Functional trait diversity of herb species in The Jena Experiment: Plastic responses or genetic variability?

Abstract

Background
Human activities have caused rapid and continuous changes to the environment on local and global scale. These alterations lead to dramatic changes in the biotic structure and composition of communities (e.g. population size, distribution area), either due to the loss of species or to the introduction of new species. The consequences of biodiversity loss or changes in community composition for the functioning of ecosystems have been increasingly come into the focus of ecological research during the last decade.
Consequently, understanding the factors underlying the coexistence of many plant species at small spatial scale and processes of community assembly are a challenging issue in current ecological research. Plant community assembly is influenced by numerous interacting factors (Chesson 2000), including among others the diversity, quality and quantity of available resources (Petraitis et al. 1989; Chesson 2000; Kassen et al. 2000), trophic interactions such as the presence of herbivores and pathogens (Gallet et al. 2007; Meyer and Kassen 2007; Benmayor et al. 2008; Friman et al. 2008), disturbance (Petraitis et al. 1989; Roxburgh et al. 2004; Cadotte 2007) or phylogenetic history (Cavender-Bares et al. 2009). Different models predict how the distribution and abundances of species are determined as the neutral concept (Bell 2001; Hubbell 2001) and the classical concept of niche-based models (Hutchinson 1957; MacArthur and Levins 1967). The neutral theory of biodiversity and biogeography states that under the assumption that all species are equivalent to each other in all important ecological respects no single species has a competitive advantage or disadvantage. Therefore, species do not exclude each other (Bell 2000; Hubbell 2001, 2005), and stochasticity in species colonisation, extinction and speciation (MacArthur and Wilson 1963, 1967; Hubbell 2001; Volkov et al. 2003) explains community assembly and species coexistence. In contrast, the niche concept assumes that community dynamics are mainly evoked by differences in species’ reproductive success and mortality. Based on differences in resource acquisition and use, species thereby avoid competition and are able to coexist (Hardin 1960; Chesson 2000). However, a separate niche-based and neutral model may be insufficient to describe community dynamics (Leibold and McPeek 2006). Both niche and neutral processes play interactive roles. Niche-based processes may be of minor importance when average fitness differences among species are small (Pielou 1978), i.e. in communities close to neutrality. Coexisting species exhibit processes that reduce both fitness differences and the relative intensity of interspecific competition. The environmental conditions under which individual species in a plant community must acquire essential resources such as water, carbon dioxide, light and mineral nutrients depend on the characteristics of the surroundings and the interactions with neighbouring plants. Trade-offs in requirements for multiple resources enable numerous competitors to coexist and shape community structure (Bonsall et al. 2004; Tilman 2004; Gilbert et al. 2006). The greater the fitness differences between species, the stronger the stabilizing mechanisms need to be and vice versa (Chesson 2000). Stabilizing mechanisms themselves base on trade-offs of species functional characteristics (e.g. stronger competitors are weaker dispersers; Tilman 1994) or fluctuation-dependent mechanisms (e.g. the storage effect; Pacala and Tilman 1994) that require temporal or spatial variation in the environment (Chesson 1985). The evolved and evolving trade-offs of species life-history traits may set distinct constraints on community assembly. Thus, it is necessary to illuminate the role of particular functional traits and of trait variation within and between species for the assembly of plant communities and the functioning of ecosystems.
Knowledge about the mechanism controlling trait variation within coexisting plant communities is important. Experiments with manipulated biodiversity levels can be used to clarify the role of single species within communities (Dassler et al. 2008, Thein et al. 2008) and for ecosystem functioning (Schmid et al. 2002). Most biodiversity experiments have been conducted in grasslands and aimed to quantify biodiversity effects on plant primary productivity (Balvanera et al. 2006) as an ecosystem process. However, several studies have shown that the overall positive community response to increasing plant diversity is accompanied by mixed responses of individual species (e.g. Hooper & Vitousek 1997; Tilman et al. 1997; Hector et al. 1999; van Ruijven and Berendse 2003; Marquard et al. 2009) or different genotypes of single species (Vellend and Geber 2005; Fridley et al. 2007; Silvertown et al. 2009).
Analysing the role of individual species in ecological communities is an important prerequisite for a mechanistic understanding of community assembly and dynamics. Plant species are characterized through functional characteristics, which can modify plant fitness via their effects on growth, reproduction and survival (Violle et al. 2007). Plant functional traits are measurable morphological, physiological and phenological attributes at the individual level that directly or indirectly affect overall plant fitness (Lavorel et al. 1997; Violle et al. 2007). Plant traits have been used to establish functional classifications of organisms (Lavorel et al. 1997) or to quantify the functional diversity of communities (de Bello et al. 2009). However, these functional traits are variable between and within species (Albert et al. 2010), but so far the importance of trait variation within populations and species or between specie for the assembly of community and ecosystem processes is not well understood. Variation in species trait values have been recently investigated as responses of functional traits to gradients in plant diversity (Gubsch et al.2011, Roscher 2011) or trait trade-offs (Reich et al. 2003, Diaz et al. 2004, Wright et al. 2005). It is supposed that the increasing variety of traits in more diverse communities lead to more efficient and complete resource use than in less diverse and, hence, more similar communities (Tilman et al. 1997; Loreau 1998). According to the ―optimal allocation theory‖ (Bloom et al. 1985) plants tend to adjust their allocation and invest a higher proportion to organs that optimize the acquisition of the most limiting resource. A general assumption in plant biology is that intraspecific trait variation is significantly smaller than interspecific trait variation (Kraft et al. 2008). However, empirical studies have shown that functional traits can vary as much within as between species (Hodge 2004; Valladares and Niinemets 2008; Albert et al. 2010; Fajardo and Piper 2010).
When analyzing interspecific trait variation it has to be taken into account the expectation that closely related species are more likely to have similar responses to the biotic and abiotic environment (Gomez et al. 2010) and share a number of traits (e.g. symbiotic N2 fixation of legumes) than less closely related species. Therefore, it is promising to test species phylogenetic relatedness to predict which of them may coexist. This topic has only recently received increasing attention (Webb et al. 2002; Cadotte et al. 2008; Cavender-Bares et al. 2009), since molecular sequence data of numerous species become available and phylogenetic trees can be built and integrated in analyses. In natural communities the phylogenetic pattern in species composition is often a phylogenetically non-random sample of a wider species pool (Webb et al. 2002; Cavender-Bares et al. 2009; Vamosi et al. 2009). If congeneric species are overrepresented in communities, it may be assumed that they must share ecological traits that influence community assembly and that these traits evolve more slowly than the rate of appearance of new species. Recent studies of the phylogenetic distribution of ecological traits tended to emphasize the conservative nature of plant trait evolution and their potential role for community assembly (Webb 2000; Prinzing et al. 2001; Webb et al. 2002; Ackerly 2003, 2004). However, other studies have shown that traits that influence community structure as soil moisture tolerance are evolutionary labile (Cavender-Bares et al. 2004; Silvertown et al. 1999). Thus, differences in trait values are the result of both phylogenetic inertia and natural selection of the environment (Felsenstein 1985). Strong selection pressures and fast (co- )evolution are common in nature (Thompson 2005), placing evolutionary and ecological dynamics on similar timescales (Fussmann et al. 2007). Thus, functional trait values cannot be considered as fixed characteristics of species, and it is required to consider effects of trait evolution (local adaptation). The observed local variability would be due to the presence of several genotypes within populations. Genetic diversity can have a stabilizing effect (sensu Chesson 2000) on coexistence (Taylor and Aarssen 1990; Laird and Schamp 2006) of different species. Indeed, there exist a few empirical examples of large fine-scaled genetic diversity and its relationship to community-level processes (Turkington 1979; Aarssen and Turkington 1985; Vavrek 1998). For example, it has been shown that Daphnia species with different genotypes in the same population often display greater levels of niche differentiation than apparent among many species (Leibold and Tessier 1991; Tessier and Leibold 1997). Competitive interactions may be assumed to be a consequence and a potential cause of local genetic diversity (Vellend and Geber 2005) Therefore, local genetic and species diversity should be correlated (Vellend 2003).
While trait variation of plant species may have genetic base (Hodge 2004; Valladares and Niinemets 2008) it may also be founded on phenotypic plasticity, which are both integrated by measures of phenotypic variability (Byars et al. 2007). Phenotypic plasticity is the observed local variability of an individual and is dependent on the plasticity of given genotypes. It is well known that the ability of plant species to adapt their phenotype in response to the abiotic or biotic environment is important for optimized resource acquisition. The adaptive value of phenotypic plasticity for individual plant species is largely accepted (Sultan 1995, 2000; Schlichting & Pigliucci 1998). However, the role of phenotypic plasticity for the outcome of species interactions and its consequences for plant community assembly is not yet well understood (Callaway et al. 2003; Valladares et al. 2006). Many functional traits which are supposed to be important for the outcome of competition and associated processes of community assembly are known to be highly plastic. For instance, root length and root demography strongly respond to supply levels of nutrients (Hodge 2004), and leaf architecture and leaf number are known to be highly dependent on light availability (Pigliucci et al. 2003; Valladares and Niinemets 2008). Trait values adapted to a local environment determine a species ecological strategy (McGill et al. 2006; Westoby and Wright 2006). Environmental filters will locally limit the range of ecological strategies and may result in trait convergence of species within a community (McArthur and Levins 1967; Grime 2006; Funk et al.2008). However, phenotypic plasticity allows organisms to adjust to a large range of conditions without evolutionary change (Grassein et al. 2010). As a consequence, trait convergence within a habitat is not solely due to genetic similarities between species but may often be explained as a significant part by plastic responses, i.e. phenotypic similarity despite genetic divergence. Trait plasticity may allow species to shift their ecological strategy to fit current environmental conditions and enable them to pass the ecological filter. Likewise, trait divergence among communities is often thought to be a consequence of community assembly rules. However, it may equally well be due to phenotypic plasticity induced by divergent environmental conditions.
For a long time it was assumed that life history traits of interacting species are uniform within species and remain unchanged over time (Agrawal et al. 2007). It was suspected that the relatively slow time scale of evolutionary changes renders an evolutionary perspective of community ecology unnecessary. However, it is unclear how much of observed variation in plant community composition is explainable by phenotypic plasticity of traits across a wide range of environments, by the phylogenetic relatedness of traits of single species within a plant community or the influence of genotypes within single species on plant community composition and functioning.

Thesis outline
The central topics of this thesis are the mechanism underlying variation in the performance of single plant species in experimental grasslands of different diversity. The thesis is based on data recorded in the Jena Experiment, a large-scale biodiversity experiment in Germany, which was designed to clarify the role of plant diversity for ecosystem functioning, element cycling and trophic interactions (Roscher et al. 2004).
In chapter 1, I have surveyed the role of plant diversity (species number, legume presence) on the variation of functional traits of 27 non-legume forb species and analysed their relationships to species phyloge10netic history and growth forms. In chapter 2, I examined whether variation in plant individual performance in response to neighborhood diversity is due to phenotypic plasticity or to genotypic variation within single plant species. I established the offspring of seed families of five forb species collected in monocultures or in 60-species mixture after five years of selection in the Jena Experiment. Then, I transplanted or replanted the offspring to the plot of their own origin and into the respective monoculture or 60-species mixture to assess whether five yerars of selection in plant communities of different diversity led to a genetic differentiation or whether trait variation is exclusively due to phenotypic plasticity of the investigated forb species.
In chapter 3, I explored whether plants of T. officinale originating from sites with presumably different selection regimes, either a density-independent mortality by weeding (r-selection regime) or density- dependent mortality by increasing interspecific competition along a species richness gradient (K-selection regime) over 5 years have developed traits expected under r- or K-selection in a common environment.