Sea-level rise and the emergence of a keystone grazer alter the geomorphic evolution and ecology of southeast US salt marshes

Abstract

Keystone species have large ecological effects relative to their abundance and have been identified in many ecosystems. However, global change is pervasively altering environmental conditions, potentially elevating new species to keystone roles. Here, we reveal that a historically innocuous grazer-the marsh crab Sesarma reticulatum-is rapidly reshaping the geomorphic evolution and ecological organization of southeastern US salt marshes now burdened by rising sea levels. Our analyses indicate that sea-level rise in recent decades has widely outpaced marsh vertical accretion, increasing tidal submergence of marsh surfaces, particularly where creeks exhibit morphologies that are unable to efficiently drain adjacent marsh platforms. In these increasingly submerged areas, cordgrass decreases belowground root:rhizome ratios, causing substrate hardness to decrease to within the optimal range for Sesarma burrowing. Together, these bio-physical changes provoke Sesarma to aggregate in high-density grazing and burrowing fronts at the heads of tidal creeks (hereafter, creekheads). Aerial-image analyses reveal that resulting "Sesarma-grazed" creekheads increased in prevalence from 10 ± 2% to 29 ± 5% over the past <25 y and, by tripling creek-incision rates relative to nongrazed creekheads, have increased marsh-landscape drainage density by 8 to 35% across the region. Field experiments further demonstrate that Sesarma-grazed creekheads, through their removal of vegetation that otherwise obstructs predator access, enhance the vulnerability of macrobenthic invertebrates to predation and strongly reduce secondary production across adjacent marsh platforms. Thus, sea-level rise is creating conditions within which Sesarma functions as a keystone species that is driving dynamic, landscape-scale changes in salt-marsh geomorphic evolution, spatial organization, and species interactions.

Keywords: biodiversity; bioturbation; ecosystem engineer; herbivory; morphodynamics.

Fig. 1.

Sea-level rise, submergence, and Sesarma-grazing trends. (A) Relative sea-level rise recorded at the Charleston, SC (northern; red); Fort Pulaski, GA (central; blue); and Fernandina Beach, FL (southern; green) NOAA tide stations from 1940 to 2019. Trend lines and black text denote the average annual rate of sea-level rise (SLR) during the 1940 to 1998 (T1) and 1999 to 2019 (T2) time periods. (B) Rates of salt-marsh-platform vertical accretion measured via ²¹⁰Pb, SET, ¹³⁷Cs, and Feldspar marker horizon methods are shown as mean + SE for each method for salt marshes located in each subregion. Dashed lines refer to the relative rate of sea-level rise in each subregion at T1 and T2. (C) First-order approximations of the duration of tidal submergence, or inundation time (hours per day), experienced by salt-marsh creekheads under each of five marsh vertical accretion-rate scenarios. The dashed gray line denotes the boundary of T1 and T2. (D) Aerial-image analysis of 1-km² areas at each of nine sites (site name abbrevations are reported inset and across panels) revealed that grazed creek prevalence increased at all sites between TP1 (light shading) and TP2 (dark shading) and that the elongation rate between the two time points is faster for grazed creeks than ungrazed creeks in all locations. (E) At all sites, marsh-drainage density increased with the rise in grazed creek prevalence observed between TP1 and TP2. (F) Across all sites, grazed creek prevalence at TP2 strongly predicted the percent change in drainage density between the two time points. Model results are presented (inset) and aerial images depicting changes in creek length between TP1 and TP2 are shown (E and F, Lower).

Fig. 2.

Geospatial drivers of Sesarma-grazed creekhead distribution. (A) Drainage ratios of grazed and incipient-grazed creeks were six times higher than those of ungrazed creeks. (B) Marginal incipient-grazed creeks (five minimum drainage ratios) and ungrazed creeks (five maximum drainage ratios) were assessed by using linear regression analyses. Results identified a threshold drainage ratio of 266 m² per m tidal creek (dashed blue and green regression lines). Above this line, we suggest that the volume of water that requires drainage per tidal cycle (i.e., tidal prism) is greater than the creek-drainage capacity, and, as a result, grazing is likely to initiate. Below this line, the creek’s hydraulic capacity is sufficient to drain the adjacent marsh platform, and the creek remains ungrazed. (C) Five creeks with a history of grazing at TP1 that transitioned to an ungrazed status at TP2 show that this transition away from grazing coincides with the creek transitioning from above to below the identified threshold drainage ratio.

Fig. 3.

ROMS simulations. (A–C) ROMS simulations were conducted by using three idealized model bathymetries that differed only in the length of the tidal creek, such that their drainage ratios were those of grazed (A; 849 m² per m of tidal creek), threshold (B; 266 m² per m of tidal creek), and ungrazed conditions (C; 132 m² per m of tidal creek). Submergence, or inundation time, is presented on a scale of blue color, with darker hues representing longer periods of submergence. In all panels, a location standardized for elevation (+0.70 m ASL) and proximity to tidal creekhead (20 m) is shown as a red diamond. (D) Inundation time at this reference point is presented for the three bathymetries. (E) Adjusting the elevation of the threshold simulation for relative rates of sea-level rise, inundation time is presented for the threshold drainage ratio in 1940. (F and G) Percent increases in inundation time between 1940 and both 1999 (F) and 2019 (G) are depicted on a color scale of yellow (low) to red (intermediate) to purple (high). (H) Changes in inundation time at the reference point are shown between 1940, 1999, and 2019.

Fig. 4.

Sesarma effects on invertebrate communities. Surveys of the border and platform zones in Sesarma-grazed (A) and ungrazed marshes (B) reveal differences in invertebrate community biomass and composition (C). In C, grayscale colors denote macrobenthic invertebrate functional groups comprising the community, and column heights and error bars represent the mean invertebrate biomass ± SE, respectively, of 56 replicate survey quadrats per marsh type and zone; values were averaged across regional sites because no significant effect of site was found. Image credit: C. Ortals.

Fig. 5.

Experimental results. (A) The predation rate on mussel aggregations deployed on grazed (blue) and ungrazed (green) creek borders and marsh platforms, reported as the percent of each mussel aggregation consumed after 4 wk (data are shown as the mean ± SE of eight aggregations per creek type and zone; data are pooled across three sites). (B) Classification tree analysis of predation rates on mussels (dark brown icons) and snails (light brown icons) revealed a hierarchy of factors controlling benthic macroinvertebrate survival. For both mussels and snails, predator exclusion (i.e., full cage vs. control and elevated cage) explained the greatest degree of variance in the data, followed by creek type (i.e., ungrazed vs. grazed) and then zone (i.e., platform vs. border).

Fig. 6.

Sesarma’s community importance and effects on salt-marsh interaction networks. (A) Sesarma’s community importance in controlling cordgrass biomass, mussel survivorship, macrobenthic invertebrate community biomass, and creek elongation, averaged across border and platform zones at the three Sapelo Island sites. All data are shown as mean ± SE of a minimum of 24 replicate measurements per grazed and ungrazed creekshed assessed for each factor. Positive community importance reflects an increase in the metric, while negative values reflect a decrease in the metric when Sesarma are present in higher density (grazed creeks) as compared to lower densities (ungrazed creeks). Species with community importance values far greater than ±1 (denoted by dashed lines) are considered “keystone” species. (B and C) Conceptual diagram summarizing the likely differences in species interaction networks in southeastern US Atlantic salt marshes in this “historic” period of 1940 to 1999 (B) vs. the contemporary period of 1999 to 2019 when Sesarma-grazed creeks have become prevalent features (C) due to Sesarma’s direct and indirect effects (colored and gray arrows, respectively) on other community members.