Repetitive desiccation events weaken a salt marsh mutualism

Abstract

Salt marshes suffered large‐scale degradation in recent decades. Extreme events such as hot and dry spells contributed significantly to this, and are predicted to increase not only in intensity, but also in frequency under future climate scenarios. Such repetitive extreme events may generate cumulative effects on ecosystem resilience. It is therefore important to elucidate how marsh vegetation responds to repetitive stress, and whether changes in key species interactions can modulate vegetation resilience. In this study, we investigated how moderate but repetitive desiccation events, caused by the combined effects of drought and high temperatures, affect cordgrass (Spartina alterniflora), the dominant habitat‐forming grass in southeastern US salt marshes. In a 4‐month field experiment, we simulated four consecutive desiccation events by periodically excluding tidal flooding and rainfall, while raising temperature. We crossed this desiccation treatment with the presence/absence of ribbed mussels (Geukensia demissa) – a mutualist of cordgrass known to enhance its desiccation resilience – and with grazing pressure by the marsh periwinkle (Littoraria irrorata) that is known to suppress cordgrass’ desiccation resilience. We found that each subsequent desiccation event deteriorated sediment porewater conditions, resulting in high salinity (53 ppt), low pH‐levels (3.7) and increased porewater Al and Fe concentrations (≈800 μmol/L and ≈1,500 μmol/L) upon rewetting. No effects on porewater chemistry were found as a result of snail grazing, while ribbed mussels strongly mitigated desiccation effects almost to control levels and increased cordgrass biomass by approximately 128%. Importantly, although cordgrass generally appeared healthy above‐ground at the end of the experiment, we found clear negative responses of the repetitive desiccation treatment on cordgrass below‐ground biomass, on proline (osmolyte) levels in shoots and on the number of tillers (−40%), regardless of mussel and/or snail presence. Synthesis. Even though the mutualism with mussels strongly mitigated chemical effects in the sediment porewater throughout the experiment, mussels could not buffer the adverse ecophysiological effects observed in cordgrass tissue. Our results therefore suggest that although mussels may alleviate desiccation stress, the predicted increased frequency and intensity of hot dry spells may eventually affect saltmarsh resilience by stressing the mutualism beyond its buffering capacity.

Ribbed mussel Geukensia demissa population response to living shoreline design and ecosystem development

“…Moreover, mussels enhance marsh resilience by capturing sediment and promoting accretion, particularly important in areas experiencing high rates of sea level rise and/or with barriers to landward marsh migration. Furthermore, in the southeastern USA, through their mutualistic relationship with cordgrass, ribbed mussels may alleviate stress (high soil salinity, soil acidification) for cordgrass by enhancing water storage and nutrient availability (Angelini et al 2016, Derksen‐Hooijberg et al 2019). As the climate continues to warm, extreme events such as droughts are expected to increase in severity and frequency (Hansen et al 2012) and ribbed mussels may contribute to the resistance and/or recovery of salt marshes to droughts throughout their range.…”

“…Geukensia demissa (ribbed mussel) is a key bivalve species in salt marshes that enhances marsh resilience (Bertness et al 2015, Derksen‐Hooijberg et al 2019), nitrogen removal (Jordan and Valiela 1982, Galimany et al 2017, Bilkovic et al 2017 b , Isdell 2018), and water and habitat quality (Ward and Shumway 2004, Angelini et al 2015, Isdell 2018, Kreeger et al 2018). Ribbed mussels actively manipulate their habitat, fundamentally influencing the productivity of the marsh through their mutualistic relationship with Spartina alterniflora (cordgrass henceforth).…”

Facilitation of a tropical seagrass by a chemosymbiotic bivalve increases with environmental stress

“…For example, across a large set of experimental reforestations in a Mediterranean climate, the facilitative effect of nurse shrubs on growth and survival of woody seedlings was found to be strongest at low altitudes and on sunny, drier slopes (Gómez‐Aparicio et al., 2004). Recent work in US salt marshes shows that ribbed mussels increase cordgrass resilience to drought but are unlikely to mitigate all negative effects when cordgrass is subjected to repeated desiccation events (Angelini et al., 2016; Derksen‐Hooijberg et al., 2019). In seagrass ecosystems, knowledge of lucinid abundances and distributions, in combination with environmental monitoring (e.g.…”

“…A number of studies show that facultative mutualisms are vital to the persistence of foundation species, conferring benefits such as greater tolerance to environmental stress (e.g. thermal or drought; Afkhami, McIntyre, & Strauss, 2014; Angelini et al., 2016; Derksen‐Hooijberg et al., 2019; Redman, Sheehan, Stout, Rodriguez, & Henson, 2002) and resistance to long‐term loss of biomass (Peres et al., 2016).…”

Facultative mutualisms: A double‐edged sword for foundation species in the face of anthropogenic global change

“…During drought, the mutualism therefore buffers a second stressor in ways similar to scenario 2. Recent work, however, suggests that intense or repetitive droughts may ultimately exceed the mutualism's buffering capacity (Derksen‐Hooijberg et al., 2019). Should these extreme events increase in both severity and frequency as predicted, the salinity‐buffering mechanism will be under intensifying pressure, increasing the likelihood of salt marsh collapse (Angelini et al., 2016; Derksen‐Hooijberg et al., 2019).…”