Fine roots are crucial to ecosystem processes, consuming up to 40% of all carbon fixed by photosynthesis in terrestrial ecosystems and supplying most of the nutrients and water to above-ground tissues (Litton, Raich & Ryan 2007). Although below-ground niche partitioning is regarded as a fundamental factor explaining plant species coexistence (Hutchings, John & Wiljesinghe 2003; Silvertown 2004), few in situ ecological studies have evaluated the role of below-ground components structuring plant communities (Casper, Schenk & Jackson 2003) and only a handful of recent studies have resolved species-specific root patterns in mixed forest communities (Comas & Eissenstat 2009; Espeleta, West & Donovan 2009; Meinen, Hertel & Leuschner 2009; Holdaway et al. 2011). As a consequence, fine root trait variation among and within species in natural conditions is still largely unknown, hindering the scaling of root traits from individual plants and species to the community level. This lack of understanding about below-ground community dynamics also precludes inferences about the role of fine root traits in plant community assembly (Westoby & Wright 2006).
A central goal in plant ecology is to understand the factors associated with morphological trait variation in plant populations and communities (Mooney & Dunn 1970; Grime 2006). Variation in traits among species is often larger than trait variation within species, resulting in phylogenetically determined, canalized trait differences. At the population level within species, traits can be affected by intraspecific genetic variation, but an individual may also vary its phenotype to cope with environmental heterogeneity (i.e. plasticity sensu Valladeres, Gianoli & Gómez 2007). The magnitude of both interspecific and intraspecific trait variation in natural communities has been rarely quantified (Lake & Ostling 2009). At the community level, community-aggregated traits (i.e. trait values averaged across individuals or species in a community, weighted by abundance; Shipley 2010) reflect major environmental constraints on plant traits. They are also important starting points for predicting how the accumulation of alternative trait sets from competing species can maximize community-wide efficiency in the uptake of limiting resources (Westoby & Wright 2006). Deterministic (niche) models predict that plant community assembly is the result of interaction between environmental filtering effects and interspecific competition, with both forces defining the realized niche of the species (Weiher, Clarke & Keddy 1998; Cornwell & Ackerly 2009). Neutral theory assumes ecological equivalence among individuals and a stochastic partitioning of resources, implying that traits could have a random distribution with respect to both the environment and community composition (Hubbell 2001). However, even under neutral dynamics, if species differ in their traits, community composition can determine community-aggregated trait values.
Previous research, focused mostly on leaf and stem traits, has found that deterministic (i.e. competitive and filtering mechanisms) rather than stochastic processes are involved in the landscape-scale distribution of community traits (Ackerly & Cornwell 2007; Kraft, Valencia & Ackerly 2008). Abiotic factors, such as moisture availability, were correlated with above-ground community-aggregated trait shifts along environmental gradients, and this change was correlated with species turnover (Cornwell & Ackerly 2009). These results suggest that filtering effects are more important than competitive interactions or intraspecific trait plasticity. The distribution of below-ground plant traits with respect to environmental gradients remains mostly uninvestigated (Schenk 2006). Although there are clearly canalized differences between plant lineages in root traits (Baylis 1975; Brundrett 2002), roots are also highly plastic and interactive organs, capable of responding physiologically and morphologically to both biotic and abiotic factors (Hodge 2004; Wijesinghe, John & Hutchings 2005). In fact, they often express traits, particularly among woody plants, not necessarily correlated with leaf trait syndromes (Comas & Eissenstat 2004; Withington et al. 2006; McCormack et al. 2012), which has limited our understanding of the factors affecting root trait trade-offs.
Relatively few hypotheses have been formally proposed to link root traits and soil properties at the community level. Several previous studies have examined species-specific root traits within natural communities (Comas & Eissenstat 2004, 2009; Espeleta, West & Donovan 2009; Alvarez-Uria & Körner 2011; Holdaway et al. 2011). However, the ability to test for environmental filtering versus competitive interactions has been hampered by focusing on only a few species or lack of information about soil properties or neighbour species where roots were found. A few studies have shown alternative root morphological patterns between communities established in contrasting environmental conditions (Taub & Goldberg 1996; Holdaway et al. 2011), indicating strong filtering effects shaping the distribution of community-aggregated root traits at large scales. Nevertheless, community responses to environmental gradients may be mediated by population-level root trait plasticity. Trees can modify root morphology as a response to nutrient availability and moisture gradients (Coleman 2007; Richter et al. 2007; Kazda & Schmid 2009). Finally, the existence of highly contrasting root traits among co-occurring species has also been demonstrated (Roumet, Urcelay & Diaz 2006; Comas & Einssestat 2009; Meinen, Hertel & Leuschner 2009), suggesting some degree of niche segregation within communities.
In addition to environmental effects, the distribution of below-ground traits could also be influenced by the outcome of interactions among species. Although the ability of roots to react to interspecific competition has been recorded under controlled conditions (Cahill & Casper 2000; Gersani 2001; Bartelheimer, Steinlein & Beyschlag 2006), the importance of this interaction has not been quantified under natural conditions. It has been predicted that competitive displacement would limit similarity among coexisting species, producing a nonrandom, even spacing of traits among species in direct competition (Stubbs & Wilson 2004). This pattern could be generated through competitive exclusion from a site, or trait plasticity in response to competition (Cornwell & Ackerly 2009). Thus, it is still not clear whether soil properties limit the range of morphological variation among plants that co-occur in the same habitat or whether competitive interactions lead coexisting species to exploit distinct niches, enhancing morphological differentiation between them (Fitter 1991).
To distinguish between these scenarios, we had three primary objectives.
- Examine intraspecific root trait variation in multiple tree species under a range of natural conditions and determine whether the observed variation was related to soil properties and/or the identity of root neighbours.
- Determine whether, at a given location, the distribution of root traits among species is most often consistent with environmental filtering, competitive displacement or neutral assembly. If environmental filtering due to soil properties is the main driver in root trait assembly, we would expect species to show alternative root morphologies associated with distinct ranges of soil properties. A potential correlation between root traits and soil properties could arise through either species turnover or intraspecific root plasticity in response to soil properties. Under neutral assembly, species distributions would be unrelated to soil properties, and root traits could only be correlated with soil properties through plasticity.
- Finally, we wanted to quantify the response of community-aggregated traits to soil properties and species composition. This response was then interpreted in the context of results from our other objectives regarding community assembly and intraspecific plasticity.