Publications by authors named "Christiane Werner"

48 Publications

Fertilized graminoids intensify negative drought effects on grassland productivity.

Glob Chang Biol 2021 Jun 21;27(11):2441-2457. Epub 2021 Mar 21.

Department of Soil and Environment, Sveriges Landbruksuniversitet (SLU), Uppsala, Sweden.

Droughts can strongly affect grassland productivity and biodiversity, but responses differ widely. Nutrient availability may be a critical factor explaining this variation, but is often ignored in analyses of drought responses. Here, we used a standardized nutrient addition experiment covering 10 European grasslands to test if full-factorial nitrogen, phosphorus, and potassium addition affected plant community responses to inter-annual variation in drought stress and to the extreme summer drought of 2018 in Europe. We found that nutrient addition amplified detrimental drought effects on community aboveground biomass production. Drought effects also differed between functional groups, with a negative effect on graminoid but not forb biomass production. Our results imply that eutrophication in grasslands, which promotes dominance of drought-sensitive graminoids over forbs, amplifies detrimental drought effects. In terms of climate change adaptation, agricultural management would benefit from taking into account differential drought impacts on fertilized versus unfertilized grasslands, which differ in ecosystem services they provide to society.
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http://dx.doi.org/10.1111/gcb.15583DOI Listing
June 2021

Physiological responses of date palm (Phoenix dactylifera) seedlings to seawater and flooding.

New Phytol 2021 03 23;229(6):3318-3329. Epub 2020 Dec 23.

Chair of Tree Physiology, Institute of Forest Sciences, Albert-Ludwigs-Universität Freiburg, Georges-Köhler-Allee 53, Freiburg, 79110, Germany.

In their natural environment along coast lines, date palms are exposed to seawater inundation and, hence, combined stress by salinity and flooding. To elucidate the consequences of this combined stress on foliar gas exchange and metabolite abundances in leaves and roots, date palm seedlings were exposed to flooding with seawater and its major constituents under controlled conditions. Seawater flooding significantly reduced CO assimilation, transpiration and stomatal conductance, but did not affect isoprene emission. A similar effect was observed upon NaCl exposure. By contrast, flooding with distilled water or MgSO did not affect CO /H O gas exchange or stomatal conductance significantly, indicating that neither flooding itself, nor seawater sulfate, contributed greatly to stomatal closure. Seawater exposure increased Na and Cl contents in leaves and roots, but did not affect sulfate contents significantly. Metabolite analyses revealed reduced abundances of foliar compatible solutes, such as sugars and sugar alcohols, whereas nitrogen compounds accumulated in roots. Reduced transpiration upon seawater exposure may contribute to controlling the movement of toxic ions to leaves and, therefore, can be seen as a mechanism to cope with salinity. The present results indicate that date palm seedlings are tolerant towards seawater exposure to some extent, and highly tolerant to flooding.
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http://dx.doi.org/10.1111/nph.17123DOI Listing
March 2021

Heat Waves Change Plant Carbon Allocation Among Primary and Secondary Metabolism Altering CO Assimilation, Respiration, and VOC Emissions.

Front Plant Sci 2020 14;11:1242. Epub 2020 Aug 14.

Ecosystem Physiology, University of Freiburg, Freiburg, Germany.

Processes controlling plant carbon allocation among primary and secondary metabolism, i.e., carbon assimilation, respiration, and VOC synthesis are still poorly constrained, particularly regarding their response to stress. To investigate these processes, we simulated a 10-day 38°C heat wave, analysing real-time carbon allocation into primary and secondary metabolism in the Mediterranean shrub . We traced position-specific C-labeled pyruvate into daytime VOC and CO emissions and during light-dark transition. Net CO assimilation strongly declined under heat, due to three-fold higher respiration rates. Interestingly, day respiration also increased two-fold. Decarboxylation of the C1-atom of pyruvate was the main process driving daytime CO release, whereas the C2-moiety was not decarboxylated in the TCA cycle. Heat induced high emissions of methanol, methyl acetate, acetaldehyde as well as mono- and sesquiterpenes, particularly during the first two days. After 10-days of heat a substantial proportion of C-labeled pyruvate was allocated into synthesis of VOCs. Thus, during extreme heat waves high respiratory losses and reduced assimilation can shift plants into a negative carbon balance. Still, plants enhanced their investment into VOC synthesis despite associated metabolic CO losses. We conclude that heat stress re-directed the proportional flux of key metabolites into pathways of VOC biosynthesis most likely at the expense of reactions of plant primary metabolism, which might highlight their importance for stress protection.
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http://dx.doi.org/10.3389/fpls.2020.01242DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7456945PMC
August 2020

Water Stable Isotopes in Ecohydrological Field Research: Comparison Between and Destructive Monitoring Methods to Determine Soil Water Isotopic Signatures.

Front Plant Sci 2020 14;11:387. Epub 2020 Apr 14.

Ecosystem Physiology, University of Freiburg, Freiburg, Germany.

Ecohydrological isotope based field research is often constrained by a lack of temporally explicit soil water data, usually related to the choice of destructive sampling in the field and subsequent analysis in the laboratory. New techniques based on gas permeable membranes allow to sample soil water vapor and infer soil liquid water isotopic signatures. Here, a membrane-based soil water vapor sampling method was tested at a grassland site in Freiburg, Germany. It was further compared with two commonly used destructive sampling approaches for determination of soil liquid water isotopic signatures: cryogenic vacuum extraction and centrifugation. All methods were tested under semi-controlled field conditions, conducting an experiment with dry-wet cycling and two isotopically different labeling irrigation waters. We found mean absolute differences between cryogenic vacuum extraction and vapor measurements of 0.3-14.2‰ (δO) and 0.4-152.2‰ (δH) for soil liquid water. The smallest differences were found under natural abundance conditions of H and O, the strongest differences were observed after irrigation with labeled waters. Labeling strongly increased the isotopic variation in soil water: Mean soil water isotopic signatures derived by cryogenic vacuum extraction were -11.6 ± 10.9‰ (δO) and +61.9 ± 266.3‰ (δH). The soil water vapor method showed isotopic signatures of -12.5 ± 9.4‰ (δO) and +169.3 ± 261.5‰ (δH). Centrifugation was unsuccessful for soil samples due to low water recovery rates. It is therefore not recommended. Our study highlights that the soil water vapor method captures the temporal dynamics in the isotopic signature of soil water well while the destructive approach also includes the natural lateral isotopic heterogeneity. The different advantages and limitations of the three methods regarding setup, handling and costs are discussed. The choice of method should not only consider prevailing environmental conditions but the experimental design and goal. We see a very promising tool in the soil water vapor method, capturing both temporal developments and spatial variability of soil water processes.
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http://dx.doi.org/10.3389/fpls.2020.00387DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7171290PMC
April 2020

Photosynthetic cyclic electron transport provides ATP for homeostasis during trap closure in Dionaea muscipula.

Ann Bot 2020 03;125(3):485-494

Chair of Tree Physiology, Institute of Forest Sciences, University of Freiburg, Freiburg, Germany.

Background And Aims: The processes connected with prey capture and the early consumption of prey by carnivorous Dionaea muscipula require high amounts of energy. The aim of the present study was to identify processes involved in flytrap energy provision and ATP homeostasis under these conditions.

Methods: We determined photosynthetic CO2 uptake and chlorophyll fluorescence as well as the dynamics of ATP contents in the snap traps upon closure with and without prey.

Key Results: The results indicate that upon prey capture, a transient switch from linear to cyclic electron transport mediates a support of ATP homeostasis. Beyond 4 h after prey capture, prey resources contribute to the traps' ATP pool and, 24 h after prey capture, export of prey-derived resources to other plant organs may become preferential and causes a decline in ATP contents.

Conclusions: Apparently, the energy demand of the flytrap for prey digestion and nutrient mining builds on both internal and prey-derived resources.
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http://dx.doi.org/10.1093/aob/mcz185DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7061167PMC
March 2020

Nitrogen Loading Enhances Stress Impact of Drought on a Semi-natural Temperate Grassland.

Front Plant Sci 2019 30;10:1051. Epub 2019 Aug 30.

Ecosystem Physiology, Freiburg University, Freiburg, Germany.

Two important threats to the sustainable functioning of seminatural grasslands in temperate zones are (1) nutrient loading due to agricultural fertilization and pollution, and (2) the increase of extreme drought events due to climate change. These threats may cause substantial shifts in species diversity and abundance and considerably affect the carbon and water balance of ecosystems. The synergistic effects between those two threats, however, can be complex and are poorly understood. Here, we experimentally investigated the effects of nitrogen addition and extreme drought (separately and in combination) on a seminatural temperate grassland, located in Freiburg (South Germany). To study the grassland response, we combined eddy-covariance techniques with open gas exchange systems. Open gas exchange chambers were connected to an infrared gas analyzer and water isotope spectrometer, which allowed the partitioning of net ecosystem exchange and evapotranspiration. Vegetation parameters were described by species richness, species abundance, and leaf area index. Our results suggest that grassland communities, strongly weakened in their stress response by nitrogen loading, can substantially lose their carbon sink function during drought. While nitrogen addition caused a significant loss in forb species (-25%), precipitation reduction promoted a strong dominance of grass species at season start. Consequently, the grass-dominated and species-poor community suffered from a strong above-ground dieback during the dry summer months, likely caused by lower water use efficiency and weaker drought adaptations of the species community. Over the growing season (April-September), the carbon sequestration of the studied grassland was reduced by more than 60% as a consequence of nitrogen addition. Nitrogen addition in combination with precipitation reduction decreased carbon sequestration by 73%. Eutrophication can severely threaten the resilient functioning of grasslands, in particular when drought periods will increase as predicted by future climate scenarios. Our findings emphasize the importance of preserving high diversity of grasslands to strengthen their resistance against extreme events such as droughts.
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http://dx.doi.org/10.3389/fpls.2019.01051DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6730263PMC
August 2019

Heat stress increases the use of cytosolic pyruvate for isoprene biosynthesis.

J Exp Bot 2019 10;70(20):5827-5838

Institute of Ecosystem Physiology, University Freiburg, Freiburg, Germany.

The increasing occurrence of heatwaves has intensified temperature stress on terrestrial vegetation. Here, we investigate how two contrasting isoprene-emitting tropical species, Ficus benjamina and Pachira aquatica, cope with heat stress and assess the role of internal plant carbon sources for isoprene biosynthesis in relation to thermotolerance. To our knowledge, this is the first study to report isoprene emissions from P. aquatica. We exposed plants to two levels of heat stress and determined the temperature response curves for isoprene and photosynthesis. To assess the use of internal C sources in isoprene biosynthesis, plants were fed with 13C position-labelled pyruvate. F. benjamina was more heat tolerant with higher constitutive isoprene emissions and stronger acclimation to higher temperatures than P. aquatica, which showed higher induced isoprene emissions at elevated temperatures. Under heat stress, both isoprene emissions and the proportion of cytosolic pyruvate allocated into isoprene synthesis increased. This represents a mechanism that P. aquatica, and to a lesser extent F. benjamina, has adopted as an immediate response to sudden increase in heat stress. However, in the long run under prolonged heat, the species with constitutive emissions (F. benjamina) was better adapted, indicating that plants that invest more carbon into protective emissions of biogenic volatile organic compounds tend to suffer less from heat stress.
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http://dx.doi.org/10.1093/jxb/erz353DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6812709PMC
October 2019

Effects of mesophyll conductance on vegetation responses to elevated CO concentrations in a land surface model.

Glob Chang Biol 2019 05 23;25(5):1820-1838. Epub 2019 Mar 23.

Department of Ecosystem Physiology, University of Freiburg, Freiburg, Germany.

Mesophyll conductance (g ) is known to affect plant photosynthesis. However, g is rarely explicitly considered in land surface models (LSMs), with the consequence that its role in ecosystem and large-scale carbon and water fluxes is poorly understood. In particular, the different magnitudes of g across plant functional types (PFTs) are expected to cause spatially divergent vegetation responses to elevated CO concentrations. Here, an extensive literature compilation of g across major vegetation types is used to parameterize an empirical model of g in the LSM JSBACH and to adjust photosynthetic parameters based on simulated A  - C curves. We demonstrate that an explicit representation of g changes the response of photosynthesis to environmental factors, which cannot be entirely compensated by adjusting photosynthetic parameters. These altered responses lead to changes in the photosynthetic sensitivity to atmospheric CO concentrations which depend both on the magnitude of g and the climatic conditions, particularly temperature. We then conducted simulations under ambient and elevated (ambient + 200 μmol/mol) CO concentrations for contrasting ecosystems and for historical and anticipated future climate conditions (representative concentration pathways; RCPs) globally. The g -explicit simulations using the RCP8.5 scenario resulted in significantly higher increases in gross primary productivity (GPP) in high latitudes (+10% to + 25%), intermediate increases in temperate regions (+5% to + 15%), and slightly lower to moderately higher responses in tropical regions (-2% to +5%), which summed up to moderate GPP increases globally. Similar patterns were found for transpiration, but with a lower magnitude. Our results suggest that the effect of an explicit representation of g is most important for simulated carbon and water fluxes in the boreal zone, where a cold climate coincides with evergreen vegetation.
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http://dx.doi.org/10.1111/gcb.14604DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6487956PMC
May 2019

A pool-weighted perspective on the two-water-worlds hypothesis.

New Phytol 2019 05 9;222(3):1271-1283. Epub 2019 Feb 9.

Chair of Ecosystem Physiology, University of Freiburg, Georges-Köhler-Allee 53/54, Freiburg, 79110, Germany.

The 'two-water-worlds' hypothesis is based on stable isotope differences in stream, soil and xylem waters in dual isotope space. It postulates no connectivity between bound and mobile soil waters, and preferential plant water uptake of bound soil water sources. We tested the pool-weighted impact of isotopically distinct water pools for hydrological cycling, the influence of species-specific water use and the degree of ecohydrological separation. We combined stable isotope analysis (δ O and δ H) of ecosystem water pools of precipitation, groundwater, soil and xylem water of two distinct species (Quercus suber, Cistus ladanifer) with observations of soil water contents and sap flow. Shallow soil water was evaporatively enriched during dry-down periods, but enrichment faded strongly with depth and upon precipitation events. Despite clearly distinct water sources and water-use strategies, both species displayed a highly opportunistic pattern of root water uptake. Here we offer an alternative explanation, showing that the isotopic differences between soil and plant water vs groundwater can be fully explained by spatio-temporal dynamics. Pool weighting the contribution of evaporatively enriched soil water reveals only minor annual impacts of these sources to ecosystem water cycling (c. 11% of bulk soil water and c. 14% of transpired water).
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http://dx.doi.org/10.1111/nph.15670DOI Listing
May 2019

A prolonged dry season and nitrogen deposition interactively affect CO fluxes in an annual Mediterranean grassland.

Sci Total Environ 2019 Mar 12;654:978-986. Epub 2018 Nov 12.

Forest Research Centre, School of Agriculture, University of Lisbon, Lisbon, Portugal.

Mediterranean annual grasslands are species-diverse ecosystems of high economic and ecological value. CO and water fluxes in these grasslands are triggered by the first rains in autumn, after a long hot and dry summer. Climate change scenarios project altered rainfall patterns, such as prolonged dry season into the autumn, while simultaneously nitrogen (N) deposition is increasing globally. However, how these global change drivers will interact to affect Mediterranean grassland CO, water fluxes and productivity is still unclear. In a greenhouse experiment, we subjected the seedbank of an annual Mediterranean grassland to a factorial treatment, by prolonging the dry season by 0 days (i.e. no autumn drought), 50 days and 100 days and crossing these drought treatments with two levels of N deposition: no N and N addition. A delayed onset of the rain season, i.e., a prolonged dry season, induced lower CO and water fluxes throughout the growing season and a lower aboveground biomass by the end of the study period. However, N addition attenuated the effects on NEE, Reco and GPP, but did not affect aboveground biomass or functional group composition. A prolonged dry season also lowered the productivity of forbs, the dominant functional group in our grassland. Our results anticipate important effects of interacting global change drivers on Mediterranean grassland functioning.
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http://dx.doi.org/10.1016/j.scitotenv.2018.11.091DOI Listing
March 2019

Isotopic evidence for oligotrophication of terrestrial ecosystems.

Nat Ecol Evol 2018 11 22;2(11):1735-1744. Epub 2018 Oct 22.

Key Laboratory of Ecosystem Network Observation and Modeling, Institute of Geographic Sciences and Natural Resources Research, Chinese Academy of Sciences, Beijing, China.

Human societies depend on an Earth system that operates within a constrained range of nutrient availability, yet the recent trajectory of terrestrial nitrogen (N) availability is uncertain. Examining patterns of foliar N concentrations and isotope ratios (δN) from more than 43,000 samples acquired over 37 years, here we show that foliar N concentration declined by 9% and foliar δN declined by 0.6-1.6‰. Examining patterns across different climate spaces, foliar δN declined across the entire range of mean annual temperature and mean annual precipitation tested. These results suggest declines in N supply relative to plant demand at the global scale. In all, there are now multiple lines of evidence of declining N availability in many unfertilized terrestrial ecosystems, including declines in δN of tree rings and leaves from herbarium samples over the past 75-150 years. These patterns are consistent with the proposed consequences of elevated atmospheric carbon dioxide and longer growing seasons. These declines will limit future terrestrial carbon uptake and increase nutritional stress for herbivores.
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http://dx.doi.org/10.1038/s41559-018-0694-0DOI Listing
November 2018

Water fluxes mediated by vegetation: emerging isotopic insights at the soil and atmosphere interfaces.

New Phytol 2019 03 19;221(4):1754-1763. Epub 2018 Nov 19.

Ecosystem Physiology, University of Freiburg, 79110, Freiburg, Germany.

Plants mediate water fluxes within the soil-vegetation-atmosphere continuum. This water transfer in soils, through plants, into the atmosphere can be effectively traced by stable isotopologues of water. However, rapid dynamic processes have only recently gained attention, such as adaptations in root water uptake depths (within hours to days) or the imprint of transpirational fluxes on atmospheric moisture, particularly promoted by the development of real-time in-situ water vapour stable isotope observation techniques. We focus on open questions and emerging insights at the soil-plant and plant-atmosphere interfaces, as we believe that these are the controlling factors for ecosystem water cycling. At both interfaces, complex pictures of interacting ecophysiological and hydrological processes emerge: root water uptake dynamics depend on both spatiotemporal variations in water availability and species-specific regulation of adaptive root conductivity within the rooting system by, for example, modulating soil-root conductivity in response to water and nutrient demands. Similarly, plant water transport and losses are a fine-tuned interplay between species-specific structural and functional strategies of water use and atmospheric processes. We propose that only by explicitly merging insights from distinct disciplines - for example, hydrology, plant physiology and atmospheric sciences - will we gain a holistic picture of the impact of vegetation on processes governing the soil-plant-atmosphere continuum.
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http://dx.doi.org/10.1111/nph.15547DOI Listing
March 2019

Real-time carbon allocation into biogenic volatile organic compounds (BVOCs) and respiratory carbon dioxide (CO2) traced by PTR-TOF-MS, 13CO2 laser spectroscopy and 13C-pyruvate labelling.

PLoS One 2018 25;13(9):e0204398. Epub 2018 Sep 25.

Ecosystem Physiology, Institute of Forest Sciences, Faculty of Environment and Natural Resources, Albert-Ludwigs-University Freiburg, Freiburg, Germany.

Our understanding of biogenic volatile organic compound (BVOC) emissions improved substantially during the last years. Nevertheless, there are still large uncertainties of processes controlling plant carbon investment into BVOCs, of some biosynthetic pathways and their linkage to CO2 decarboxylation at central metabolic branching points. To shed more light on carbon partitioning during BVOC biosynthesis, we used an innovative approach combining δ13CO2 laser spectroscopy, high-sensitivity proton-transfer-reaction time-of-flight mass spectrometry and a multiple branch enclosure system in combination with position-specific 13C-metabolite labelling. Feeding experiments with position-specific 13C-labelled pyruvate, a central metabolite of BVOC synthesis, enabled online detection of carbon partitioning into 13C-BVOCs and respiratory 13CO2. Measurements of trace gas emissions of the Mediterranean shrub Halimium halimifolium revealed a broad range of emitted BVOCs. In general, [2-13C]-PYR was rapidly incorporated into emitted acetic acid, methyl acetate, toluene, cresol, trimethylbenzene, ethylphenol, monoterpenes and sesquiterpenes, indicating de novo BVOC biosynthesis of these compounds. In contrast, [1-13C]-pyruvate labelling substantially increased 13CO2 emissions in the light indicating C1-decarboxylation. Similar labelling patterns of methyl acetate and acetic acid suggested tightly connected biosynthetic pathways and, furthermore, there were hints of possible biosynthesis of benzenoids via the MEP-pathway. Overall, substantial CO2 emission from metabolic branching points during de novo BVOC biosynthesis indicated that decarboxylation of [1-13C]-pyruvate, as a non-mitochondrial source of CO2, seems to contribute considerably to daytime CO2 release from leaves. Our approach, combining synchronised BVOC and CO2 measurements in combination with position-specific labelling opens the door for real-time analysis tracing metabolic pathways and carbon turnover under different environmental conditions, which may enhance our understanding of regulatory mechanisms in plant carbon metabolism and BVOC biosynthesis.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0204398PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6155514PMC
March 2019

Terpenoid Emissions of Two Mediterranean Woody Species in Response to Drought Stress.

Front Plant Sci 2018 23;9:1071. Epub 2018 Jul 23.

Ecosystem Physiology, University of Freiburg, Freiburg, Germany.

Drought is a major environmental constrain affecting plant performance and survival, particularly in Mediterranean ecosystems. Terpenoids may play a protective role under these conditions, however, observations of drought effects on plant terpenoid emissions are controversial ranging from decreased emissions to unaffected or increased release of terpenoids. In the present study we investigated terpenoid emissions of cork oak () and gum rockrose () in response to summer drought stress in 2017. Pre-dawn leaf water potential (Ψ) decreased from -0.64 to -1.72 MPa in and from -1.69 to -4.05 MPa in , indicating a transition from mild to severe drought along summer. Total terpenoid emissions decreased with drought, but differed significantly between species ( < 0.001) and in response to Ψ, air temperature and assimilation rates. emitted a large variety of >75 compounds comprising monoterpenes, sesquiterpenes and even diterpenes, which strongly decreased from 1.37 ± 0.23 μg gh to 0.40 ± 0.08 μg gh ( < 0.001) in response to drought. Total emission rates were positively correlated to air temperature ( < 0.001). behavior points toward terpenoid leaf storage depletion and reduced substrate availability for terpenoid synthesis with increasing drought, most likely accelerated by high air temperatures. emitted mainly monoterpenes and emissions declined significantly from June (0.50 ± 0.08 μg gh) to August (0.29 ± 0.02 μg gh) ( < 0.01). Emission rates were weakly correlated with net assimilation rates ( = 0.19, < 0.001), but did not respond strongly to Ψ and air temperature. Early onset of drought in 2017 most likely reduced plant metabolism in , resulting in diminished, but stable terpenoid fluxes. Calculation of standard emission factors (at 30°C) revealed contrasting emission patterns of decreasing, unaffected, or increasing fluxes of single terpenoid compounds. Unaffected or drought-enhanced emissions of compounds such as α-pinene, camphene or manoyl oxide may point toward a specific role of these terpenoids in abiotic stress adaptation. In conclusion, these results suggest a strong negative, but species- and compound-specific effect of severe drought on terpenoid fluxes in Mediterranean ecosystems.
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http://dx.doi.org/10.3389/fpls.2018.01071DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6064746PMC
July 2018

Quantifying differences in water and carbon cycling between paddy and rainfed rice (Oryza sativa L.) by flux partitioning.

PLoS One 2018 6;13(4):e0195238. Epub 2018 Apr 6.

Department of Ecosystem Physiology, University of Freiburg, Freiburg, Germany.

Agricultural crops play an important role in the global carbon and water cycle. Global climate change scenarios predict enhanced water scarcity and altered precipitation pattern in many parts of the world. Hence, a mechanistic understanding of water fluxes, productivity and water use efficiency of cultivated crops is of major importance, i.e. to adapt management practices. We compared water and carbon fluxes of paddy and rainfed rice by canopy scale gas exchange measurements, crop growth, daily evapotranspiration, transpiration and carbon flux modeling. Throughout a monsoon rice growing season, soil evaporation in paddy rice contributed strongly to evapotranspiration (96.6% to 43.3% from initial growth to fully developed canopy and amounted to 57.9% of total water losses over the growing seasons. Evaporation of rainfed rice was significantly lower (by 65% on average) particularly before canopy closure. Water use efficiency (WUE) was significantly higher in rainfed rice both from an agronomic (WUEagro, i.e. grain yield per evapotranspiration) and ecosystem (WUEeco, i.e. gross primary production per evapotranspiration) perspective. However, our results also show that higher WUE in rainfed rice comes at the expense of higher respiration losses compared to paddy rice (26% higher on average). Hence, suggestions on water management depend on the regional water availability (i.e. Mediterranean vs. Monsoon climate) and the balance between higher respiratory losses versus a potential reduction in CH4 and other greenhouse gas emissions. Our results suggest that a shift from rainfed/unsaturated soil to waterlogged paddy conditions after closure of the rice canopy might be a good compromise towards a sustainable use of water while preserving grain yield, particularly for water-limited production areas.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0195238PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5889072PMC
July 2018

Towards physiologically meaningful water-use efficiency estimates from eddy covariance data.

Glob Chang Biol 2018 02 11;24(2):694-710. Epub 2017 Oct 11.

Department of Physical Geography and Ecosystem Science, Lund University, Lund, Sweden.

Intrinsic water-use efficiency (iWUE) characterizes the physiological control on the simultaneous exchange of water and carbon dioxide in terrestrial ecosystems. Knowledge of iWUE is commonly gained from leaf-level gas exchange measurements, which are inevitably restricted in their spatial and temporal coverage. Flux measurements based on the eddy covariance (EC) technique can overcome these limitations, as they provide continuous and long-term records of carbon and water fluxes at the ecosystem scale. However, vegetation gas exchange parameters derived from EC data are subject to scale-dependent and method-specific uncertainties that compromise their ecophysiological interpretation as well as their comparability among ecosystems and across spatial scales. Here, we use estimates of canopy conductance and gross primary productivity (GPP) derived from EC data to calculate a measure of iWUE (G , "stomatal slope") at the ecosystem level at six sites comprising tropical, Mediterranean, temperate, and boreal forests. We assess the following six mechanisms potentially causing discrepancies between leaf and ecosystem-level estimates of G : (i) non-transpirational water fluxes; (ii) aerodynamic conductance; (iii) meteorological deviations between measurement height and canopy surface; (iv) energy balance non-closure; (v) uncertainties in net ecosystem exchange partitioning; and (vi) physiological within-canopy gradients. Our results demonstrate that an unclosed energy balance caused the largest uncertainties, in particular if it was associated with erroneous latent heat flux estimates. The effect of aerodynamic conductance on G was sufficiently captured with a simple representation. G was found to be less sensitive to meteorological deviations between canopy surface and measurement height and, given that data are appropriately filtered, to non-transpirational water fluxes. Uncertainties in the derived GPP and physiological within-canopy gradients and their implications for parameter estimates at leaf and ecosystem level are discussed. Our results highlight the importance of adequately considering the sources of uncertainty outlined here when EC-derived water-use efficiency is interpreted in an ecophysiological context.
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http://dx.doi.org/10.1111/gcb.13893DOI Listing
February 2018

Heterogeneous environments shape invader impacts: integrating environmental, structural and functional effects by isoscapes and remote sensing.

Sci Rep 2017 06 23;7(1):4118. Epub 2017 Jun 23.

Ecosystem Physiology, University of Freiburg, Georges-Köhler-Allee 53/54, 79110, Freiburg, Germany.

Spatial heterogeneity of ecosystems crucially influences plant performance, while in return plant feedbacks on their environment may increase heterogeneous patterns. This is of particular relevance for exotic plant invaders that transform native ecosystems, yet, approaches integrating geospatial information of environmental heterogeneity and plant-plant interaction are lacking. Here, we combined remotely sensed information of site topography and vegetation cover with a functional tracer of the N cycle, δN. Based on the case study of the invasion of an N-fixing acacia in a nutrient-poor dune ecosystem, we present the first model that can successfully predict (R  = 0.6) small-scale spatial variation of foliar δN in a non-fixing native species from observed geospatial data. Thereby, the generalized additive mixed model revealed modulating effects of heterogeneous environments on invader impacts. Hence, linking remote sensing techniques with tracers of biological processes will advance our understanding of the dynamics and functioning of spatially structured heterogeneous systems from small to large spatial scales.
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http://dx.doi.org/10.1038/s41598-017-04480-4DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5482842PMC
June 2017

The response of ecosystem water-use efficiency to rising atmospheric CO concentrations: sensitivity and large-scale biogeochemical implications.

New Phytol 2017 Mar 7;213(4):1654-1666. Epub 2016 Nov 7.

Department of Ecosystem Physiology, University of Freiburg, 79085, Freiburg, Germany.

Ecosystem water-use efficiency (WUE) is an important metric linking the global land carbon and water cycles. Eddy covariance-based estimates of WUE in temperate/boreal forests have recently been found to show a strong and unexpected increase over the 1992-2010 period, which has been attributed to the effects of rising atmospheric CO concentrations on plant physiology. To test this hypothesis, we forced the observed trend in the process-based land surface model JSBACH by increasing the sensitivity of stomatal conductance (g ) to atmospheric CO concentration. We compared the simulated continental discharge, evapotranspiration (ET), and the seasonal CO exchange with observations across the extratropical northern hemisphere. The increased simulated WUE led to substantial changes in surface hydrology at the continental scale, including a significant decrease in ET and a significant increase in continental runoff, both of which are inconsistent with large-scale observations. The simulated seasonal amplitude of atmospheric CO decreased over time, in contrast to the observed upward trend across ground-based measurement sites. Our results provide strong indications that the recent, large-scale WUE trend is considerably smaller than that estimated for these forest ecosystems. They emphasize the decreasing CO sensitivity of WUE with increasing scale, which affects the physiological interpretation of changes in ecosystem WUE.
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http://dx.doi.org/10.1111/nph.14288DOI Listing
March 2017

Impact of Leaf Traits on Temporal Dynamics of Transpired Oxygen Isotope Signatures and Its Impact on Atmospheric Vapor.

Front Plant Sci 2017 18;8. Epub 2017 Jan 18.

Ecosystem Physiology, University Freiburg Freiburg, Germany.

Oxygen isotope signatures of transpiration (δ ) are powerful tracers of water movement from plant to global scale. However, a mechanistic understanding of how leaf morphological/physiological traits effect δ is missing. A laser spectrometer was coupled to a leaf-level gas-exchange system to measure fluxes and isotopic signatures of plant transpiration under controlled conditions in seven distinct species (). We analyzed the role of stomatal conductance ( ) and leaf water content () on the temporal dynamics of δ following changes in relative humidity (). Changes in rH were applied from 60 to 30% and from 30 to 60%, which is probably more than covering the maximum step changes occurring under natural conditions. Further, the impact of and on isotopic non-steady state isofluxes was analyzed. Following changes in , temporal development of δ was well described by a one-pool modeling approach for most species. Isofluxes of δ were dominantly driven by stomatal control on , particularly for the initial period of 30 min following a step change. Hence, the deviation of isofluxes from isotopic steady state can be large, even though plants transpire near to isotopic steady state. Notably, not only transpiration rate and stomatal conductance, but also the leaf traits stomatal density (as a measure of g) and leaf water content are significantly related to the time constant (τ) and non-steady-state isofluxes. This might provide an easy-to-access means of a priori assumptions for the impact of isotopic non-steady-state transpiration in various ecosystems. We discuss the implications of our results from leaf to ecosystem scale.
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http://dx.doi.org/10.3389/fpls.2017.00005DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5241305PMC
January 2017

The carnivorous Venus flytrap uses prey-derived amino acid carbon to fuel respiration.

New Phytol 2017 Apr 2;214(2):597-606. Epub 2017 Jan 2.

Institute of Forest Sciences, Chair of Tree Physiology, University of Freiburg, Georges-Köhler-Allee 53/54, Freiburg, 79110, Germany.

The present study was performed to elucidate the fate of carbon (C) and nitrogen (N) derived from protein of prey caught by carnivorous Dionaea muscipula. For this, traps were fed C/ N-glutamine (Gln). The release of CO was continuously monitored by isotope ratio infrared spectrometry. After 46 h, the allocation of C and N label into different organs was determined and tissues were subjected to metabolome, proteome and transcriptome analyses. Nitrogen of Gln fed was already separated from its C skeleton in the decomposing fluid secreted by the traps. Most of the Gln-C and Gln-N recovered inside plants were localized in fed traps. Among nonfed organs, traps were a stronger sink for Gln-C compared to Gln-N, and roots were a stronger sink for Gln-N compared to Gln-C. A significant amount of the Gln-C was respired as indicated by C-CO emission, enhanced levels of metabolites of respiratory Gln degradation and increased abundance of proteins of respiratory processes. Transcription analyses revealed constitutive expression of enzymes involved in Gln metabolism in traps. It appears that prey not only provides building blocks of cellular constituents of carnivorous Dionaea muscipula, but also is used for energy generation by respiratory amino acid degradation.
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http://dx.doi.org/10.1111/nph.14404DOI Listing
April 2017

Isoscapes resolve species-specific spatial patterns in plant-plant interactions in an invaded Mediterranean dune ecosystem.

Tree Physiol 2016 12 1;36(12):1460-1470. Epub 2016 Sep 1.

Department of Ecosystem Physiology, University of Freiburg, Georges-Köhler-Allee 53/54, 79110, Freiburg, Germany.

Environmental heterogeneity and plant-plant interactions are key factors shaping plant communities. However, the spatial dimension of plant-plant interactions has seldom been addressed in field studies. This is at least partially rooted in a lack of methods that can accurately resolve functional processes in a spatially explicit manner. Isoscapes, that is, spatially explicit representations of stable isotope data, provide a versatile means to trace functional changes on spatial scales, for example, related to N-cycling (foliar δN) and water use efficiency (WUE, foliar δC). In a case study in a nutrient-depleted Mediterranean dune ecosystem, we analysed the spatial impact of the invasive N-fixing Acacia longifolia on three native species of different functional types using δN and δC isoscapes and spatial autocorrelation analyses. Isoscapes revealed strong spatial patterns in δN and δC with pronounced species-specific differences, demonstrating distinct spatial ranges of plant-plant interactions. A coniferous tree and an ericaceous dwarf shrub showed significant enrichment in δN within a range of 5-8 m surrounding the canopy of A. longifolia, indicating input of N originating from symbiotic N-fixation by the invader. In the dwarf shrub, which was most responsive to invader influence, enrichment in δC additionally demonstrated spatially explicit changes to WUE, while a native N-fixer was unresponsive to the presence of the invader. Furthermore, δN and δC isoscapes yielded different patterns, indicating that plant-plant interactions can have distinct spatial distributions and ranges based on the process measured. Additionally, the magnitude of the effect differed between field situations with high and low invasion pressure. This study highlights that the spatial scale must be accounted for when assessing the effects and outcome of species interactions. Functional tracers such as stable isotopes enable us to quantify spatial ranges of plant-plant interactions, providing empirical data that can help to better understand and predict complex species interactions in multifaceted natural environments.
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http://dx.doi.org/10.1093/treephys/tpw075DOI Listing
December 2016

A Spatially Explicit Dual-Isotope Approach to Map Regions of Plant-Plant Interaction after Exotic Plant Invasion.

PLoS One 2016 27;11(7):e0159403. Epub 2016 Jul 27.

Biodiversity, Evolution and Ecology of Plants, Biocentre Klein Flottbek and Botanical Garden, University of Hamburg, Hamburg, Germany.

Understanding interactions between native and invasive plant species in field settings and quantifying the impact of invaders in heterogeneous native ecosystems requires resolving the spatial scale on which these processes take place. Therefore, functional tracers are needed that enable resolving the alterations induced by exotic plant invasion in contrast to natural variation in a spatially explicit way. 15N isoscapes, i.e., spatially referenced representations of stable nitrogen isotopic signatures, have recently provided such a tracer. However, different processes, e.g. water, nitrogen or carbon cycles, may be affected at different spatial scales. Thus multi-isotope studies, by using different functional tracers, can potentially return a more integrated picture of invader impact. This is particularly true when isoscapes are submitted to statistical methods suitable to find homogeneous subgroups in multivariate data such as cluster analysis. Here, we used model-based clustering of spatially explicit foliar δ15N and δ13C isoscapes together with N concentration of a native indicator species, Corema album, to map regions of influence in a Portuguese dune ecosystem invaded by the N2-fixing Acacia longifolia. Cluster analysis identified regions with pronounced alterations in N budget and water use efficiency in the native species, with a more than twofold increase in foliar N, and δ13C and δ15N enrichment of up to 2‰ and 8‰ closer to the invader, respectively. Furthermore, clusters of multiple functional tracers indicated a spatial shift from facilitation through N addition in the proximity of the invader to competition for resources other than N in close contact. Finding homogeneous subgroups in multi-isotope data by means of model-based cluster analysis provided an effective tool for detecting spatial structure in processes affecting plant physiology and performance. The proposed method can give an objective measure of the spatial extent of influence of plant-plant interactions, thus improving our understanding of spatial pattern and interactions in plant communities.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0159403PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4963087PMC
July 2017

Metabolic Fate of the Carboxyl Groups of Malate and Pyruvate and their Influence on δ(13)C of Leaf-Respired CO2 during Light Enhanced Dark Respiration.

Front Plant Sci 2016 3;7:739. Epub 2016 Jun 3.

Institute of Agricultural Sciences, ETH Zurich Zurich, Switzerland.

The enhanced CO2 release of illuminated leaves transferred into darkness, termed "light enhanced dark respiration (LEDR)", is often associated with an increase in the carbon isotope ratio of the respired CO2 (δ(13)CLEDR). The latter has been hypothesized to result from different respiratory substrates and decarboxylation reactions in various metabolic pathways, which are poorly understood so far. To provide a better insight into the underlying metabolic processes of δ(13)CLEDR, we fed position-specific (13)C-labeled malate and pyruvate via the xylem stream to leaves of species with high and low δ(13)CLEDR values (Halimium halimifolium and Oxalis triangularis, respectively). During respective label application, we determined label-derived leaf (13)CO2 respiration using laser spectroscopy and the (13)C allocation to metabolic fractions during light-dark transitions. Our results clearly show that both carboxyl groups (C-1 and C-4 position) of malate similarly influence respiration and metabolic fractions in both species, indicating possible isotope randomization of the carboxyl groups of malate by the fumarase reaction. While C-2 position of pyruvate was only weakly respired, the species-specific difference in natural δ(13)CLEDR patterns were best reflected by the (13)CO2 respiration patterns of the C-1 position of pyruvate. Furthermore, (13)C label from malate and pyruvate were mainly allocated to amino and organic acid fractions in both species and only little to sugar and lipid fractions. In summary, our results suggest that respiration of both carboxyl groups of malate (via fumarase) by tricarboxylic acid cycle reactions or by NAD-malic enzyme influences δ(13)CLEDR. The latter supplies the pyruvate dehydrogenase reaction, which in turn determines natural δ(13)CLEDR pattern by releasing the C-1 position of pyruvate.
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http://dx.doi.org/10.3389/fpls.2016.00739DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4891945PMC
July 2016

Resolving rapid dynamics of soil-plant-atmosphere interactions.

New Phytol 2016 May;210(3):767-9

Department of Ecosystem Physiology, University Freiburg, Georges-Köhler-Allee 53/54, Freiburg, 79110, Germany.

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http://dx.doi.org/10.1111/nph.13936DOI Listing
May 2016

Soil water availability and capacity of nitrogen accumulation influence variations of intrinsic water use efficiency in rice.

J Plant Physiol 2016 Apr 19;193:26-36. Epub 2016 Feb 19.

Department of Plant Ecology, BayCEER, University of Bayreuth, 95440, Bayreuth, Germany.

Leaf intrinsic water use efficiency (WUEi) coupling maximum assimilation rate (Amax) and transpirable water lost via stomatal conductance (gsc) has been gaining increasing concern in sustainable crop production. Factors that influence leaf Amax and WUEi in rice (Oryza sativa L. cv Unkang) at flooding and rainfed conditions were evaluated. Positive correlations for leaf nitrogen content (Nm) and maximum carboxylation rate (Vcmax), for nitrogen allocation in Rubisco enzymes and mesophyll conductance (gm) were evident independent of cropping cultures. Rainfed rice exhibited enriched canopy leaf average Nm resulting in higher Amax, partially supporting improved leaf WUEi. Maximum WUEi (up to 0.14 μmol mmol(-1)) recorded in rainfed rice under drought conditions resulted from increasing gm/gsc ratio while at cost of significant decline in Amax due to hydraulically constrained gsc. Amax sensitivity related to gsc which was regulated by plant hydraulic conductance. WUEi was tightly correlated to Vcmax/gsc and gm/gsc ratios across the paddy and rainfed not to light environment, morphological and physiological traits, highlighting enhance capacity of Nm accumulation in rainfed rice with gsc at moderately high level similar to paddy rice facilitate optimization in Amax and WUEi while, is challenged by drought-vulnerable plant hydraulic conductance.
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http://dx.doi.org/10.1016/j.jplph.2016.02.003DOI Listing
April 2016

Synergy of extreme drought and shrub invasion reduce ecosystem functioning and resilience in water-limited climates.

Sci Rep 2015 Oct 13;5:15110. Epub 2015 Oct 13.

Agroecosystem Research, BayCEER, University Bayreuth, Universitätsstr. 30, 95447 Bayreuth, Germany.

Extreme drought events and plant invasions are major drivers of global change that can critically affect ecosystem functioning and alter ecosystem-atmosphere exchange. Invaders are expanding worldwide and extreme drought events are projected to increase in frequency and intensity. However, very little is known on how these drivers may interact to affect the functioning and resilience of ecosystems to extreme events. Using a manipulative shrub removal experiment and the co-occurrence of an extreme drought event (2011/2012) in a Mediterranean woodland, we show that native shrub invasion and extreme drought synergistically reduced ecosystem transpiration and the resilience of key-stone oak tree species. Ecosystem transpiration was dominated by the water use of the invasive shrub Cistus ladanifer, which further increased after the extreme drought event. Meanwhile, the transpiration of key-stone tree species decreased, indicating a competitive advantage in favour of the invader. Our results suggest that in Mediterranean-type climates the invasion of water spending species and projected recurrent extreme drought events may synergistically cause critical drought tolerance thresholds of key-stone tree species to be surpassed, corroborating observed higher tree mortality in the invaded ecosystems. Ultimately, this may shift seasonally water limited ecosystems into less desirable alternative states dominated by water spending invasive shrubs.
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http://dx.doi.org/10.1038/srep15110DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4602198PMC
October 2015

Allocation of freshly assimilated carbon into primary and secondary metabolites after in situ ¹³C pulse labelling of Norway spruce (Picea abies).

Tree Physiol 2015 Nov 29;35(11):1176-91. Epub 2015 Sep 29.

Soil Biogeochemistry, Martin-Luther University Halle-Wittenberg, von-Seckendorff-Platz 3, 06120 Halle, Germany.

Plants allocate carbon (C) to sink tissues depending on phenological, physiological or environmental factors. We still have little knowledge on C partitioning into various cellular compounds and metabolic pathways at various ecophysiological stages. We used compound-specific stable isotope analysis to investigate C partitioning of freshly assimilated C into tree compartments (needles, branches and stem) as well as into needle water-soluble organic C (WSOC), non-hydrolysable structural organic C (stOC) and individual chemical compound classes (amino acids, hemicellulose sugars, fatty acids and alkanes) of Norway spruce (Picea abies) following in situ (13)C pulse labelling 15 days after bud break. The (13)C allocation within the above-ground tree biomass demonstrated needles as a major C sink, accounting for 86% of the freshly assimilated C 6 h after labelling. In needles, the highest allocation occurred not only into the WSOC pool (44.1% of recovered needle (13)C) but also into stOC (33.9%). Needle growth, however, also caused high (13)C allocation into pathways not involved in the formation of structural compounds: (i) pathways in secondary metabolism, (ii) C-1 metabolism and (iii) amino acid synthesis from photorespiration. These pathways could be identified by a high (13)C enrichment of their key amino acids. In addition, (13)C was strongly allocated into the n-alkyl lipid fraction (0.3% of recovered (13)C), whereby (13)C allocation into cellular and cuticular exceeded that of epicuticular fatty acids. (13)C allocation decreased along the lipid transformation and translocation pathways: the allocation was highest for precursor fatty acids, lower for elongated fatty acids and lowest for the decarbonylated n-alkanes. The combination of (13)C pulse labelling with compound-specific (13)C analysis of key metabolites enabled tracing relevant C allocation pathways under field conditions. Besides the primary metabolism synthesizing structural cell compounds, a complex network of pathways consumed the assimilated (13)C and kept most of the assimilated C in the growing needles.
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http://dx.doi.org/10.1093/treephys/tpv083DOI Listing
November 2015

Differences in foraging ecology align with genetically divergent ecotypes of a highly mobile marine top predator.

Oecologia 2015 Dec 26;179(4):1041-52. Epub 2015 Aug 26.

Animal Behaviour, University of Bielefeld, Bielefeld, Germany.

Foraging differentiation within a species can contribute to restricted gene flow between ecologically different groups, promoting ecological speciation. Galapagos sea lions (Zalophus wollebaeki) show genetic and morphological divergence between the western and central archipelago, possibly as a result of an ecologically mediated contrast in the marine habitat. We use global positioning system (GPS) data, time-depth recordings (TDR), stable isotope and scat data to compare foraging habitat characteristics, diving behaviour and diet composition of Galapagos sea lions from a western and a central colony. We consider both juvenile and adult life stages to assess the potential role of ontogenetic shifts that can be crucial in shaping foraging behaviour and habitat choice for life. We found differences in foraging habitat use, foraging style and diet composition that aligned with genetic differentiation. These differences were consistent between juvenile and adult sea lions from the same colony, overriding age-specific behavioural differences. Our study contributes to an understanding of the complex interaction of ecological condition, plastic behavioural response and genetic make-up of interconnected populations.
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http://dx.doi.org/10.1007/s00442-015-3424-1DOI Listing
December 2015

High intraspecific ability to adjust both carbon uptake and allocation under light and nutrient reduction in Halimium halimifolium L.

Front Plant Sci 2015 7;6:609. Epub 2015 Aug 7.

Ecosystem Physiology, University of Freiburg Freiburg, Germany ; AgroEcosystem Research, Bayreuth Center of Ecology and Environmental Research (BayCEER), University of Bayreuth Bayreuth, Germany.

The allocation of recently assimilated carbon (C) by plants depends on developmental stage and on environmental factors, but the underlying mechanisms are still a matter of debate. In the present study, we investigated the regulation of C uptake and allocation and their adjustments during plant growth. We induced different allocation strategies in the Mediterranean shrub Halimium halimifolium L. by a reduction of light (Low L treatment) and nutrient availability (Low N treatment) and analyzed allocation parameters as well as morphological and physiological traits for 15 months. Further, we conducted a (13)CO2 pulse-labeling and followed the way of recently assimilated carbon to eight different tissue classes and respiration for 13 days. The plant responses were remarkably distinct in our study, with mainly morphological/physiological adaptions in case of light reduction and adjustment of C allocation in case of nutrient reduction. The transport of recently assimilated C to the root system was enhanced in amount (c. 200%) and velocity under nutrient limited conditions compared to control plants. Despite the 57% light reduction the total biomass production was not affected in the Low L treatment. The plants probably compensated light reduction by an improvement of their ability to fix C. Thus, our results support the concept that photosynthesis is, at least in a medium term perspective, influenced by the C demand of the plant and not exclusively by environmental factors. Finally, our results indicate that growing heterotrophic tissues strongly reduce the C reflux from storage and structural C pools and therefore enhance the fraction of recent assimilates allocated to respiration. We propose that this interruption of the C reflux from storage and structural C pools could be a regulation mechanism for C translocation in plants.
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http://dx.doi.org/10.3389/fpls.2015.00609DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4528176PMC
August 2015