Interactive effects of salinity and inundation on native Spartina foliosa, invasive S. densiflora, and their hybrid from San Francisco Estuary, California

Authors: GALLEGO-TEVAR, BLANCA - University Of Seville; Grewell, Brenda; Futrell, Caryn; DRENOVSKY, REBECCA - John Carroll University; CASTILLO, JESUS - University Of Seville

Submitted to: Annals of Botany
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 10/15/2019
Publication Date: 10/22/2019
Citation: Gallego-Tevar, B., Grewell, B.J., Futrell, C.J., Drenovsky, R.E., Castillo, J.M. 2019. Interactive effects of salinity and inundation on native Spartina foliosa, invasive S. densiflora, and their hybrid from San Francisco Estuary, California. Annals Of Botany. 125(2):377-389. https://doi.org/10.1093/aob/mcz170.
DOI: https://doi.org/10.1093/aob/mcz170

Interpretive Summary: Tidal marsh plant communities occur along inundation and salinity gradients in coastal estuaries. These species provide significant ecosystem functions and services including flood protection, shoreline erosion control, sediment retention, nutrient cycling, fish and wildlife habitat, and food web support. Sea level rise (SLR) associated with climate change is increasing permanent submersion and aqueous salinity levels in intertidal wetlands. Invasion of these wetlands by non-native plant species and their continued spread are also recognized outcomes of global environmental change. Understanding the responses of native and invasive tidal wetland plant species and their hybrids to interacting physiological stresses imposed by SLR is key to native species conservation in tidally flooded ecosystems. In a mesocosm experiment, we evaluated the interactive stress effects of three inundation depths (4.5, 35.5 and 55 cm) and four aqueous salinity levels (0.5, 10, 20 and 40 ppt) on 27 functional trait responses of native Spartina foliosa (Pacific cordgrass), invasive S. densiflora (Dense-flowered cordgrass) and their hybrid S. densiflora x S. foliosa from San Francisco Estuary. We found that the combined effect of salinity and inundation led to synergetic effects in biochemical changes in leaves of the plants that influence their stress tolerance. The native S. foliosa increased exudation of sodium from its leaves, and allocated more resources to increased production of glycinebetaine concentration in leaves to maintain osmotic balance as a stress tolerance response. With increasing inundation, S. foliosa also increased production of roots. However, the fitness costs due to the interacting stresses included reduced growth, overall biomass production, and sexual reproduction. S. foliosa was less sensitive to salinity than invasive S. densiflora and the hybrid, though both the native and invasive parental species were highly growth-limited in response to increased inundation and salinity. S. densiflora was fast-growing in low stress conditions and tolerated moderate interactive stresses. It produced high biomass with high allocation to reproductive tissues in shallow freshwater. With increasing stress factors, it increased leaf rolling as a morphological response to reduce uptake of saline water, and produced a higher concentration of proline in leaves. Overall the photosynthetic rate of invasive S. densiflora was reduced with increases in the interacting stresses. The invasive hybrid taxa produced more biomass, rhizome reserves and tillers than either of its parental species, achieving high fitness even under the most stressful conditions. Genetic recombination in hybrid plants can generate genotypes that express phenotypes outside the normal range of variation in traits observation in the gene pools of either parent species. These transgressive phenotypes can hae higher fitness in novel or changing environments than their parents. Our results demonstrate that transgressivity and phenotypic plasticity of the S. densiflora x S. foliosa hybrid improved its capacity to deal with flooding stress more so than its response to increasing salinity. Results of our experiment provide evidence that populations of native S. foliosa and invasive S. densiflora will experience reduced fitness in responses to physiological stresses imposed by SLR, whereas their hybrid is more tolerant of stresses imposed by this environmental change. As a result, hybrid invasiveness may be sustained and management should be directed towards control of S. densiflora to prevent of new opportunities for hybrid formation.

Technical Abstract: Background and Aim: Sea Level Rise (SLR) associated with climate change is intensifying permanent submersion and salinity in salt marshes. Understanding the responses of native and invasive halophytes and their hybrids to interacting physiological stresses imposed by SLR is key to native species conservation. Methods: In a mesocosm experiment, we evaluated interactive stress effects of three inundation depths (4.5, 35.5 and 55 cm) and four aqueous salinities (0.5, 10, 20 and 40 ppt) on 27 functional traits of native Spartina foliosa, invasive S. densiflora and their hybrid S. densiflora x S. foliosa from San Francisco Estuary. Key Results: The combined effect of salinity and inundation led to synergetic effects in leaf biochemical stress indicators. S. foliosa behaved as a stress-tolerant species, with high leaf Na exudation rate and glycinebetaine concentrations increasing with stress. S. foliosa had low allocation to sexual reproduction and biomass production, and increased root biomass with inundation. S. foliosa was less sensitive to salinity than S. densiflora and the hybrid but was highly growth-limited in response to increased inundation and salinity. S. densiflora was fast-growing in low stress conditions and tolerated moderate interactive stresses. It produced high biomass with high allocation to reproductive tissues in shallow freshwater. With increasing stress it increased leaf rolling and proline accumulation and reduced photosynthesis. The hybrid produced more biomass, rhizome reserves and tillers than its parents, achieving high fitness even under the most stressful conditions. Transgressivity and phenotypic plasticity improved its capacity to deal with flooding stress more so than its response to increasing salinity. Conclusions: Populations of S. foliosa and S. densiflora will experience reduced fitness, whereas their hybrid is more tolerant of stresses imposed by SLR. As a result, hybrid invasiveness may be sustained and management should be directed towards prevention of new hybrid formation.