Experience of inundation or drought alters the responses of plants to subsequent water conditions

Shu Wang; Ragan M. Callaway; Dao-Wei Zhou; Jacob Weiner

doi:10.1111/1365-2745.12649

Experience of inundation or drought alters the responses of plants to subsequent water conditions

Shu Wang, Ragan M. Callaway, Dao-Wei Zhou, Jacob Weiner

Section for Organismal Biology

21 Citations (Scopus)

Abstract

The availability of water is often highly variable over the life of a plant in nature, and most plants experience episodic extremes in water scarcity and abundance. The importance of plant plasticity in coping with such experiences is widely recognized, but little is known about how plastic responses to current conditions are affected by prior environmental experiences. * Our objectives were to investigate the effects of early inundation or drought on the subsequent responses of plant species to the same, opposite or more favourable conditions. * To address these questions, we subjected four invasive and four native herbaceous perennial species from different habitats (xeric, mesic, hydric) to two rounds of hydrological treatments (drought, moderate water, inundation) and analysed the effects of the early treatments on survival and performance (total biomass and relative growth) of individuals in the later treatments. * In general, (i) early drought reduced the performance of more species than did early inundation, and decreased the final total mass of all species; (ii) early inundation and early drought did not lead to lower survival immediately or later, but improved the relative growth of survivors across all late conditions; (iii) late drought resulted in the highest mortality and lowest performance after any early treatment. * With respect to habitat of origin: (i) early inundation was more beneficial for species from wet habitats than for other species; (ii) species from xeric habitats had the strongest drought tolerance after early drought; (iii) mesic species were more likely to suffer reduced later growth after either inundation or drought experience. Invasive species benefitted more from early inundation than did native species, but native species grew better after experiencing early drought. * Results indicate that early exposure to inundation or drought conditions alters how plants respond to later conditions and suggest that exposure to extreme events can induce physiological or morphological changes that improve tolerance for either extreme conditions later. This increased tolerance can be at the cost of poorer performance under more benign conditions. * Synthesis. Early inundation or drought experience may be harmful immediately, but can be beneficial for the later growth of plants. The ability of species to utilize early hydrological experiences was associated with the water range of their habitats and whether the species is invasive or native. The ability to modulate future plastic responses may be as important as short-term plasticity in adapting to temporal environmental heterogeneity. Such ‘metaplasticity’ can optimize current performance, while avoiding the potential costs of maintaining a high degree of plasticity throughout life.

Original language	English
Journal	Journal of Ecology
Volume	105
Issue number	1
Pages (from-to)	176-187
Number of pages	12
ISSN	0022-0477
DOIs	https://doi.org/10.1111/1365-2745.12649
Publication status	Published - 1 Jan 2017

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@article{73fad58837b94094aaf9f21b9895469e,

title = "Experience of inundation or drought alters the responses of plants to subsequent water conditions",

abstract = "The availability of water is often highly variable over the life of a plant in nature, and most plants experience episodic extremes in water scarcity and abundance. The importance of plant plasticity in coping with such experiences is widely recognized, but little is known about how plastic responses to current conditions are affected by prior environmental experiences. * Our objectives were to investigate the effects of early inundation or drought on the subsequent responses of plant species to the same, opposite or more favourable conditions. * To address these questions, we subjected four invasive and four native herbaceous perennial species from different habitats (xeric, mesic, hydric) to two rounds of hydrological treatments (drought, moderate water, inundation) and analysed the effects of the early treatments on survival and performance (total biomass and relative growth) of individuals in the later treatments. * In general, (i) early drought reduced the performance of more species than did early inundation, and decreased the final total mass of all species; (ii) early inundation and early drought did not lead to lower survival immediately or later, but improved the relative growth of survivors across all late conditions; (iii) late drought resulted in the highest mortality and lowest performance after any early treatment. * With respect to habitat of origin: (i) early inundation was more beneficial for species from wet habitats than for other species; (ii) species from xeric habitats had the strongest drought tolerance after early drought; (iii) mesic species were more likely to suffer reduced later growth after either inundation or drought experience. Invasive species benefitted more from early inundation than did native species, but native species grew better after experiencing early drought. * Results indicate that early exposure to inundation or drought conditions alters how plants respond to later conditions and suggest that exposure to extreme events can induce physiological or morphological changes that improve tolerance for either extreme conditions later. This increased tolerance can be at the cost of poorer performance under more benign conditions. * Synthesis. Early inundation or drought experience may be harmful immediately, but can be beneficial for the later growth of plants. The ability of species to utilize early hydrological experiences was associated with the water range of their habitats and whether the species is invasive or native. The ability to modulate future plastic responses may be as important as short-term plasticity in adapting to temporal environmental heterogeneity. Such {\textquoteleft}metaplasticity{\textquoteright} can optimize current performance, while avoiding the potential costs of maintaining a high degree of plasticity throughout life.",

keywords = "drought, habitat range, inundation, invasiveness, metaplasticity, plasticity, priming effect, stress memory, stress tolerance, temporal heterogeneity",

author = "Shu Wang and Callaway, {Ragan M.} and Dao-Wei Zhou and Jacob Weiner",

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T1 - Experience of inundation or drought alters the responses of plants to subsequent water conditions

AU - Wang, Shu

AU - Callaway, Ragan M.

AU - Zhou, Dao-Wei

AU - Weiner, Jacob

PY - 2017/1/1

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N2 - The availability of water is often highly variable over the life of a plant in nature, and most plants experience episodic extremes in water scarcity and abundance. The importance of plant plasticity in coping with such experiences is widely recognized, but little is known about how plastic responses to current conditions are affected by prior environmental experiences. * Our objectives were to investigate the effects of early inundation or drought on the subsequent responses of plant species to the same, opposite or more favourable conditions. * To address these questions, we subjected four invasive and four native herbaceous perennial species from different habitats (xeric, mesic, hydric) to two rounds of hydrological treatments (drought, moderate water, inundation) and analysed the effects of the early treatments on survival and performance (total biomass and relative growth) of individuals in the later treatments. * In general, (i) early drought reduced the performance of more species than did early inundation, and decreased the final total mass of all species; (ii) early inundation and early drought did not lead to lower survival immediately or later, but improved the relative growth of survivors across all late conditions; (iii) late drought resulted in the highest mortality and lowest performance after any early treatment. * With respect to habitat of origin: (i) early inundation was more beneficial for species from wet habitats than for other species; (ii) species from xeric habitats had the strongest drought tolerance after early drought; (iii) mesic species were more likely to suffer reduced later growth after either inundation or drought experience. Invasive species benefitted more from early inundation than did native species, but native species grew better after experiencing early drought. * Results indicate that early exposure to inundation or drought conditions alters how plants respond to later conditions and suggest that exposure to extreme events can induce physiological or morphological changes that improve tolerance for either extreme conditions later. This increased tolerance can be at the cost of poorer performance under more benign conditions. * Synthesis. Early inundation or drought experience may be harmful immediately, but can be beneficial for the later growth of plants. The ability of species to utilize early hydrological experiences was associated with the water range of their habitats and whether the species is invasive or native. The ability to modulate future plastic responses may be as important as short-term plasticity in adapting to temporal environmental heterogeneity. Such ‘metaplasticity’ can optimize current performance, while avoiding the potential costs of maintaining a high degree of plasticity throughout life.

AB - The availability of water is often highly variable over the life of a plant in nature, and most plants experience episodic extremes in water scarcity and abundance. The importance of plant plasticity in coping with such experiences is widely recognized, but little is known about how plastic responses to current conditions are affected by prior environmental experiences. * Our objectives were to investigate the effects of early inundation or drought on the subsequent responses of plant species to the same, opposite or more favourable conditions. * To address these questions, we subjected four invasive and four native herbaceous perennial species from different habitats (xeric, mesic, hydric) to two rounds of hydrological treatments (drought, moderate water, inundation) and analysed the effects of the early treatments on survival and performance (total biomass and relative growth) of individuals in the later treatments. * In general, (i) early drought reduced the performance of more species than did early inundation, and decreased the final total mass of all species; (ii) early inundation and early drought did not lead to lower survival immediately or later, but improved the relative growth of survivors across all late conditions; (iii) late drought resulted in the highest mortality and lowest performance after any early treatment. * With respect to habitat of origin: (i) early inundation was more beneficial for species from wet habitats than for other species; (ii) species from xeric habitats had the strongest drought tolerance after early drought; (iii) mesic species were more likely to suffer reduced later growth after either inundation or drought experience. Invasive species benefitted more from early inundation than did native species, but native species grew better after experiencing early drought. * Results indicate that early exposure to inundation or drought conditions alters how plants respond to later conditions and suggest that exposure to extreme events can induce physiological or morphological changes that improve tolerance for either extreme conditions later. This increased tolerance can be at the cost of poorer performance under more benign conditions. * Synthesis. Early inundation or drought experience may be harmful immediately, but can be beneficial for the later growth of plants. The ability of species to utilize early hydrological experiences was associated with the water range of their habitats and whether the species is invasive or native. The ability to modulate future plastic responses may be as important as short-term plasticity in adapting to temporal environmental heterogeneity. Such ‘metaplasticity’ can optimize current performance, while avoiding the potential costs of maintaining a high degree of plasticity throughout life.

KW - drought, habitat range, inundation, invasiveness, metaplasticity, plasticity, priming effect, stress memory, stress tolerance, temporal heterogeneity

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DO - 10.1111/1365-2745.12649

M3 - Journal article

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