Common garden experiments reveal acquisitive strategies for responding to drought in seedlings of forest tree species: a commentary on ‘Clinal variations in seedling traits and responses to water availability correspond to seed-source environmental gradients in a foundational dryland tree species’

Abstract

This article comments on:

Georgia L. Vasey, Alexandra K. Urza, Jeanne C. Chambers, Elizabeth G. Pringle and Peter J. Weisberg. Clinal variations in seedling traits and responses to water availability correspond to seed-source environmental gradients in a foundational dryland tree species, Annals of Botany, Volume 132, Issue 2, 25 July 2023, Pages 203–216, https://doi.org/10.1093/aob/mcad041

The extent to which plants are genetically adapted to their environment, and their capacity to respond to environmental changes via phenotypic plasticity, are key questions in evolutionary ecology, especially in the context of ongoing climate change. Specifically, identifying crucial environmental factors that are potential drivers of these adaptations is indispensable to predict future plant responses. In this issue of Annals of Botany, Vasey et al. (2023) implement a common garden experiment to assess growth and allometric traits of 23 populations of the conifer Pinus monophylla distributed along a wide climatic gradient of water availability and precipitation seasonality. Importantly, they carefully analyse both above- and below-ground traits and their response to four water availability treatments in seedlings. In general, early life stages are subjected to high selective pressures, making this the most critical period for species persistence. In species of arid ecosystems, it is not uncommon to find seedling mortalities of >90 % associated with water scarcity (Vizcaíno-Palomar et al., 2014). Thus, deciphering the adaptive strategies for responding to drought at this vulnerable life stage is essential for predicting species responses to climate change, as, for forest tree species, the regeneration niche is narrower than the adult niche.

At the interspecific level, a trade-off between growth potential and resistance to abiotic stresses has been described such that species that have evolved in harsher environments are expected to exhibit lower growth rates coupled with higher stress resistance (Reich, 2014). However, to what extent intraspecific patterns mirror those observed at higher taxonomic scales is still an unresolved question (Cochrane et al., 2015). The rigorous methodological approach carried out by Vasey et al. (2023) reveals that, contrary to the pattern at the interspecific level, seedlings from arid populations grew more both above and below ground than those from populations in environments with higher water availability.

The evolution of an acquisitive strategy under dry conditions has also been reported in other tree species at early life stages (Ramírez-Valiente et al., 2021, 2022). Higher growth rates might favour the construction of deeper roots that allow seedlings to reach wetter soil layers and maintain a higher water potential under dry conditions (Matías et al., 2014). In contrast, at later life stages, the negative effects of higher growth rates and plant size might counteract their potential benefits. Specifically, larger height increases resistance to water transport and larger growth rates are usually associated with larger vessel sizes which could increase the risk of hydraulic failure (Menezes-Silva et al., 2019). Overall, this would result in a change in resource-use strategies along ontogeny, due to a shift in the carbon and water balance across developmental stages and plant size (Fig. 1). Results reported in several species are consistent with these ideas. For example, in Pinus pinaster, studies on seedlings have shown that populations from dry areas exhibit increased growth and survival, whereas the pattern seems to be the opposite in juvenile and adult trees, for which populations from mesic areas exhibit the largest growth rates (Ramírez-Valiente et al., 2022). In contrast, in some Mediterranean species, a conservative resource-use strategy with more sclerophyllous drought-tolerant leaves, coupled with increased relative investment in below-ground growth, has been reported not only in adults but also in seedlings from dry provenances as a mechanism to maintain physiological homeostasis during dry periods (e.g. Solé-Medina et al., 2022). These two potential alternatives, an acquisitive-escape strategy of faster growth versus a conservative strategy with increased drought tolerance, as well as the role of ontogeny in drought responses, may be influenced by phylogeny, biome and life form, but further research is needed to determine the drivers of these contrasting strategies.

Fig. 1.

Hypotheses regarding the effect of ontogeny on resource-use strategies under two potential scenarios. Scenario 1 is shown in (A) and (B) based on results in Ramírez-Valiente et al. (2022) and Vasey et al. (2023), where seedlings from drier and warmer areas exhibited higher growth potential and survival rates under dry conditions. In this scenario, species seem to change from an acquisitive resource-use strategy at the seedling stage to a more conservative strategy at later life stages with populations with lower growth and increased drought tolerance having higher survival probabilities. Scenario 2 is shown in (C) and (D) based on results from some Mediterranean oak species, where seedlings and adult trees maintain a conservative resource-use strategy across all life stages (Solé-Medina et al., 2022). Note that the hypothetical scenarios could represent different species or the same species in different biomes, highlighting the need for species- and biome-specific empirical results precluding generalizations based on specific life stages.

Another remarkable effort performed by Vasey et al. (2023) is in assessing differences in phenotypic plasticity among populations, an under-explored and overlooked process in many studies on adaptation and responses to climate change. Population-specific responses to environmental factors are common in forest tree species (Matesanz & Ramírez-Valiente, 2019), allowing them to cope with a range of environmental conditions. In this issue, Vasey et al. (2023) highlight the importance of the seasonal distribution of water availability as a selective factor for phenotypic plasticity. The importance of the role of timing of soil water availability, and not simply the annual climatic mean, is becoming more frequently acknowledged, and the results of this article support this notion. Importantly, Vasey et al. (2023) detected an association between drought responses and phenotypic plasticity, with populations from more arid areas having an acquisitive strategy and higher phenotypic plasticity. This result is consistent with previous studies and suggests that phenotypic plasticity of traits should be considered when studying resource-use strategies along aridity gradients (Solé-Medina et al., 2022).

In summary, the growing body of research conducted at the intraspecific level provides mounting evidence for the existence of extensive within-species genetic variation affecting environmental stress responses. Intraspecific patterns might be species- and biome-specific, since different environmental conditions might exert contrasting selective pressures, even as different species inhabiting the same biome might cope with environmental stress by alternative functional strategies. Consequently, predicting populations’ responses requires empirical data under common garden experiments to separate genetic and plastic responses. Thus, research covering under-studied species, especially pioneer or key species for ecosystem functioning such as the conifer Pinus monophylla, is essential if we are to ensure species persistence.