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

1. Background: 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. 2. Methods: 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. 3. Results and Conclusions: 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. 4. 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.