Enhanced susceptibility to oiling may limit denitrification recovery in marshes subjected to woody encroachment

Coastal salt marshes provide valuable ecosystem services but are subjected to multiple concomitant stressors that may impact their ability to provide those services. Global climate change has led to the poleward expansion of mangroves into salt marshes on each continent where mangroves and marshes co-occur. In the northern Gulf of Mexico, warming winter temperatures have resulted in the expansion of Avicennia germinans (black mangrove) into forb-dominated salt marshes, resulting in a shift in ecosystem structure that can impact the ecosystem services marshes provide, including biogeochemical processes such as nitrogen removal. There have been limited studies addressing how mangrove expansion impacts nitrogen removal rates in salt marshes, but it is possible that mangroves enhance microbial nitrogen removal capacity through more efficient oxygen translocation to sediments. However, mangroves are more sensitive to oiling (such as occurred during the 2010 Deepwater Horizon spill) than marsh plants, such as Spartina alterniflora, which have a higher turnover. Thus, even if they enhance nitrogen removal, if they cannot withstand disturbances such as oiling, there still may be a loss of function associated with woody encroachment. We conducted a field study to assess the impact of woody encroachment in mediating biogeochemical recovery 7 to 8 years after the Deepwater Horizon oil spill. We collected sediments from S. alterniflora- and A. germinans-dominated plots in the Chandeleur Islands (LA, United States), a chain of barrier islands in the northern Gulf of Mexico subjected to a range of oiling following the spill. We compared nitrate reduction rates (denitrification and dissimilatory nitrate reduction to ammonium), microbial community composition, and denitrifier marker gene abundance at sites subjected to light and moderate oiling using a combination of isotope pairing on sediment slurries, 16S sequencing, and qPCR. We predicted that overall, denitrification rates and microbial functional capacity would be enhanced in mangrove-dominated sediments. We also predicted that these enhancements would be diminished at the more intensely oiled site due to the higher susceptibility of A. germinans to oiling. Denitrification potential rates were higher in mangrove sediments at the lightly oiled site, whereas dissimilatory nitrate reduction to ammonium potential rates were higher in marsh sediments. Indicator analysis of 16S rRNA data selected putative sulfur cycling taxa as indicators of marsh sediments, suggesting that changes in oxygen availability associated with encroachment may be driving the differences in process rates. There was no difference in process rates between plant types at the moderately oiled site, where heavily weathered oil residue was still present. Sediment nutrient stocks were lower in moderately oiled mangrove plots than in lightly oiled mangrove plots, suggesting that sediment fertility recovery following the spill may have been slower in the mangroves, contributing to a change in ecosystem function. This study shows that woody encroachment has the potential to impact both the biogeochemical services that marshes provide and their response to and recovery from disturbances.