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Long-term bacteria-fungi-plant associations in permafrost soils inferred from palaeometagenomics
(2024)
The arctic is warming 2 – 4 times faster than the global average, resulting in a strong feedback on northern ecosystems such as boreal forests, which cover a vast area of the high northern latitudes. With ongoing global warming, the treeline subsequently migrates northwards into tundra areas. The consequences of turning ecosystems are complex: on the one hand, boreal forests are storing large amounts of global terrestrial carbon and act as a carbon sink, dragging carbon dioxide out of the global carbon cycle, suggesting an enhanced carbon uptake with increased tree cover. On the other hand, with the establishment of trees, the albedo effect of tundra decreases, leading to enhanced soil warming. Meanwhile, permafrost thaws, releasing large amounts of previously stored carbon into the atmosphere. So far, mainly vegetation dynamics have been assessed when studying the impact of warming onto ecosystems. Most land plants are living in close symbiosis with bacterial and fungal communities, sustaining their growth in nutrient poor habitats. However, the impact of climate change on these subsoil communities alongside changing vegetation cover remains poorly understood. Therefore, a better understanding of soil community dynamics on multi millennial timescales is inevitable when addressing the development of entire ecosystems. Unravelling long-term cross-kingdom dependencies between plant, fungi, and bacteria is not only a milestone for the assessment of warming on boreal ecosystems. On top, it also is the basis for agriculture strategies to sustain society with sufficient food in a future warming world.
The first objective of this thesis was to assess ancient DNA as a proxy for reconstructing the soil microbiome (Manuscripts I, II, III, IV). Research findings across these projects enable a comprehensive new insight into the relationships of soil microorganisms to the surrounding vegetation. First, this was achieved by establishing (Manuscript I) and applying (Manuscript II) a primer pair for the selective amplification of ancient fungal DNA from lake sediment samples with the metabarcoding approach. To assess fungal and plant co-variation, the selected primer combination (ITS67, 5.8S) amplifying the ITS1 region was applied on samples from five boreal and arctic lakes. The obtained data showed that the establishment of fungal communities is impacted by warming as the functional ecological groups are shifting. Yeast and saprotroph dominance during the Late Glacial declined with warming, while the abundance of mycorrhizae and parasites increased with warming. The overall species richness was also alternating. The results were compared to shotgun sequencing data reconstructing fungi and bacteria (Manuscripts III, IV), yielding overall comparable results to the metabarcoding approach. Nonetheless, the comparison also pointed out a bias in the metabarcoding, potentially due to varying ITS lengths or copy numbers per genome.
The second objective was to trace fungus-plant interaction changes over time (Manuscripts II, III). To address this, metabarcoding targeting the ITS1 region for fungi and the chloroplast P6 loop for plants for the selective DNA amplification was applied (Manuscript II). Further, shotgun sequencing data was compared to the metabarcoding results (Manuscript III). Overall, the results between the metabarcoding and the shotgun approaches were comparable, though a bias in the metabarcoding was assumed. We demonstrated that fungal shifts were coinciding with changes in the vegetation. Yeast and lichen were mainly dominant during the Late Glacial with tundra vegetation, while warming in the Holocene lead to the expansion of boreal forests with increasing mycorrhizae and parasite abundance. Aside, we highlighted that Pinaceae establishment is dependent on mycorrhizal fungi such as Suillineae, Inocybaceae, or Hyaloscypha species also on long-term scales.
The third objective of the thesis was to assess soil community development on a temporal gradient (Manuscripts III, IV). Shotgun sequencing was applied on sediment samples from the northern Siberian lake Lama and the soil microbial community dynamics compared to ecosystem turnover. Alongside, podzolization processes from basaltic bedrock were recovered (Manuscript III). Additionally, the recovered soil microbiome was compared to shotgun data from granite and sandstone catchments (Manuscript IV, Appendix). We assessed if the establishment of the soil microbiome is dependent on the plant taxon and as such comparable between multiple geographic locations or if the community establishment is driven by abiotic soil properties and as such the bedrock area. We showed that the development of soil communities is to a great extent driven by the vegetation changes and temperature variation, while time only plays a minor role. The analyses showed general ecological similarities especially between the granite and basalt locations, while the microbiome on species-level was rather site-specific. A greater number of correlated soil taxa was detected for deep-rooting boreal taxa in comparison to grasses with shallower roots. Additionally, differences between herbaceous taxa of the late Glacial compared to taxa of the Holocene were revealed.
With this thesis, I demonstrate the necessity to investigate subsoil community dynamics on millennial time scales as it enables further understanding of long-term ecosystem as well as soil development processes and such plant establishment. Further, I trace long-term processes leading to podzolization which supports the development of applied carbon capture strategies under future global warming.
Keeping cool on hot days
(2023)
Long-lived organisms are likely to respond to a rapidly changing climate with behavioral flexibility. Animals inhabiting the arid parts of southern Africa face a particularly rapid rise in temperature which in combination with food and water scarcity places substantial constraints on the ability of animals to tolerate heat. We investigated how three species of African antelope-springbok Antidorcas marsupialis, kudu Tragelaphus strepsiceros and eland T. oryx-differing in body size, habitat preference and movement ecology, change their activity in response to extreme heat in an arid savanna. Serving as a proxy for activity, dynamic body acceleration data recorded every five minutes were analyzed for seven to eight individuals per species for the three hottest months of the year. Activity responses to heat during the hottest time of day (the afternoons) were investigated and diel activity patterns were compared between hot and cool days. Springbok, which prefer open habitat, are highly mobile and the smallest of the species studied, showed the greatest decrease in activity with rising temperature. Furthermore, springbok showed reduced mean activity over the 24 h cycle on hot days compared to cool days. Large-bodied eland seemed less affected by afternoon heat than springbok. While eland also reduced diurnal activity on hot days compared to cool days, they compensated for this by increasing nocturnal activity, possibly because their predation risk is lower. Kudu, which are comparatively sedentary and typically occupy shady habitat, seemed least affected during the hottest time of day and showed no appreciable difference in diel activity patterns between hot and cool days. The interplay between habitat preference, body size, movement patterns, and other factors seems complex and even sub-lethal levels of heat stress have been shown to impact an animal's long-term survival and reproduction. Thus, differing heat tolerances among species could result in a shift in the composition of African herbivore communities as temperatures continue to rise, with significant implications for economically important wildlife-based land use and conservation.
Animal movement is a crucial aspect of life, influencing ecological and evolutionary processes. It plays an important role in shaping biodiversity patterns, connecting habitats and ecosystems. Anthropogenic landscape changes, such as in agricultural environments, can impede the movement of animals by affecting their ability to locate resources during recurring movements within home ranges and, on a larger scale, disrupt migration or dispersal. Inevitably, these changes in movement behavior have far-reaching consequences on the mobile link functions provided by species inhabiting such extensively altered matrix areas. In this thesis, I investigate the movement characteristics and activity patterns of the European hare (Lepus europaeus), aiming to understand their significance as a pivotal species in fragmented agricultural landscapes. I reveal intriguing results that shed light on the importance of hares for seed dispersal, the influence of personality traits on behavior and space use, the sensitivity of hares to extreme weather conditions, and the impacts of GPS collaring on mammals' activity patterns and movement behavior.
In Chapter I, I conducted a controlled feeding experiment to investigate the potential impact of hares on seed dispersal. By additionally utilizing GPS data of hares in two contrasting landscapes, I demonstrated that hares play a vital role, acting as effective mobile linkers for many plant species in small and isolated habitat patches. The analysis of seed intake and germination success revealed that distinct seed traits, such as density, surface area, and shape, profoundly affect hares' ability to disperse seeds through endozoochory. These findings highlight the interplay between hares and plant communities and thus provide valuable insights into seed dispersal mechanisms in fragmented landscapes.
By employing standardized behavioral tests in Chapter II, I revealed consistent behavioral responses among captive hares while simultaneously examining the intricate connection between personality traits and spatial patterns within wild hare populations. This analysis provides insights into the ecological interactions and dynamics within hare populations in agricultural habitats. Examining the concept of animal personality, I established a link between personality traits and hare behavior. I showed that boldness, measured through standardized tests, influences individual exploration styles, with shy and bold hares exhibiting distinct space use patterns. In addition to providing valuable insights into the role of animal personality in heterogeneous environments, my research introduced a novel approach demonstrating the feasibility of remotely assessing personality types using animal-borne sensors without additional disturbance of the focal individual.
While climate conditions severely impact the activity and, consequently, the fitness of wildlife species across the globe, in Chapter III, I uncovered the sensitivity of hares to temperature, humidity, and wind speed during their peak reproduction period. I found a strong response in activity to high temperatures above 25°C, with a particularly pronounced effect during temperature extremes of over 35°C. The non-linear relationship between temperature and activity was characterized by contrasting responses observed for day and night. These findings emphasize the vulnerability of hares to climate change and the potential consequences for their fitness and population dynamics with the ongoing rise of temperature.
Since such insights can only be obtained through capturing and tagging free-ranging animals, I assessed potential impacts and the recovery process post-collar attachment in Chapter IV. For this purpose, I examined the daily distances moved and the temporal-associated activity of 1451 terrestrial mammals out of 42 species during their initial tracking period. The disturbance intensity and the speed of recovery varied across species, with herbivores, females, and individuals captured and collared in relatively secluded study areas experiencing more pronounced disturbances due to limited anthropogenic influences.
Mobile linkers are essential for maintaining biodiversity as they influence the dynamics and resilience of ecosystems. Furthermore, their ability to move through fragmented landscapes makes them a key component for restoring disturbed sites. Individual movement decisions determine the scale of mobile links, and understanding variations in space use among individuals is crucial for interpreting their functions. Climate change poses further challenges, with wildlife species expected to adjust their behavior, especially in response to high-temperature extremes, and comprehending the anthropogenic influence on animal movements will remain paramount to effective land use planning and the development of successful conservation strategies.
This thesis provides a comprehensive ecological understanding of hares in agricultural landscapes. My research findings underscore the importance of hares as mobile linkers, the influence of personality traits on behavior and spatial patterns, the vulnerability of hares to extreme weather conditions, and the immediate consequences of collar attachment on mammalian movements. Thus, I contribute valuable insights to wildlife conservation and management efforts, aiding in developing strategies to mitigate the impact of environmental changes on hare populations. Moreover, these findings enable the development of methodologies aimed at minimizing the impacts of collaring while also identifying potential biases in the data, thereby benefiting both animal welfare and the scientific integrity of localization studies.
Climate change of anthropogenic origin is affecting Earth’s biodiversity and therefore ecosystems and their services. High latitude ecosystems are even more impacted than the rest of Northern Hemisphere because of the amplified polar warming. Still, it is challenging to predict the dynamics of high latitude ecosystems because of complex interaction between abiotic and biotic components. As the past is the key to the future, the interpretation of past ecological changes to better understand ongoing processes is possible. In the Quaternary, the Pleistocene experienced several glacial and interglacial stages that affected past ecosystems. During the last Glacial, the Pleistocene steppe-tundra was covering most of unglaciated northern hemisphere and disappeared in parallel to the megafauna’s extinction at the transition to the Holocene (~11,700 years ago). The origin of the steppe-tundra decline is not well understood and knowledge on the mechanisms, which caused shifts in past communities and ecosystems, is of high priority as they are likely comparable to those affecting modern ecosystems. Lake or permafrost core sediments can be retrieved to investigate past biodiversity at transitions between glacial and interglacial stages. Siberia and Beringia were the origin of dispersal of the steppe-tundra, which make investigation this area of high priority. Until recently, macrofossils and pollen were the most common approaches. They are designed to reconstruct past composition changes but have limit and biases. Since the end of the 20th century, sedimentary ancient DNA (sedaDNA) can also be investigated. My main objectives were, by using sedaDNA approaches to provide scientific evidence of compositional and diversity changes in the Northern Hemisphere ecosystems at the transition between Quaternary glacial and interglacial stages.
In this thesis, I provide snapshots of entire ancient ecosystems and describe compositional changes between Quaternary glacial and interglacial stages, and confirm the vegetation composition and the spatial and temporal boundaries of the Pleistocene steppe-tundra. I identify a general loss of plant diversity with extinction events happening in parallel of megafauna’ extinction. I demonstrate how loss of biotic resilience led to the collapse of a previously well-established system and discuss my results in regards to the ongoing climate change. With further work to constrain biases and limits, sedaDNA can be used in parallel or even replace the more established macrofossils and pollen approaches as my results support the robustness and potential of sedaDNA to answer new palaeoecological questions such as plant diversity changes, loss and provide snapshots of entire ancient biota.
The heat is on
(2023)
Climate conditions severely impact the activity and, consequently, the fitness of wildlife species across the globe. Wildlife can respond to new climatic conditions, but the pace of human-induced change limits opportunities for adaptation or migration. Thus, how these changes affect behavior, movement patterns, and activity levels remains unclear. In this study, we investigate how extreme weather conditions affect the activity of European hares (Lepus europaeus) during their peak reproduction period. When hares must additionally invest energy in mating, prevailing against competitors, or lactating, we investigated their sensitivities to rising temperatures, wind speed, and humidity. To quantify their activity, we used the overall dynamic body acceleration (ODBA) calculated from tri-axial acceleration measurements of 33 GPS-collared hares. Our analysis revealed that temperature, humidity, and wind speed are important in explaining changes in activity, with a strong response for high temperatures above 25 & DEG;C and the highest change in activity during temperature extremes of over 35 & DEG;C during their inactive period. Further, we found a non-linear relationship between temperature and activity and an interaction of activity changes between day and night. Activity increased at higher temperatures during the inactive period (day) and decreased during the active period (night). This decrease was strongest during hot tropical nights. At a stage of life when mammals such as hares must substantially invest in reproduction, the sensitivity of females to extreme temperatures was particularly pronounced. Similarly, both sexes increased their activity at high humidity levels during the day and low wind speeds, irrespective of the time of day, while the effect of humidity was stronger for males. Our findings highlight the importance of understanding the complex relationships between extreme weather conditions and mammal behavior, critical for conservation and management. With ongoing climate change, extreme weather events such as heat waves and heavy rainfall are predicted to occur more often and last longer. These events will directly impact the fitness of hares and other wildlife species and hence the population dynamics of already declining populations across Europe.
In many species, dispersal is decisive for survival in a changing climate. Simulation models for population dynamics under climate change thus need to account for this factor. Moreover, large numbers of species inhabiting agricultural landscapes are subject to disturbances induced by human land use. We included dispersal in the HiLEG model that we previously developed to study the interaction between climate change and agricultural land use in single populations. Here, the model was parameterized for the large marsh grasshopper (LMG) in cultivated grasslands of North Germany to analyze (1) the species development and dispersal success depending on the severity of climate change in subregions, (2) the additional effect of grassland cover on dispersal success, and (3) the role of dispersal in compensating for detrimental grassland mowing. Our model simulated population dynamics in 60-year periods (2020-2079) on a fine temporal (daily) and high spatial (250 x 250 m(2)) scale in 107 subregions, altogether encompassing a range of different grassland cover, climate change projections, and mowing schedules. We show that climate change alone would allow the LMG to thrive and expand, while grassland cover played a minor role. Some mowing schedules that were harmful to the LMG nevertheless allowed the species to moderately expand its range. Especially under minor climate change, in many subregions dispersal allowed for mowing early in the year, which is economically beneficial for farmers. More severe climate change could facilitate LMG expansion to uninhabited regions but would require suitable mowing schedules along the path. These insights can be transferred to other species, given that the LMG is considered a representative of grassland communities. For more specific predictions on the dynamics of other species affected by climate change and land use, the publicly available HiLEG model can be easily adapted to the characteristics of their life cycle.
Understanding the influence of climate change and population pressure on human conflict remains a critically important topic in the social sciences. Long-term records that evaluate these dynamics across multiple centuries and outside the range of modern climatic variation are especially capable of elucidating the relative effect of-and the interaction between-climate and demography. This is crucial given that climate change may structure population growth and carrying capacity, while both climate and population influence per capita resource availability. This study couples paleoclimatic and demographic data with osteological evaluations of lethal trauma from 149 directly accelerator mass spectrometry C-14-dated individuals from the Nasca highland region of Peru. Multiple local and supraregional precipitation proxies are combined with a summed probability distribution of 149 C-14 dates to estimate population dynamics during a 700-y study window. Counter to previous findings, our analysis reveals a precipitous increase in violent deaths associated with a period of productive and stable climate, but volatile population dynamics. We conclude that favorable local climate conditions fostered population growth that put pressure on the marginal and highly circumscribed resource base, resulting in violent resource competition that manifested in over 450 y of internecine warfare. These findings help support a general theory of intergroup violence, indicating that relative resource scarcity-whether driven by reduced resource abundance or increased competition-can lead to violence in subsistence societies when the outcome is lower per capita resource availability.
Climate change projections predict that Mediterranean-type ecosystems (MTEs) are becoming hotter and drier and that fires will become more frequent and severe.
While most plant species in these important biodiversity hotspots are adapted to hot, dry summers and recurrent fire, the Interval Squeeze framework suggests that reduced seed production (demographic shift), reduced seedling establishment after fire (post fire recruitment shift), and reduction in the time between successive fires (fire interval shift) will threaten fire killed species under climate change.
One additional potential driver of accelerated species decline, however, has not been considered so far: the decrease in pollination success observed in many ecosystems worldwide has the potential to further reduce seed accumulation and thus population persistence also in these already threatened systems.
Using the well-studied fire-killed and serotinous shrub species Banksia hookeriana as an example, we apply a new spatially implicit population simulation model to explore population dynamics under past (1988-2002) and current (2003-2017) climate conditions, deterministic and stochastic fire regimes, and alternative scenarios of pollination decline.
Overall, model results suggest that while B. hookeriana populations were stable under past climate conditions, they will not continue to persist under current (and prospective future) climate.
Negative effects of climatic changes and more frequent fires are reinforced by the measured decline in seed set leading to further reduction in the mean persistence time by 12-17%.
These findings clearly indicate that declining pollination rates can be a critical factor that increases further the pressure on the persistence of fire-killed plants.
Future research needs to investigate whether other fire-killed species are similarly threatened, and if local population extinction may be compensated by recolonization events, facilitating persistence in spatially structured meta-communities.
The ongoing climate change is altering the living conditions for many organisms on this planet at an unprecedented pace. Hence, it is crucial for the survival of species to adapt to these changing conditions. In this dissertation Silene vulgaris is used as a model organism to understand the adaption strategies of widely distributed plant species to the current climate change. Especially plant species that possess a wide geographic range are expected to have a high phenotypic plasticity or to show genetic differentiation in response to the different climate conditions they grow in. However, they are often underrepresented in research.
In the greenhouse experiment presented in this thesis, I examined the phenotypic responses and plasticity in S. vulgaris to estimate its’ adaptation potential. Seeds from 25 wild European populations were collected along a latitudinal gradient and grown in a greenhouse under three different precipitation (65 mm, 75 mm, 90 mm) and two different temperature regimes (18°C, 21°C) that resembled a possible climate change scenario for central Europe. Afterwards different biomass and fecundity-related plant traits were measured.
The treatments significantly influenced the plants but did not reveal a latitudinal difference in response to climate treatments for most plant traits. The number of flowers per individual however, showed a stronger plasticity in northern European populations (e.g., Swedish populations) where numbers decreased more drastically with increased temperature and decreased precipitation.
To gain an even deeper understanding of the adaptation of S. vulgaris to climate change it is also important to reveal the underlying phylogeny of the sampled populations. Therefore, I analysed their population genetic structure through whole genome sequencing via ddRAD.
The sequencing revealed three major genetic clusters in the S. vulgaris populations sampled in Europe: one cluster comprised Southern European populations, one cluster Western European populations and another cluster contained central European populations. A following analysis of experimental trait responses among the clusters to the climate-change scenario showed that the genetic clusters significantly differed in biomass-related traits and in the days to flowering. However, half of the traits showed parallel response patterns to the experimental climate-change scenario.
In addition to the potential geographic and genetic adaptation differences to climate change this dissertation also deals with the response differences between the sexes in S. vulgaris. As a gynodioecious species populations of S. vulgaris consist of female and hermaphrodite
individuals and the sexes can differ in their morphological traits which is known as sexual dimorphism. As climate change is becoming an important factor influencing plant morphology it remains unclear if and how different sexes may respond in sexually dimorphic species. To examine this question the sex of each individual plant was determined during the greenhouse experiment and the measured plant traits were analysed accordingly. In general, hermaphrodites had a higher number of flowers but a lower number of leaves than females. With regards to the climate change treatment, I found that hermaphrodites showed a milder negative response to higher temperatures in the number of flowers produced and in specific leaf area (SLA) compared to females.
Synthesis – The significant treatment response in Silene vulgaris, independent of population origin in most traits suggests a high degree of universal phenotypic plasticity. Also, the three European intraspecific genetic lineages detected showed comparable parallel response patterns in half of the traits suggesting considerable phenotypic plasticity. Hence, plasticity might represent a possible adaptation strategy of this widely distributed species during ongoing and future climatic changes. The results on sexual dimorphism show that females and hermaphrodites are differing mainly in their number of flowers and females are affected more strongly by the experimental climate-change scenario. These results provide a solid knowledge basis on the sexual dimorphism in S. vulgaris under climate change, but further research is needed to determine the long-term impact on the breeding system for the species.
In summary this dissertation provides a comprehensive insight into the adaptation mechanisms and consequences of a widely distributed and gynodioecious plant species and leverages our understanding of the impact of anthropogenic climate change on plants.
In a changing world, phytoplankton communities face a large variety of challenges including altered light regimes. These alterations are caused by more pronounced stratification due to rising temperatures, enhanced eutrophication, and browning of lakes. Community responses toward these effects can emerge as alterations in physiology, biomass, biochemical composition, or diversity. In this study, we addressed the combined effects of changes in light and nutrient conditions on community responses. In particular, we investigated how light intensity and variability under two nutrient conditions influence (1) fast responses such as adjustments in photosynthesis, (2) intermediate responses such as pigment adaptation and (3) slow responses such as changes in community biomass and species composition. Therefore, we exposed communities consisting of five phytoplankton species belonging to different taxonomic groups to two constant and two variable light intensity treatments combined with two levels of phosphorus supply. The tested phytoplankton communities exhibited increased fast reactions of photosynthetic processes to light variability and light intensity. The adjustment of their light harvesting mechanisms via community pigment composition was not affected by light intensity, variability, or nutrient supply. However, pigment specific effects of light intensity, light variability, and nutrient supply on the proportion of the respective pigments were detected. Biomass was positively affected by higher light intensity and nutrient concentrations while the direction of the effect of variability was modulated by light intensity. Light variability had a negative impact on biomass at low, but a positive impact at high light intensity. The effects on community composition were species specific. Generally, the proportion of green algae was higher under high light intensity, whereas the cyanobacterium performed better under low light conditions. In addition to that, the diatom and the cryptophyte performed better with high nutrient supply while the green algae as well as the cyanobacterium performed better at low nutrient conditions. This shows that light intensity, light variability, and nutrient supply interactively affect communities. Furthermore, the responses are highly species and pigment specific, thus to clarify the effects of climate change a deeper understanding of the effects of light variability and species interactions within communities is important.