Alternative plant designs: consequences for community assembly and ecosystem functioning

Abstract

Background: Alternative organism designs (i.e. the existence of distinct combinations of traits leading to the same function or performance) are a widespread phenomenon in nature and are considered an important mechanism driving the evolution and maintenance of species trait diversity. However, alternative designs are rarely considered when investigating assembly rules and species effects on ecosystem functioning, assuming that single trait trade-offs linearly affect species fitness and niche differentiation.

Scope: Here, we first review the concept of alternative designs, and the empirical evidence in plants indicating the importance of the complex effects of multiple traits on fitness. We then discuss how the potential decoupling of single traits from performance and function of species can compromise our ability to detect the mechanisms responsible for species coexistence and the effects of species on ecosystems. Placing traits in the continuum of organism integration level (i.e. traits hierarchically structured ranging from organ-level traits to whole-organism traits) can help in choosing traits more directly related to performance and function.

Conclusions: We conclude that alternative designs have important implications for the resulting trait patterning expected from different assembly processes. For instance, when only single trade-offs are considered, environmental filtering is expected to result in decreased functional diversity. Alternatively, it may result in increased functional diversity as an outcome of alternative strategies providing different solutions to local conditions and thus supporting coexistence. Additionally, alternative designs can result in higher stability of ecosystem functioning as species filtering due to environmental changes would not result in directional changes in (effect) trait values. Assessing the combined effects of multiple plant traits and their implications for plant functioning and functions will improve our mechanistic inferences about the functional significance of community trait patterning.

Keywords: Biodiversity–ecosystem functioning; ecological filters; ecophysiology; functional diversity; functional ecology; many-to-one mapping; species coexistence.

Fig. 1.

Conceptual model modified from Arnold (1983) to include the concept of the organism integration level (Marks, 2007), ranging from organ-level traits (traits 1–6) to whole-organism traits (traits 7 and 8). Whole-organism traits result from different arrays of organ-level traits, including their multiple trade-offs (double-headed curved arrows). Solid arrows represent the causal relationships between phenotypical traits and performance and their consequences for fitness (evolutionary processes) and community assembly (ecological processes). The relationship between organ-level traits and performance (and consequently fitness and community assembly) is considered indirect (dashed line), as whole-organism traits more properly represent the integrated functioning of the organism. Therefore, filters should act directly on whole-organism traits and only indirectly on organ-level traits. Additionally, the community assembly process (and the resulting trait composition) can strongly influence ecosystem functioning as illustrated by the response and effect framework proposed by Suding et al. (2008).

Fig. 2.

Adaptive landscapes showing fitness values (colour scale) in the space defined by two traits. The figure displays both simple and complex relationships between traits and fitness. Straightforward relationship between trait(s) and fitness are displayed when one single trait (A) or one single combination of trait values (ecological strategy) determines fitness (B). Complex relationships between traits and fitness are displayed when different combinations of trait values show similar fitness (i.e. alternative designs). This happens when traits are substitutable in conferring a function or response to environmental factors (C) or when different ecological strategies provide similar fitness or function (D).

Fig. 3.

Adaptive landscape showing the phytosociological importance value (IV) as a performance proxy. Dominant species converge in minimum plant water potential (Ψ _min, MPa, whole-plant trait), but strongly diverge in specific leaf area (SLA, cm² g^–1, single-organ trait). The adaptive landscape is based on trait measurements of ten woody species in the Brazilian sandy coastal plains (Rosado and de Mattos, 2010, 2018).

Fig. 4,

Phytosociological importance value (IV) for four woody species in the Brazilian sandy coastal plains. Dominant species are represented by circles, and subordinate species are represented by squares. The dominance rank is explained by the minimum plant water potential (Ψ _min, MPa), which is a whole-organism trait reflecting the integrated functioning of the plant. This integrative trait, in turn, is determined by distinct arrays of organ-level traits. For instance, dominant species show contrasting values of specific leaf area (SLA, cm² g^–1). This leaf trait is highly correlated with litter decomposition rate (k, year^–1), which can be taken as a measure of the species impact on the ecosystem [data from Rosado and de Mattos (2010, 2018) and C. Dias (unpublished)].