Plant–microbe interactions change along a tallgrass prairie restoration chronosequence

Soil microbial communities are critical in determining the performance and density of species in plant communities. However, their role in regulating the success of restorations is much less clear. This study assessed the ability of soil microbial communities to regulate the growth and performance of two potentially dominant grasses and two common forbs in tallgrass prairie restorations. Specifically, we examined the effects of soil microbial communities along a restoration chronosequence from agricultural fields to remnant prairies using experimentally inoculated soils. The two grass species, Andropogon gerardii and Sorghastrum nutans, grew best with the agricultural inoculates and experienced a decline in performance in later stages of the chronosequence, indicating that the microbial community shifted from being beneficial to grasses in the early stages to inhibiting grasses in the later stages of restoration. Growth of the forb, Silphium terebinthinaceum, varied little with inoculation or position along the restoration chronosequence. Growth of Baptisia leucantha, a legume, appeared limited by nodule formation in agricultural soils, peaked in young restoration soils along with nodule formation, but decreased in older soils as the microbial community became more antagonistic. Overall, negative feedbacks tended to be less important early in restoration, but appeared important in remnant and older restored prairies. Our results provide evidence that it may be advantageous for management practices to take negative soil feedbacks into consideration when trying to recreate the diversity of tallgrass prairies.     

Plant–pollinator population dynamics

We formulate and analyze a multi-generation population dynamics model for pollinators’ mutualism with plants. The centerpiece of our model is an analytical expression for population-level plant–pollinator interactions extrapolated from a model of individual-level flowers and bees interactions. We also show that this analytical expression can be productively approximated by the Beddington–DeAngelis formula—a function used to model trophic interactions in mathematical ecology.     

Plant–pollinator community network response to species invasion depends on both invader and community characteristics

The effect of an invasive species on the species richness of its host community can range from catastrophic to negligible to beneficial. Here, we use a network model of plant–pollinator community formation to consider the influence of invader and invasion‐related properties (including physical characteristics, assignment and type of interacting partners, and number of independent introductions of the species into the community) and community properties (including connectance and nestedness) on the outcome of an invasion. As expected from empirical work, invaders with properties atypical of the regional species pool drive the strongest changes in species richness. However, we find that an increase in species richness corresponds to an increase in the community's spectral nestedness coupled with a decrease in connectance. While such a response has been observed in real invaded systems, these results differ from previous theoretical studies in which these two measures respond in a similar way outside the context of species invasions.     

Plant–pollinator interactions: comparison between an invasive and a native congeneric species

Plant–pollinator interactions determine reproductive success for animal-pollinated species and, in the case of invasive plants, they are supposed to play an important role in invasive success. We compared the invasive Senecio inaequidens to its native congener S. jacobaea in terms of interactions with pollinators. Visitor guild, visitation rate, and seed set were compared over 3 years in three sites in Belgium. Floral display (capitula number and arrangement) and phenology were quantified, and visiting insects were individually censused, i.e. number of visited capitula and time per visited capitulum. As expected from capitula resemblance, visitor guilds of both species were very similar (proportional similarity = 0.94). Senecio inaequidens was visited by 33 species, versus 36 for S. jacobaea. For both species, main visitors were Diptera, especially Syrphidae, and Hymenoptera. Visitation rate averaged 0.13 visitor per capitulum per 10 min for S. inaequidens against 0.08 for S. jacobaea. However, insects visited more capitula per plant on S. jacobaea, due to high capitula density (886 m⁻² versus 206 m⁻² for S. inaequidens), which is likely to increase self-pollen deposition considerably. Seed set of S. jacobaea was lower than that of S. inaequidens. We suggest that floral display is the major factor explaining the differences in insect visitation and seed set between the two Senecio species.     

Inferring coevolution in a plant–pollinator network

Mutualistic interactions are at the core of community dynamics, determining dispersal, colonization and differential survival and reproduction among individuals and species. Mutualistic interactions therefore affect the fitness of interaction partners, hence modifying their respective evolutionary trajectories reciprocally, potentially leading to coevolution. Although mathematical models predict coevolution in mutualistic interaction networks, no empirical data are available. By taking into account the patterns of interactions and reconstructing evolutionary change in plant and pollinator traits, we tested the hypothesis that coevolution occurs between plants and insects that interact more frequently, or more symmetrically. To test this hypothesis, we built an interaction network with data from five flowering seasons, measured plant and insect morphology, mapped morphology on the plant and insect phylogenies, and reconstructed ancestral character changes based on maximum parsimony. We calculated an index, called the coevolutionary ratio, which represents the amount of correlated change in traits that mediate the interaction between plants and pollinators (i.e. proboscis versus corolla length, and body width and corolla aperture). Our results suggest that high frequency of interaction, i.e. the number of times two species interact, does not lead to coevolution. Instead, symmetry of interaction strength, i.e. the reciprocal similarity in the mutual effect of interaction partners, may lead to coevolution, in spite of a pervasive lack of reciprocal specialization and high interaction frequency. Although the statistical signal is quite weak, our results hold for three statistical tests of very different nature. The most specialized species, expected to be under directional selection, do not show more evolutionary change than do generalist species, expected to be under different, perhaps opposing, selective pressures. By dissecting the complexity of an interaction network we show that coevolution may partially shape functional morphology of interaction partners, thus providing the closest evidence to date of mutualistic adaptation of organisms within a community.     

Shifts in desulfonating bacterial communities along a soil chronosequence in the forefield of a receding glacier

Forefields of receding glaciers are unique and sensitive environments representing natural soil chronosequences, where sulfate availability is assumed to be a limiting factor. Bacterial mineralization of organosulfur is an important sulfate-providing process in soils. We analyzed the diversity of sulfonate-desulfurizing (desulfonating) bacteria in the Damma glacier forefield on the basis of the key gene asfA by terminal restriction fragment length polymorphism and clone libraries. The community structure and sequence diversity of desulfonating bacteria differed significantly between forefield soils deglaciated in the 1990s and the 1950s. Soil age had a strong effect on the desulfonating rhizosphere communities of Agrostis rupestris , but only a slight impact on the ones from Leucanthemopsis alpina . AsfA affiliated to Polaromonas sp. was predominantly found in the more recent ice-free soils and the corresponding rhizospheres of A. rupestris , while a group of unidentified sequences was found to be dominating the matured soils and the corresponding rhizospheres of A. rupestris . The desulfonating bacterial diversity was not affected by varying levels of sulfate concentrations. The level of asfA diversity in recently deglaciated soils suggests that desulfonating bacteria are a critical factor in sulfur cycling, with defined groups dominating at different stages of soil formation.     

Abundances and potential activities of nitrogen cycling microbial communities along a chronosequence of a glacier forefield

Glacier forefields are ideal ecosystems to study the development of nutrient cycles as well as single turnover processes during soil development. In this study, we examined the ecology of the microbial nitrogen (N) cycle in bulk soil samples from a chronosequence of the Damma glacier, Switzerland. Major processes of the N cycle were reconstructed on the genetic as well as the potential enzyme activity level at sites of the chronosequence that have been ice-free for 10, 50, 70, 120 and 2000 years. In our study, we focused on N fixation, mineralization (chitinolysis and proteolysis), nitrification and denitrification. Our results suggest that mineralization, mainly the decomposition of deposited organic material, was the main driver for N turnover in initial soils, that is, ice-free for 10 years. Transient soils being ice-free for 50 and 70 years were characterized by a high abundance of N fixing microorganisms. In developed soils, ice-free for 120 and 2000 years, significant rates of nitrification and denitrification were measured. Surprisingly, copy numbers of the respective functional genes encoding the corresponding enzymes were already high in the initial phase of soil development. This clearly indicates that the genetic potential is not the driver for certain functional traits in the initial phase of soil formation but rather a well-balanced expression of the respective genes coding for selected functions.     

Climate‐sensitive ecosystem carbon dynamics along the soil chronosequence of the Damma glacier forefield,Switzerland

We performed a detailed study on the carbon build‐up over the 140‐year‐long chronosequence of the Damma glacier forefield, Switzerland, to gain insights into the organic carbon dynamics during the initial stage of soil formation and ecosystem development. We determined soil carbon and nitrogen contents and their stable isotopic compositions, as well as molecular‐level composition of the bulk soils, and recalcitrance parameters of carbon in different fractions. The chronosequence was divided into three age groups, separated by small end moraines that resulted from two glacier re‐advances. The net ecosystem carbon balance (NECB) showed an exponential increase over the last decades, with mean annual values that range from 100 g C m^?2 yr^?1 in the youngest part to over 300 g C m^?2 yr^?1 in a 60–80 years old part. However, over the entire 140‐year chronosequence, the NECB is only 20 g C m^?2 yr^?1, similar to results of other glacier forefield studies. The difference between the short‐ and long‐term NECB appears to be caused by reductions in ecosystem carbon (EC) accumulation during periods with a colder climate. We propose that two complementary mechanisms have been responsible: 1) Reductions in net primary productivity down to 50% below the long‐term mean, which we estimated using reconstructed effective temperature sums. 2) Disturbance of sites near the terminus of the re‐advanced glacier front. Stabilization of soil organic matter appeared to play only a minor role in the coarse‐grained forefield. We conclude that the forefield ecosystem, especially primary productivity, reacts rapidly to climate changes. The EC gained at warm periods is easily lost again in a cooling climate. Our conclusions may also be valid for other high mountain ecosystems and possibly arctic ecosystems.     

Variations in soil culturable bacteria communities and biochemical characteristics in the Dongkemadi glacier forefield along a chronosequence

The variations in the soil culturable bacterial communities and biochemical parameters of early successional soils from a receding glacier in the Tanggula Mountain were investigated. We examined low organic carbon (C) and nitrogen (N) contents and enzymatic activity, correlated with fewer bacterial groups and numbers in the glacier forefield soils. The soil pH values decreased, but the soil water content, organic C and total N significantly increased, along the chronosequence. The soil C/N ratio decreased in the early development soils and increased in the late development soils and it did not correlate with the soil age since deglaciation. The activities of soil urease, sucrase, protease, polyphenol oxidase, catalase, and dehydrogenase increased along the chronosequence. The numbers of culturable bacteria in the soils increased as cultured at 25°C while decreased at 4°C from younger soils to older soils. Total numbers of culturable bacteria in the soils cultured at 25°C were significantly positively correlated to the soil total N, organic C, and soil water content, as well as the activities of soil urease, sucrase, dehydrogenase, catalase, and polyphenol oxidase. We have obtained 224 isolates from the glacier forefield soils. The isolates were clustered into 28 groups by amplified ribosomal DNA restriction analysis (ARDRA). Among them, 27 groups and 25 groups were obtained from the soils at 25°C and at 4°C incubation temperatures, respectively. These groups are affiliated with 18 genera that belong to six taxa, viz, Actinobacteria, Gammaproteobacteria, Bacteroidetes, Firmicutes, Alphaproteobacteria, and Betaproteobacteria. The dominant taxa were Actinobacteria, Gammaproteobacteria, and Bacteroidetes in all the samples. The abundance and the diversity of the genera isolated at 25°C incubation temperature were greater than that at 4°C.     

Plant–mycorrhizal fungus co‐occurrence network lacks substantial structure

The interactions between plants and arbuscular mycorrhizal fungi (AMF) maintain a crucial link between macroscopic organisms and the soil microbial world. These interactions are of extreme importance for the diversity of plant communities and ecosystem functioning. Despite this importance, only recently has the structure of plant–AMF interaction networks been studied. These recent studies, which used genetic data, suggest that these networks are highly structured, very similar to plant–animal mutualistic networks. However, the assembly process of plant–AMF communities is still largely unknown, and an important feature of plant–AMF interactions has not been incorporated: they occur at an extremely localized scale. Studying plant–AMF networks in a spatial context seems therefore a crucial step. This paper studies a plant–AMF spatial co‐occurrence network using novel methodology based on information theory and a unique set of spatially explicit species‐level data. We apply three null models of which only one accounts for spatial effects. We find that the data show substantial departures from null expectations for the two non‐spatial null models. However, for the null model considering spatial effects, there are few significant co‐occurrences compared with the other two null models. Thus, plant–AMF spatial co‐occurrences seem to be mostly explained by stochasticity, with a small role for other factors related to plant–AMF specialization. Furthermore, we find that the network is not significantly nested or modular. We conclude that this plant–AMF spatial co‐occurrence network lacks substantial structure and, therefore, plants and AMF species do not track each other over space. Thus, random encounters seem more important in the first step of the assembly of plant–AMF communities. Synthesis The symbiotic interaction between plants and arbuscular mycorrhizal fungi (AMF) is crucial for ecosystem functioning. However, the factors affecting the assembly of plant‐AMF communities are poorly understood. An important factor of the assembly of plant‐AMF communities has been overlooked: plant‐AMF interactions occur at a localized spatial scale. Our study investigated the importance of space in the structure of plant‐AMF communities. We studied a plant‐AMF spatial co‐occurrence network using a unique set of spatially explicit data and applied three null models. We found that plant‐AMF spatial co‐occurrences seem to be mostly explained by stochasticity. In particular, our study shows that this plant‐AMF spatial co‐occurrence network lacks substantial structure and, therefore, plants and AMF species do not track each other over space. Thus, random encounters seem to drive the assembly of plant‐AMF communities.     

Plant–soil feedbacks of forest understorey plants transplanted in nonlocal soils along a latitudinal gradient

• Climate change is driving movements of many plants beyond, as well as within, their current distributional ranges. Even migrant plants moving within their current range may experience different plant–soil feedbacks (PSF) because of divergent nonlocal biotic soil conditions. Yet, our understanding to what extent soil biotic conditions can affect the performance of within‐range migrant plants is still very limited.
• We assessed the emergence and growth of migrant forest herbs (Milium effusum and Stachys sylvatica) using soils and seeds collected along a 1,700 km latitudinal gradient across Europe. Soil biota were manipulated through four soil treatments, i.e. unsterilized control soil (PSF_US), sterilized soil (PSF_S), sterilized soil inoculated with unsterilized home soil (PSF_S+HI) and sterilized soil inoculated with unsterilized foreign soil (PSF_S+FI, expected to occur when both plants and soil biota track climate change).
• Compared to PSF_S, PSF_US had negative effects on the growth but not emergence of both species, while PSF_S+FI only affected S. sylvatica across all seed provenances. When considering seed origin, seedling emergence and growth responses to nonlocal soils depended on soil biotic conditions. Specifically, the home–away distance effect on seedling emergence differed between the four treatments, and significant responses to chemistry either disappeared (M. effusum) or changed (S. sylvatica) from PSF_US to PSF_S.
• Soil biota emerge as an important driver of the estimated plant migration success. Our results of the effects of soil microorganisms on plant establishment provide relevant information for predictions of the distribution and dynamics of plant species in a changing climate.

     

Spatial structure of an individual‐based plant–pollinator network

The influence of space on the structure (e.g. modularity) of complex ecological networks remains largely unknown. Here, we sampled an individual‐based plant–pollinator network by following the movements and flower visits of marked bumblebee individuals within a population of thistle plants for which the identities and spatial locations of stems were mapped in a 50 × 50 m study plot. The plant–pollinator network was dominated by parasitic male bumblebees and had a significantly modular structure, with four identified modules being clearly separated in space. This indicated that individual flower visitors opted for the fine‐scale division of resources, even within a local site. However, spatial mapping of network modules and movements of bumblebee individuals also showed an overlap in the dense center of the plant patch. Model selection based on Akaike information criterion with traits as predictor variables revealed that thistle stems with high numbers of flower heads and many close neighbours were particularly important for connecting individuals within the modules. In contrast, tall plants and those near the patch center were crucial for connecting the different modules to each other. This demonstrated that individual‐based plant–pollinator networks are influenced by both the spatial structure of plant populations and individual‐specific plant traits. Additionally, bumblebee individuals with long observation times were important for both the connectivity between and within modules. The latter suggests that bumblebee individuals will still show locally restricted movements within sub‐patches of plant populations even if they are observed over a prolonged time period. Our individual‐based and animal‐centered approach of sampling ecological networks opens up new avenues for incorporating foraging behaviour and intra‐specific trait variation into analyses of plant–animal interactions across space.     

Year‐to‐year variation in the topology of a plant–pollinator interaction network

Vigorous discussion of the degree of specialization in pollination interactions, combined with advances in the analysis of complex networks, has revitalized the study of entire plant–pollinator communities. Noticeably rare, however, are attempts to quantify temporal variation in the structure of plant–pollinator networks, and to determine whether the status of species as specialists or generalists is stable. Here we show that network structure varied through time in a montane meadow community from southern California, USA, in that pollinator species did not form the same links with plant species across years. Furthermore, composition of the generalized core group of species in the network varied among summers, as did the identity of those species involved in relationships that appeared to be reciprocally specialized within any one summer. These differences appear to be related to severe drought conditions experienced in the second summer of the 3 year study. In contrast to this variation, the pollinator community remained similarly highly nested in all three summers, even though species were packed into the nested matrix differently from year to year. These results suggest that plant–pollinator networks vary in detail through time, while retaining some basic topological properties. This dynamic aspect of community‐scale interactions has implications for both ecological and evolutionary inferences about pollination mutualisms.     

Plant–Plant and Plant–Topography Interactions on a Rock Outcrop at High Altitude in Southeastern Brazil1

Plant establishment and growth on rocky outcrops in the Itatiaia massif (2400 m a.s.l.), southeastern Brazil, are limited by lack of soil and by freezing temperatures in winter nights. Mat‐forming species of different sizes and shapes on bare rock provide substrate for other plants to establish. The habitat preference of two geophytes, Stevia camporum (Asteraceae) and Alstroemeria foliosa (Alstroemeriaceae), was compared with regard to their association with the type of mat species and distinct rock topographies. The habitat preference of the mat species in regard to topography was also assessed. We found 1706 ramets of S. camporum and 1317 of A. foliosa in 253 vegetation islands ranging in size from 0.005 to 18.097 m². Mat species in these islands were Fernseea itatiaiae, Vriesea itatiaiae (both Bromeliaceae), Pleurostima gounelleana (Velloziaceae) and/or Campylopus pilifer (Dicranaceae) and other mosses. Mat species were segregated by topography. Geophytes were similarly distributed across types of topography but showed negative interspecific association. S. camporum occurred mostly on the moss‐dominated islands, whereas A. foliosa was more common in P. gounelleana islands. We found geophyte co‐occurrence in larger vegetation islands containing both P. gounelleana and mosses as mat species. Thus, the effect of topography on geophyte segregation was indirect, since topography affects mat species distribution, and the geophyte preference for distinct mat species as substrate resulted in their segregation.     

Plant–pollinator networks in semi‐natural grasslands are resistant to the loss of pollinators during blooming of mass‐flowering crops

Mass‐flowering crops lead to spatial redistributions of pollinators and to transient shortages within nearby semi‐natural grasslands, but the impacts on plant–pollinator interactions remain largely unexplored. Here, we characterised which pollinator species are attracted by oilseed rape and how this affected the structure of plant–pollinator networks in nearby grasslands. We surveyed 177 networks from three countries (Germany, Sweden and United Kingdom) in 24 landscapes with high crop cover, and compared them to 24 landscapes with low or no oilseed rape during and after crop blooming. On average 55% of grassland pollinator species were found on the crop, which attracted 8–35% of individuals away from grasslands. However, networks in the grasslands were resistant to these reductions, since mainly abundant and highly mobile species were attracted. Nonetheless, simulations indicated that network structural changes could be triggered if > 50% of individuals were attracted to the crop (a value well‐above that found in our study system), which could affect community stability and resilience to further disturbance.     

Changes in the structure and heterogeneity of vegetation and microsite environments with the chronosequence of primary succession on a glacier foreland in Ellesmere Island, high arctic Canada

Primary plant succession was investigated on a well-vegetated glacier foreland on Ellesmere Island in high arctic Canada. A field survey was carried out on four glacier moraines differing in time after deglaciation to assess vegetation development and microsite modification in the chronosequence of succession. The results showed evidence of directional succession without species replacement, which is atypical in the high arctic, reflecting the exceptionally long time vegetation development. During this successional process, Salix arctica dominated throughout all moraines. The population structures of S. arctica on these moraines implied the population growth of this species with progressing succession. The population density of S. arctica reflected the abundance of vascular plants, suggesting that development of the plant community might be related to structural changes and the growth of constituting populations. Through such growths of the population and the whole community with progressing succession, the spatial heterogeneity of vegetation gradually declines. Moreover, this vegetation homogenization is accompanied by changes in the spatial heterogeneity of microsite environments, suggesting significant plant effects on the modification of microsite environments. Accordingly, it was concluded that the directional primary succession observed on this glacier foreland is characterized by the initial sporadic colonization of plants, subsequent population growths, and the community assembly of vascular plants, accompanied by microsite modification.