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

Abstract

Facilitation of foundation species is critical to the structure, function and persistence of ecosystems. Understanding the dependence of the strength of this facilitation on environmental conditions is important for informed ecosystem management and for predicting the impacts of global change. In coastal seagrass habitats, chemosymbiotic lucinid bivalves can facilitate seagrasses by decreasing potentially toxic levels of sulphide in sediment porewater. However, variation in the strength of lucinid–seagrass facilitation with environmental context has not been experimentally investigated. We tested the hypothesis that the presence of the tiger lucine Codakia orbicularis becomes more important to the growth and survival of the seagrass Thalassia testudinum under decreased light availability and increased sulphide stress. In a mesocosm experiment, we reduced average ambient‐light to T. testudinum by 64% and/or increased sediment porewater sulphide concentrations by ~200% and compared growth and tissue chemistry of T. testudinum with and without C. orbicularis. We found that T. testudinum was better able to maintain growth under shading and sulphide stress when C. orbicularis was present. C. orbicularis strongly decreased sediment porewater sulphide, an effect that minimized sulphur build‐up in seagrass tissue and was likely achieved through bioirrigation as well as chemoautotrophy. The relative effects of C. orbicularis on T. testudinum growth were strongest in the presence of environmental stressors. Synthesis. The strength of lucinid–seagrass facilitation increases under environmental conditions that hinder the ability of seagrass to detoxify sulphide. Our results provide evidence of a potential mechanism by which the spatiotemporal association between lucinids and seagrasses is maintained and support the incorporation of interspecific facilitation into conservation and restoration strategies for foundation species in the face of increasing anthropogenic impact and global change.

Increased temperature reduces the positive effect of sulfide-detoxification mutualism on Zostera noltii nutrient uptake and growth

“…For instance, recent work revealed that the endosymbiotic gill-bacteria are also capable of nitrogen fixation (diazotrophy), which suggests that, apart from sulfide detoxification, the lucinid− bacteria consortium might also benefit seagrasses under nutrient-poor conditions by providing nitrogen (König et al 2017, Petersen et al 2017, Cardini et al 2019). In contrast, other studies have shown that sediment porewater nutrients are de creased in the presence of lucinids, suggesting that lucinids could cause or amplify nutrient limitation for seagrasses (van der Heide et al 2012, König et al 2017, Chin et al 2021. Clearly, the nutritional role of the facultative mutualistic interaction under different environmental conditions in seagrass systems is unclear.…”

“…The bacteria and the lucinid bivalves form a symbiotic relationship in which the clams transport sulfide and oxygen to their gills where the bacteria oxidize sulfide for synthesizing sugars that fuel the growth of both organisms (Cavanaugh 1983, van der Heide et al 2012. In this way, the seagrass and the lucinid−bacteria consortium engage in a facultative mutualism in which the seagrass provides the clams and their bacteria with sulfide and oxygen, while the seagrass profits from the removal of toxic sulfides (van der Heide et al 2012, van der Geest et al 2020, Chin et al 2021.…”

Inclusion of Intra- and Interspecific Facilitation Expands the Theoretical Framework for Seagrass Restoration

“…Considering differences in seagrass ontogeny as well as site characteristics and bivalve type will be key to determining the role of positive interactions and expanding the theoretical framework for restoration. In addition to nitrogen deposition, bivalves may facilitate seagrasses by reducing sulfide concentrations in the sediment (van der Heide et al, 2012;de Fouw et al, 2016;Chin, 2020;Van Der Geest et al, 2020) or by consuming and reducing epiphyte loads that could otherwise hinder seagrass photosynthesis (Peterson and Heck, 2001a,b). Although we did not test for the effect of bivalves on epiphytes in our experiments, we suspect that this mechanism would have had a stronger effect on the adult transplant experiment where clams were significantly larger than seed clams (<1 cm umbo width).…”

Nested interactions between chemosynthetic lucinid bivalves and seagrass promote ecosystem functioning in contaminated sediments

“…This holobiont was suggested to form a positive nested interaction with seagrasses (van der Heide et al, 2012). In this example of a nested ecosystem, the clam and its microbial symbionts are suggested to contribute to the removal of sulfide (toxic to the plant) from the sediments and thus to enhance seagrass growth (Chin et al, 2021). Additionally, a role of the lucinid clam Loripes orbiculatus in N provisioning to the seagrass ecosystem was recently proposed, given the ability of the symbionts to also fix atmospheric N 2 (Petersen et al, 2017;Cardini et al, 2019).…”