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Carbon and nitrogen cycles as ecological crossroads
The C and N cycles occupy a central role in ecosystem studies. In most ecosystems, the solar energy fixed in carbohydrates (assembled from CO2 and water) by plants during photosynthesis forms the basis of most available energy that is used by organisms that feed on living or dead plant material and which then circulates through foodwebs. The C compounds produced by plants also make up important “structures” in terrestrial ecosystems, such as the living plants themselves, dead wood, soil litter and soil organic matter (Bormann & Likens, 1979). The amount of plant primary production partly determines the amount of microbes and animals that can be sustained in an ecosystem. The recycling of organic matter by soil microbes and animals is a key process controlling the availability of major nutrients for plants. N is considered to be the major limiting nutrient for primary production (Vitousek, 1982; Vitousek & Howarth, 1991; Gruber & Galloway, 2008), and the C and N cycles are tightly coupled. The availability of N strongly constrains primary production and thus C inputs into ecosystems, notably because important amounts of available N are required to synthetize the proteins that constitute the enzymatic apparatus of photosynthesis (e.g., van Groenigen et al., 2006). N foraging strategies by plants, in turn, can have strong influences on C cycling, for instance by increasing belowground C allocation and providing fresh organic matter to soils, which can increase decomposition rates by soil biota and in turn lead to increased N availability (e.g., Bardgett et al., 2014; Shahzad et al., 2015). C and N acquisition strategies both can differ among plant species and are the object of numerous cooperative and competitive interactions between plants, plants and soil microbes and between soil microbes. Herbivory, pollination and even feedbacks from predation can also interact with C and N cycling. Through the production of greenhouse gases such as CO2, CH4 and N2O, C and N dynamics are also of significant importance for global biogeochemistry and climate (e.g., Schimel, 1995; Gruber & Galloway, 2008; Philippot et al., 2008; Ostle et al., 2009).
The C and N cycles are thus at the crossroads of numerous ecological interactions that link aboveground and belowground components of ecosystems (e.g., Tateno & Chapin, 1997; Wardle et al., 2004) and they strongly constrain, and are shaped by, biotic processes. As such, they are also a precious focal point for the investigator, as changes in these dynamics can help detect ecosystem changes and infer some of their causes, e.g., during ecosystem formation and development. Accordingly, they are at the heart of the core research areas of the US Long Term Ecological Research (LTER) network3 and have early on been proposed as key indicators of ecosystem development and stability (Odum, 1969) and as key attributes to monitor the success of ecological restoration projects (Aronson et al., 1993).
Furthermore, human influences on C and N cycles are major components of anthropogenic global environmental changes (Vitousek et al., 1997a; Ciais et al., 2013; Waters et al., 2016) and “markers” of the Anthropocene (Waters et al., 2016). Atmospheric CO2 concentrations have increased by 40 % between 1750 and 2011 (from 278 ppm to 390.5), with the most part due to the burning of fossil fuels (Ciais et al., 2013). This increase in CO2 can have several consequences at the individual plant level, as well as at the community and the ecosystem levels (Bazzaz, 1990), and many uncertainties remain as to how ecosystems will respond to rising CO2 concentrations on the long-term, and how these responses will feed back to global C biogeochemistry. For instance, terrestrial biogeochemical models attribute a “fertilization effect” to increased CO2 levels, in order to explain the magnitude of the terrestrial C sink (Ciais et al., 2013). However, potential nutrient and/or water limitation of primary production in the future make the long-term magnitude of this effect rather uncertain (Ciais et al., 2013).
The strong human influence on the N cycle also adds uncertainties about the future of Earth. Prior to the intensification of human activities, N could enter ecosystems through atmospheric deposition of “reactive” N species produced in the atmosphere by lightning, or through the microbial fixation of N2 by free or symbiotic bacteria (Vitousek et al., 1997b). It is estimated that human activities, through industrial N fixation (Haber-Bosch process), combustion processes and legume crops, now inject an amount of reactive N into the biosphere that is equivalent to all natural atmospheric, terrestrial and marine sources combined (Gruber & Galloway, 2008; Ciais et al., 2013).
This added N, especially for ecosystems that were N-limited, can have profound effects on N cycling rates in ecosystems. The additional N can stimulate plant growth and be retained in plant biomass and soil organic matter, but an important body of research has shown, through observational, experimental and modeling works, that added N can lead to increased losses through leaching or through gaseous emissions after microbial transformation in soils (Aber et al., 1989, 1998; Pardo et al., 2006; Lovett & Goodale, 2011; Niu et al., 2016). This phenomenon, where additional N inputs lead to increased N losses, has been coined “N saturation” (Aber et al., 1989; Niu et al., 2016). It is assumed that it is due to N inputs exceeding the capacity of plants and soils to retain added N, leading to more N being available to enter N loss pathways such as nitrification and denitrification (Lovett & Goodale, 2011; Niu et al., 2016). Many unknowns remain concerning the response of ecosystem N cycling to added N, such as the proportion of N that is retained or lost, the dominating retention and loss processes, or the precise chain of mechanisms linking the deposition of N to a saturation syndrome (Niu et al., 2016).
Overview of urban studies on carbon and nutrient cycling
Urban environments have been shown to have profound, yet still poorly understood effects on C and N cycling in ecosystems (De Kimpe & Morel, 2000; Scharenbroch et al., 2005; Kaye et al., 2006; Lorenz & Lal, 2009; Pouyat et al., 2010). There are only few syntheses and meta-analyses covering the topic, and besides papers synthetizing specific research programmes (e.g., McDonnell et al., 1997; Pickett et al., 2011) there is, to my knowledge, no international synthesis covering urban C and N biogeochemistry.
Authors have suggested that the importance of urban drivers on ecosystem processes, and their similarities across cities, could surpass natural drivers and lead to similar ecosystem responses on key ecological variables in different cities, an asumption coined the “urban ecosystem convergence hypothesis” (Pouyat et al., 2003, 2010; see also Groffman et al., 2014). If studies have indeed reported patterns of urban soil C and N accumulation worldwide (e.g., McDonnell et al., 1997; Ochimaru & Fukuda, 2007; Chen et al., 2010; Raciti et al., 2011; Gough & Elliott, 2012; Vasenev et al., 2013; Huyler et al., 2016), important unknowns remain, however, on the mechanisms leading to such accumulation.
The body of research conducted in the Urban-Rural Gradient Ecology (URGE) programme provides a good illustration of the interactive effects of urban biotic and abiotic factors on C and N biogeochemistry. The studies conducted between 1989 and 1997 in the New York metropolitan area in the URGE programme probably constitute the first intensive research conducted on urbanization effects on C and N cycling. The programme used a transect of 9 unmanaged forest sites (dominated by Quercus rubra and Quercus velutina) spanning 140 km from the Bronx borough in New York City (NYC) to rural Litchfield County, Connecticut (McDonnell et al., 1997; Carreiro et al., 2009). The studies conducted in the URGE programme mainly focused on the decomposition rates of leaf litter and N cycling. Initially, the underlying rationale was that these processes would integrate a possible urban influence, through changes in leaf litter chemistry (e.g., response to ozone) and changes in microbial processes associated to temperature and pollutants (McDonnell et al., 1997; Carreiro et al., 2009).
Decomposition rates in urban stands were found higher than in the rural stands, despite a lower chemical quality (attributed to ozone exposure) for decomposers (Pouyat et al., 1997; Carreiro et al., 1999). Higher N mineralization and much higher nitrification rates were also found in the urban stands, and despite a faster turn-over rate of litter, urban stands contained a larger stable C pool (Zhu & Carreiro, 1999, 2004a, 2004b; Pouyat et al., 2002; Carreiro et al., 2009). Urban litter was also shown to contain less microbial biomass (both fungal and bacterial) than rural stands (Carreiro et al., 1999). These rather puzzling patterns were found to be best explained by an up to ten-fold higher abundance of earthworms in urban stands (Steinberg et al., 1997), with urban earthworm populations being mostly composed of two exotic epigeic species. Their activity was experimentally associated to faster litter decay, higher N mineralization and nitrification, and C sequestration in microaggregates inside casts was seen as a possible explanation for a larger stable C pool in urban stands (McDonnell et al., 1997; Pouyat et al., 2002; Carreiro et al., 2009). Other factors, such as higher temperatures in urban stands, higher heavy metal content in urban soils and long-term exposure to higher atmospheric N deposition rates (Lovett et al., 2000) are considered to possibly interact with the influence of earthworms (Pouyat & Turechek, 2001; Pouyat & Carreiro, 2003; Carreiro et al., 2009). For instance, the strong stimulation of nitrifiers by earthworms could make nitrifiers more prompt to nitrify the ammonium deposited from the atmosphere, thus leading to even higher nitrification rates (Carreiro et al., 2009). Other studies conducted on this gradient have, for instance, shown a decrease in methane uptake by urban soils (Goldman et al., 2005) and reduced mycorrhization in urban sites when compared to rural sites (Baxter et al., 1999). Detailed summaries of the URGE programme results can be found in McDonnell et al. (1997), Cadenasso et al. (2007), Carreiro et al. (2009) and Pouyat et al. (2009).
Studies conducted in other cities have reported similar results. Koerner & Klopatek (2010) conducted a study in and around Phoenix (Arizona) on communities dominated by the bush Larrea tridentata and found higher levels of soil organic C, total N and nitrate levels in urban sites but found higher soil respiration rates in rural sites, possibly because of reduced soil moisture and litter quality in urban sites. Urban sites did not show the island of fertility effect observed in more natural communities dominated by L. Tridentata: urban interplant soils contained similar levels of total N and nitrate than soils under plant canopy. Higher N levels in urban sites were attributed to higher atmospheric N depositions in urban sites, which were also considered to cause the disappearance of the “fertility island” pattern in urban sites. Rao et al. (2013) studied N deposition levels and the fate of deposited N on an urban-rural gradient spanning 100 km westward from Boston (Massachusetts). They showed that urban sites received almost twice as much N, mostly in the form of ammonium, than rural sites. Dual isotope analysis of leached nitrate showed that, for 5 of their 9 studied sites, the leached nitrate came almost entirely from nitrification in soils, suggesting that deposited N is first microbially transformed before leaching. In France, Pellissier et al. (2008) report significantly higher nitrate concentration in urban soils than in soils from peri-urban and rural sites in and around Rennes, which was attributed to higher N deposition.
The long-term carbon and nitrogen dynamics in “Haussmannian ecosystems” as a case study
In the first months of this research, I started to discuss with city managers in Paris, both to better understand green space management in Paris and, importantly, to obtain the authorization (see Appendix 2) to do fieldwork in Paris. These discussions proved very useful to identify the case study that I would work on, namely the tree plantations that populate Parisian sidewalks.
The establishment of street plantations in Paris rests on similar principles since the 19th century and the Haussmannian works that introduced street tree plantations as part of the Parisian landscape (Pellegrini, 2012). When planting a new sapling (of age 7-9), a pit about 1 m 30 deep and 3 m wide is opened in the sidewalk and filled with a newly imported peri-urban agricultural soil (Paris Green Space and Environmental Division, pers. comm.). If soil is already in place for a previous tree, it is entirely excavated, disposed of and replaced by a newly imported agricultural soil from the surrounding region. Tree age thus provides a good proxy of soil-tree system age, e.g., the time that a tree and soil have interacted in street conditions (Kargar et al., 2013, 2015). Aboveground litter is completely exported and no fertilizers are applied by city managers. Thus, they were pretty appealing for someone interested in the dynamics of systems very much directly exposed (e.g., Bettez et al., 2013) to a range of typical urban factors (traffic and domestic gaseous emissions, high amounts of impervious surface and thus a strong heat island effect, strong human density etc.). As systems dominated by trees, very long-lived organisms, they also seemed suited for studying the long-term response of soil-plant systems to the city (Calfapietra et al., 2015). They also seemed to constitute an interesting case study from a C and N cycling perspective. They were systems where the combination of aboveground litter exportation, exogenous N inputs (atmosphere, animals), uncertainties about root ecology, and more generally about soil ecology and long-term tree response to the street environment, made it particularly challenging – and interesting! – to try and predict the temporal trends that could be found in C and N cycling.
Furthermore, in the Parisian context, the potential existence of long-term trends in street plantation biogeochemistry is also of interest for city managers. It is currently assumed that soils get exhausted in nutrients with time and that when replacing a tree, existing soils must be replaced by a newly imported peri-urban soil. This “soil exhaustion” hypothesis has never been tested empirically, which implied that a study on long-term C and N cycling in Parisian street soil- tree systems could also help assess whether the assumption of a time-related soil exhaustion, on which current practices are based, could be confirmed or not. For ecologists, contrary to the soil exhaustion hypothesis, the fact that plants (especially perennials), through the accumulation of dead and live plant material and microbial biomass in soils, can lead to an increase in soil organic matter and nutrients and have a “fertility island” effect in the landscape (e.g., Jackson & Caldwell, 1993; Mordelet et al., 1993) is well established. However, as stressed above, whether this applies to street systems is a rather opened question.
Studying temporal dynamics of urban soil-plant systems might also help anticipate their future trajectories in a changing environment, which has received relatively little attention. For instance, current estimates of the cooling potential of urban soil-plant systems might not reflect their future potentials, if plant productivity and evapotranspiration come to be affected by water shortages imposed by climate change. The focus, currently, is so to speak more on how to use ecosystems for urban climate change adaptation, but how urban ecosystems will themselves adapt to climate change is highly uncertain and a relatively opened question (Rankovic et al., 2012). This has important consequences for projects of urban ecological engineering, because it can impede the long-term efficiency of projects. It is also important for adjusting the care provided to urban streets and soils, to improve their own living conditions.
On this point, some very basic features of street soil-tree systems are very poorly known. There is a rather widespread acknowledgement that urban trees have a shorter lifespan than their rural or forest conspecifics (Quigley, 2004; Roman et al., 2015). However, the causes of this decline seems nor well identified nor much hierarchized in the literature. In terms of design choices, some fundamental aspects can be in cause. For instance, tree pit size (surface, volume) seems to be a critical point for tree growth and lifespan, probably because of the constraints it imposes on water infiltration and overall available water and nutrient quantities for trees (Kopinga, 1991; Day & Amateis, 2011). In Paris, because of space constraints on sidewalks, the current policy leads to numerous trees being planted in even smaller soil volumes, which could prove harmful to trees. A study of long-term C and N cycling could also bring information, for instance via the detection of signs of nutrient limitation or water stress, to the discussion of how trees fare under current practices and what could be done to improve their situation.
Table of contents :
SUMMARY
EXTENDED SUMMARY
REMERCIPDFEMENTS
TABLE OF CONTENTS
GENERAL INTRODUCTION
1. ECOLOGY AND THE FIRST URBAN CENTURY
2. CARBON AND NITROGEN DYNAMICS IN URBAN ECOSYSTEMS
2.1. Carbon and nitrogen cycles as ecological crossroads
2.2. Overview of urban studies on carbon and nutrient cycling
3. THE LONG-TERM CARBON AND NITROGEN DYNAMICS IN “HAUSSMANNIAN ECOSYSTEMS” AS A CASE STUDY
CHAPTER 1 LONG-TERM TRENDS IN CARBON AND NITROGEN CYCLING IN PARISIAN STREET SOIL-TREE SYSTEMS
1. INTRODUCTION
2. MATERIALS AND METHODS
2.1. Site description and chronosequence design
2.2. Sample collection and processing
2.3. Soil characteristics
2.4. C and N contents and isotope ratios
2.5. Statistical analyses
3. RESULTS
3.1. Soil characteristics
3.2. Soil C and N contents and isotope ratios
3.3. Foliar δ13C and δ15N and N content
3.4. Soil and plant coupling
4. DISCUSSION
4.1. Age-related trends in soil organic C: Accumulation of root C?
4.2. Age-related trends in N cycling: Rapid N saturation of street systems?
4.3. Uncertainties linked to potential legacy effects
5. CONCLUSION
CHAPTER 2 LEGACY OR ACCUMULATION? A STUDY OF LONG-TERM SOIL ORGANIC MATTER DYNAMICS IN HAUSSMANNIAN TREE PLANTATIONS IN PARIS
1. INTRODUCTION
2. MATERIALS AND METHODS
2.1. Site description and chronosequence design
2.2. Sample collection and processing
2.3. Soil characteristics
2.4. Physical fractionation procedure
2.5. Mineralogical analysis of clay fractions by X-ray diffraction
2.6. C and N contents and isotope ratios
2.7. Soil incubation, CO2 and 13C-CO2 analysis
2.8. Statistical analyses
3. RESULTS
3.1. Soil texture, quality of fractionation and clay minerals
3.2. Soil C and N contents and isotope ratios
3.3. Root C and N contents and isotope ratios
3.4. C mineralization and δ13C-CO2
3.5. Soil and plant coupling
4. DISCUSSION
4.1. Evidence of recent C and N accumulation in street soils
4.2. Possible mechanisms for root-C accumulation in street soils
4.3. Street trees diversify their N sources
5. CONCLUSION
CHAPTER 3 STRUCTURE AND ACTIVITY OF MICROBIAL N-CYCLING COMMUNITIES ALONG A 75-YEAR URBAN SOIL-TREE CHRONOSEQUENCE
1. INTRODUCTION
2. MATERIALS AND METHODS
2.1. Site description and chronosequence design
2.2. Sample collection and processing
2.3. Real-time quantitative PCR
2.4. Potential nitrifying and denitrifying activities
2.5. Statistical analyses
3. RESULTS
3.1. Abundances of soil AOB and AOA
3.2. Abundances of soil bacterial denitrifiers
3.3. Potential nitrification and denitrification
3.4. Correlations among microbial parameters and between microbial, soil and plant parameters
in street systems
4. DISCUSSION
5. CONCLUSION
GENERAL DISCUSSION
1. THE LONG-TERM DYNAMICS OF HAUSSMANNIAN ECOSYSTEMS: A SCENARIO
1.1. Summary of chapters
1.2. Possible interpretations for long-term C and N dynamics in street systems
1.3. Beyond silver lindens? Insights from black locust plantations and pollinators
2. PERSPECTIVES FOR FUTURE WORKS AND STREET PLANTATION MANAGEMENT
3. “GLOBAL CHANGE IN YOUR STREET!”: ECOLOGY IN THE FIRST URBAN CENTURY
REFERENCES
