Freeze tolerance of poleward‐spreading mangrove species weakened by soil properties of resident salt marsh competitor

• Published in: The Journal of ecology Vol. 108; no. 4; pp. 1725 - 1737
• Main Authors: Chen, Enjian, Blaze, Julie A., Smith, Rachel S., Peng, Shaolin, Byers, James E., Randall Hughes, A.
• Format: Journal Article
• Language: English
• Published: Oxford Blackwell Publishing Ltd 01-07-2020
• Subjects: allelopathy; Aquatic plants; Avicennia germinans; biotic resistance; Climate change; Colonization; dark septate endophyte fungi; Endophytes; Fitness; Freezing; Fungi; global change ecology; Global warming; invasion ecology; Laboratories; Mangrove swamps; Mangroves; Plant species; plant–soil (below‐ground) interactions; plant–soil feedbacks; Range extension; Ratios; Rhizosphere; Roots; Salt marshes; Saltmarshes; Seedlings; Soil environment; Soil properties; Soil treatment; Soils; Spartina alterniflora; Species; Spores; Survival
• ISSN: 0022-0477; 1365-2745
• DOI: 10.1111/1365-2745.13350

Increasing temperatures associated with climate change are shifting plant species to higher latitudes. Soil communities could aid the plants’ shift into novel areas by harbouring fewer soil‐borne antagonists or more mutualists that influence the fitness and stress tolerance of the shifting species. Alternatively, they could contain novel antagonists or fewer mutualists. Thus, soil communities could positively or negatively affect plant range expansion, particularly if they influence plants’ responses to climate, such as freeze tolerance, that feedback to affect expansion.
We used the northward range expansion of the black mangrove, Avicennia germinans, into a system dominated by marsh cordgrass, Spartina alterniflora, in northern Florida, USA to study how the novel soil environment (i.e. S. alterniflora soil) affects mangrove fitness, susceptibility to cold stress and the colonization of mutualist fungi. We quantified abundance of root mutualistic fungi in mixed marsh‐mangrove habitat and conducted a laboratory experiment to test effects of steam‐sterilized and live soils from A. germinans and S. alterniflora on the growth, condition, fungal colonization and freeze tolerance of A. germinans seedlings.
In the field, we found two times higher dark septate endophyte (DSE) colonization of A. germinans roots and three times higher fungal spore density in A. germinans soil compared to S. alterniflora roots and soil. In the laboratory experiment, seedlings in steamed S. alterniflora soil treatments had 50%–65% survival after freezing, compared to 0% survival in treatments with live S. alterniflora soil. A. germinans live soil mixed with S. alterniflora steamed soil yielded A. germinans roots with the highest DSE colonization and seedlings with greater shoot biomass and lower root:shoot ratios. S. alterniflora live soil lowered the freeze tolerance of A. germinans, decreased mangrove survival and depressed DSE colonization.
Synthesis. S. alterniflora soil could impede A. germinans establishment in salt marsh communities. As climate warming gradually allows A. germinans to displace S. alterniflora, the rhizosphere could become increasingly hospitable to A. germinans. Our work suggests the soil community associated with resident species mediates climatic stressors to affect expansion success.
Soil communities could positively or negatively affect plant range expansion, particularly if they influence plants’ responses to climate, such as freeze tolerance, that feedback to affect expansion. We found that Avicennia germinans seedlings in steam‐sterilized Spartina alterniflora soil treatments had 50%–65% survival after freezing, compared to 0% survival in treatments with live S. alterniflora soil. As climate warming gradually allows A. germinans to displace S. alterniflora, the rhizosphere could become increasingly hospitable to A. germinans.