From community ecology to functional ecology
Describing the communities
The first steps of ecology have been characterized by descriptive and classification tasks. What is a species? How can we classify them? How many species are living in a given place?
The word “species” has received considerable attention in biology for hundreds of years. It all began with the idea of classifying and giving names to plants, animals, etc in order to make oneself understood and to communicate, but also to get a more comprehensible pattern of the diversity observed in Nature and to order it. At the beginning, the species concept did not require any precise definition and all the animals that looked like a sheep were called a sheep. Then, with the discovery of new unidentified organisms, things started to get more complicated. It called for precisely define what a species was. But since the word “species” appeared in the scientific literature, its meaning has been evolving into a multitude of definitions (24 species concepts, Mayden 1997). The biological species concept (BSC) has been introduced by Mayr in 1957. It is still the most used and popular concept: a species is defined as a “group of interbreeding natural populations that are reproductively isolated from other such groups”. Moreover, offspring have to be fertile. The main problem with BSC is that most of the life on the planet does not reproduce sexually but asexually (cloning, vegetative reproduction) (Ereshefsky 2010) and inter-specific hybridizations are common, e.g. within plants. Following the BSC concept of species, asexual organisms would actually not form species. The phylogenetic species concept (PSC) is complementary as it is not only used to sort organisms but also consider their evolution. Many other species concepts are found in the literature. We could see this pluralist approach as sterile discussion among scientists, but it actually illustrates the multitude of research approaches and the points of view used to approach the organization of living organisms. Each concept has its limits and weaknesses, but the main question is: “What does best fit the biological question?” Those old concerns are still questioned and some researchers keep working on the way of sorting living organisms (de Queiroz 2007). As stated above, one of the old questions in ecology also deals with the evaluation of biodiversity. Species are considered as one of the fundamental units in ecology. With the definition of the “biodiversity”, we can easily conceive why. The term “biodiversity” has been defined as “the variability among living organisms from all sources including, inter-alia, terrestrial, marine and other aquatic ecosystems, and the ecological complexes of which they are part: this includes diversity within species, between species and of ecosystems” (definition from the Convention of Biological Diversity, Rio de Janeiro, 1992). Given the central place given to the species-level, the multitude of species concepts remains problematic in the case of biodiversity assessment: depending on the species definition and the classification we choose, it will give different estimates of biodiversity. Recently, Cadotte et al. (2010) used the two concepts stated above (BSC and PSC) to propose a new assessment method of biodiversity index based on phylogeny. They integrated the species richness (number of species in a community), their abundance and their evolutionary ecology. Consequently, they assumed that a community composed of three closely related species would be less diverse than a community composed of three phylogenetically distant species. In addition, different indices can be used to estimate the diversity: the species richness (number of species in a community), the Gini-Simpson index and the Shannon index (both take into account the richness and the evenness), all grouped into the Hill numbers considered as a general approach to measure diversity (Hill 1973, Chao et al. 2014). Finally, the scale of the taxonomic diversity measurement has been discussed by Whittaker in 1960, who proposed different measurements, such as the local diversity (α-diversity), regional diversity (γ-diversity) and the between site diversity index (β-diversity). The choice of the classification, the index and the scale of diversity measurements can influence the estimation of diversity, and these questionings are still at the heart of community ecology studies.
Characterizing the assemblage of species
The following questions concern the assemblages of species within communities. Why are there more species in some places than in others? How do species interact and coexist within a community? Does one facilitate the development of another? Is there competition? What are the relative influences of temperature and soil characteristics in the complexity of plant communities? How does composition evolve temporally?
Ecological niche is defined as a hypervolume with n-dimensions (Hutchinson 1957) which holds all the environmental conditions that allow a species to have a positive growth rate (Grinnell 1917). This complete hypervolume is called the “fundamental niche”, however it cannot be estimated as it is not possible to test all the conditions where the species could persist (Panzacchi et al. 2014). The niche that we observe is the “realized niche” and is shaped by the biotic interactions and the limitations of dispersion. Therefore, the realized niche can fluctuates with changes in the environment. Other concepts are linked to the ecological niche. The “Grinnellian niche” (Grinnell 1917) refers to the species requirements essential for its survival, while the “Eltonian niche” (Elton 1927) refers to how a species impacts its local environment (the “function”). In both cases, the concept of resources is central, whatever the niche definition.
The aims of community ecology as a scientific discipline are to answer those questions and to elucidate the processes underlying the composition pattern of communities. In this context, 4 approaches mainly focus on the ecological interactions among organisms and with their abiotic environment. The interactions among organisms (competition, facilitation, predation, parasitism, symbiosis, mutualism, neutralism, commensalism) happen on a single or several axis of the species ecological niche (box 1) such as food, time or space.
Species can compete on the spatial axis, but not on the food axis if food resources used by the species are not limiting. Facing the global environmental changes discussed above, species need to adapt their habitat, diet selection or their activity rhythm; or to move or to die. Similarly to the ecological niche, interactions among species can be summarized as a hypervolume with n-dimensions, where n represents the number of interactions a species maintained with the n other species. During this thesis, I mainly focused on the dietary (or feeding) niche of species. Without additional information, the word “niche” should be interpreted as “dietary (or feeding) niche”.
Finding general rules in community structuration
More recent questions have emerged to understand how the assemblage of species works. What are the functions of the species in the community? How does a certain assemblage of species influence the ecosystem processes? How can we generalize our local conclusions to more general pattern at a wider scale?
The taxonomic vision does not reflect the function of organisms and does not allow to give general principles about community assembly (Cornwell & Ackerly 2009, Spasojevic and Suding 2012, Mason et al 2012), neither to predict the abundance of species (Shipley et al. 2006, Laughlin et al 2012), nor to understand the influence of organisms on ecosystem functioning (Diaz & Cabido 2001, Lavorel & Garnier 2002). About 25 years ago, the functional approach of communities has been introduced (Lavorel & Garnier 2002, Cornelissen et al. 2003, Violle et al. 2007) in a context where ecologists were wondering if universal laws could also govern ecology (Lawton 1999, McGill et al. 2006).
Based on individuals, the functional ecology describes the organisms with their biological characteristics (e.g. vegetative height, specific leaf area, root density) and their functions (e.g. light interception, resource intake, nutrient and water absorption) within their environment instead of describing them with their taxonomic identity (Calow 1987). Following the review of “traits” definitions given by Violle et al. (2007), that details how the meaning of the term “trait” varies among studies, we used the definition of traits at the individual-level following Garnier & Navas (2013), i.e. “a trait is any morphological, physiological or phenological feature measurable at the level of individual only, from the cell to whole-organism level, without reference to the environment or any other level of organization”. According to this definition, a trait is not influenced by environmental factors or other level of organization (Violle et al. 2007). Species that are taxonomically different can actually be similar in terms of functions and biological characteristics (morphological, chemical, phenological, biomechanical measurements). These features that have a direct impact on the fitness (survival, growth or reproduction) are called functional traits (Lavorel et al. 1997, Violle et al. 2007). The value of a functional trait is the result of compromises among the different functions of the plants (Diaz & Cabido 1997). The use of independent functional traits allows describing general plant functional strategies useful for the understanding of ecosystem functioning (Lavorel et al. 1997). For example, leaf dry matter content (LDMC) is negatively correlated with specific leaf area (SLA): species with strong LDMC (weak SLA) are composed of a low density of foliar tissue, a low photosynthetic rate not allowing a high resource intake but a high conservation ability, and in turn a slow growth rate. These species are called “conservative” species. The opposite are the “exploitative” species and are dominant in fertile environment (Grime et al. 1997, Reich et al. 1999).
In absolute terms, taking into account the individual variability would theoretically allow completely overcoming the species concept (Albert et al. 2010, Albert et al. 2012). However, this requires a huge amount of work and because a species trait is usually the mean trait value measured from some individuals, it does not overcome the species concept. The use of well-chosen functional traits can however reveal general functions and strategies not determined with the single taxonomic approach. However, nowadays, the importance of intra-specific variability is highly studied (Albert et al. 2012, Violle et al. 2012, Albert et al. 2015) and its omission could lead to misinterpretations of ecosystem functioning. This is discussed hereafter in 1.3.
The functional approach is useful as indicator of population/community structure, dynamics and assembly at local (Kraft et al. 2008, Angert 2009) and biogeographic scales (Swenson 2010, Siefert 2013), to quantify functional diversity of communities (de Bello et al. 2009), to describe the relationships between traits (Reich et al. 1997, Wright et al. 2004, Onoda et al. 2011), to describe the distribution of traits according to environmental gradients (Thuiller et al. 2004, Albert et al. 2010), to relate functioning of ecosystems and services associated (Diaz et al. 2007a), to explain the relationship between traits and fundamental/realized niche (McGill et al. 2006), to mechanistically understand trophic network (Ibanez et al. 2013a) or to predict community response to disturbance (Deraison et al. 2015). For example, plant functional traits such as plant height, or leaf mass, are well correlated to herbivory pressure (Diaz et al. 2001). Although the relationship between traits and herbivory pressure is usually non-linear, it is possible to predict the response of easily measurable plant traits to grazing, even in communities that are taxonomically diverse. Indeed, cattle grazing tends to favor annual over perennial plants, short plants over tall plants, rosette and stoloniferous rather than tussock architecture, prostate rather than erect forms (Diaz et al. 2007b). Consequently, the functional approach allows a more mechanistic understanding of the forces shaping the communities and their dynamics, and to generalize results across organisms and ecosystems (McGill et al. 2006).
Nowadays, researchers are trying to reveal general ecological theories of community assembly (Pavoine & Bonsall 2011) through the combination of indices of diversity based on traits (functional richness, functional evenness, functional divergence, functional dispersion, Mason et al. 2005, Villéger et al. 2008, Laliberté & Legendre 2010), taxonomy and phylogeny (Pavoine & Bonsall 2011 and references therein). Especially, several studies tried to relate the diversity of traits with species diversity (Mayfield et al. 2005, Holdaway & Sparrow 2006, Grime 2006, Villéger et al. 2010). Some of these studies demonstrate the absence of relationship between trait and species diversity (Mason et al. 2008), which emphasizes their complementary use. In this thesis, we particularly used the twofold taxonomic and functional approach in the study of the coexistence between chamois (Rupicapra rupicapra) and mouflon (Ovis gmelini musimon) on the feeding axis of the ecological niche (paper II). Indeed, knowing the plant species eaten by two species is helpful to study the inter-specific competition, as the food limitation acts at the plant species level. If two primary consumers compete for the same plant species, according to the competitive exclusion concept, they can be forced to feed on different plant species (taxonomic niche), but reach the same energy requirements (functional niche), which would not impact their dynamic. The complementary use of these two approaches at different scales could sharply change our vision of community structure.
Downscaling ecological studies at the intra-specific level in order to better understand the dynamic of communities and ecosystem functioning
Most of the studies on niche in community ecology focus on the mean trait of species, suggesting that individuals behave in the same way (Layman et al. 2015). For example, when investigating the inter-specific interactions between chamois and sheep, La Morgia & Bassano (2009) limited their overlap measurement to the mean diets of species. However, as already stated by Darwin (1859), individuals can differ because of genetic diversity or phenotypic plasticity (Byars et al. 2007), or because biotic interactions alter their trait value (e.g. competition, Gross et al. 2009). For example, in the case of plant species, the inclusion of intra-specific variability can help to distinguish populations that differ in their trait values along environmental gradients (Albert et al. 2010). Summarizing data with species-mean values overestimates the contribution of rare species (Paine et al. 2011). Therefore, the omission of intra-specific variability can lead to misinterpretation of community functioning (Jung et al. 2010). For instance, aboveground net primary productivity (ANPP) increased with plant genotypic diversity because of higher niche complementarity, in an experimentally low diverse community (Crutsinger et al. 2006). If the objective of a study is to determine the factors influencing the ANPP, then the omission of intra-specific variability could prevent a correct interpretation of results. In the study of La Morgia & Bassano (2009), if the overlap measurement had been measured between all pairs of individuals instead of between the mean diets of chamois and sheep, they could have been able to determine whether only a subset of chamois individuals were affected by sheep. This information can be particularly important to solve management problems and change our vision of species conservation (Bolnick et al. 2003). Indeed, protecting the habitat of a species based on the mean habitat preferences whereas the species displays a strong among-individual variation is not adapted.
Because natural selection, and then adaptation, acts at the individual level, studying the intra-specific variability is essential to understand how populations adapt to their environment and figure out the evolution of their realized niche (Tinker et al. 2008, Pires et al. 2013, Salvidio et al. 2014). When food resource decreased in autumn, salamander populations increased their population niche breadth thanks to a strong diet specialization of individuals on alternate food items (Salvidio et al. 2014). Without this multi-level approach, authors would have not been able to explain the mechanism responsible of the population niche breadth increase. These improvements could also help to better predict how a population or a species would numerically, spatially and behaviorally respond to environmental changes (Bolnick et al. 2011). For example, if one of the resources used by an herbivore population with a high among-7 individual variability decreases, only a subset of individuals would be impacted. Without among-individual variation measurement, predictions about the evolution of the population would have led to suggest that all the individuals suffered from the decrease of the resource, and we would have predicted a decrease of the whole individual’s fitness instead of only some individuals. Hence, including the intra-specific variability in models describing the population dynamic could help to improve the predictive power of the study (Bolnick et al. 2003).
Intra-specific variation can also affect ecological interactions and in turn community assembly (Hughes et al. 2008, Bolnick et al. 2011), both in low diversity communities (Crutsinger et al. 2006, Hughes et al. 2008) and in more diverse systems (Cornwell & Ackerly 2009, Jung et al. 2010, Paine et al. 2011). For instance, the increase in the resource diversity available to herbivores increased the arthropod richness thanks to associations between particular herbivores and particular host-plant genotype, hence favoring the number of ecological interactions between plants and herbivores (Crutsinger et al. 2006). In a context of increasing spatial overlap among species due to an increase of population size, a stronger inter-specific competition could differentially impact the individuals of a targeted species according to its degree of among-individual variation. Indeed, it is only a subset of individuals (fig.1a) or all the individuals (fig.1b) that could be affected by an overlapping species (in red in fig.1). Hence, intra-specific variation promotes species coexistence by limiting similarity with competing species and by adjusting the trait values of individuals and species to their abiotic requirements (environmental filtering, Jung et al. 2010). Individual-level data appear as a more sensitive indicator of niche differentiation and environmental filtering than species-mean data (Jung et al. 2010).
Given the importance of intra-specific variability in communities response to environmental changes, in biodiversity assemblage or in network functioning (Dupont et al. 2014, Willmer & Finlayson 2014, Tur et al. 2015), an increasing number of researchers try to take it into account. For example, Tur et al. (2014) downscaled the understanding of plant-pollinator network at the intra-specific level and showed that the different parameters (linkage density, connectance, nestedness, interaction diversity) describing the structure of networks significantly changed in response of a high degree of individual specialization.
Including the intra-specific variability within ecological studies is not only useful to explain spatial or fine-temporal community composition variation, but also to explore evolutionary processes at a larger temporal scale. Indeed, in an evolutionary perspective, because environmental filters act at the individual-level, different survival, growth and reproduction can be observed among individuals leading to changes in allele frequencies, which in turn may modify the evolution of the population through natural selection (Bolnick et al. 2003).
Table of contents :
CHAPTER I: HOW TO GET EXCITED ABOUT ECOLOGY
1.1 PICTURE OF THE ACTUAL WORLD
1.2 FROM COMMUNITY ECOLOGY TO FUNCTIONAL ECOLOGY
1.3 DOWNSCALING ECOLOGICAL STUDIES AT THE INTRA-SPECIFIC LEVEL IN ORDER TO BETTER
UNDERSTAND THE DYNAMIC OF COMMUNITIES AND ECOSYSTEM FUNCTIONING
CHAPTER II: THEORETICAL CONTEXT
2.1 LARGE HERBIVORES AS A GOOD STUDY MODEL
2.2 DIET AS A LINKAGE BETWEEN TWO TROPHIC LEVELS
MATERIAL & METHODS
CHAPTER III: ROE DEER, CHAMOIS AND MOUFLON IN THE BAUGES MASSIF
3.1 BAUGES MASSIF
3.2 THIS WORK TAKES PLACE IN AN ALREADY WELL-STUDIED ECOSYSTEM
3.3 STUDIED SPECIES
CHAPTER IV: OVERVIEW OF DATABASES
4.1 DNA-METABARCODING AS THE METHOD TO IDENTIFY THE DIETS (PAPERS I-II-III-NOTE)
4.2 PLANT FUNCTIONAL TRAITS MEASUREMENTS (PAPERS II-III-NOTE)
4.3 NIRS MEASUREMENTS (PAPERS IV-NOTE)
4.4 RESOURCE AVAILABILITY (PAPERS II-III)
4.5 SYNTHETIC VIEW OF THE DATABASES USED FOR EACH ANALYSIS
SUMMARY OF RESULTS
CHAPTER V: GENERAL INFORMATION ABOUT THE DIETS
5.1 DATABASE INFORMATION
5.2 PLANT SPECIES IDENTIFIED IN FAECES
CHAPTER VI: RESULTS FROM PAPERS AND ADDITIONAL ANALYSES
6.1 FROM COMMUNITY TO INDIVIDUALS (PAPER I)
6.2 THE RELATIVE IMPORTANCE OF FOOD QUANTITY AND QUALITY IN THE LARGE HERBIVORE DIET SELECTION (PAPERS II-III)
6.3 HOW DO INTRODUCED SPECIES INFLUENCE PLANT-HERBIVORE INTERACTIONS? ARE INTRODUCED SPECIES ALWAYS HARMFUL FOR ECOSYSTEMS? (PAPERS II-III)
6.4 THE UNEXPECTED IMPORTANCE OF BIOMECHANICAL TRAITS IN THE LARGE HERBIVORE DIET SELECTION CRITERIA (PAPER III)
6.5 A BIT OF METHODOLOGY: IS THE USE OF NIRS RELEVANT AND USEFUL FOR ESTIMATING DIET AND PLANT QUALITY? (PAPERS IV-NOTE)
SYNTHESIS, PERSPECTIVES & DIRECTIONS
7.1 METHODOLOGICAL CONSIDERATIONS
7.1 PLANT-HERBIVORES INTERACTIONS
7.3 INTEGRATING FUNCTIONAL INTERACTIONS BETWEEN LARGE HERBIVORES AND PLANT
COMMUNITIES INTO SPECIES DISTRIBUTION MODELS
LIST OF APPENDICES 13