lotus corniculatus), as well as their local soils, were reciprocally transplanted between three sites across an Atlantic-Continental gradient in Europe and grown in common gardens in either their home soil or foreign soils. Growth and reproductive traits were measured over two growing seasons. In both species, we found significant environmental and genetic effects on most of the growth and reproductive traits and a significant interaction between the two environmental effects of soil and climate. The grass species showed significant home site advantage in most of the fitness components, which indicated adaptation to climate. We found no indication that the grass was adapted to local soil conditions. The legume showed a significant home soil advantage for number of fruits only and thus a weak indication of adaptation to soil and no adaptation to climate. Our results show that the importance of climate and soil factors as drivers of local adaptation is species-dependent. This could be related to differences in interactions between plant species and soil biota.