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

Abstract

Seagrass meadows form essential ecological components in coastal zones but are rapidly declining worldwide due to anthropogenic impacts, including eutrophication and climate change-related heat waves. An important consequence of increased eutrophication is organic matter input in the sediment, which, together with raised temperatures, stimulates the production of toxic sulfide. Although multiple recent studies have highlighted that seagrass can engage in a mutualistic relationship with lucinid bivalves alleviating sulfide toxicity in the rhizosphere, it remains unclear how this mutualism is affected by temperature and eutrophication. To unravel this relation, we investigated the response of the seagrass Zostera noltii to contrasting sediment organic matter conditions, temperatures and presence/absence of the lucinid clam Loripes orbiculatus in a full-factorial mesocosm experiment. Results demonstrate that temperature increased porewater sulfide and nutrient levels, particularly in treatments with high sediment organic matter content. Interestingly, L. orbiculatus reduced not only sulfide levels, but also porewater nutrients. The removal of sulfide in turn stimulated Z. noltii growth, despite lower nutrient availability. Finally, increased temperature suppressed the mutualistic benefit for Z. noltii as sulfide detoxification became hampered. We conclude that, as eutrophication remains an issue in the coastal zone and temperature extremes will likely become more common in the future, seagrass meadows where lucinids occur may need to increasingly rely on this mutualism. At the same time, however, this interaction will become more strained, with an inherent increasing risk of mutualism breakdown.

A facultative mutualism facilitates European seagrass meadows

“…Our SEM analyses supports the hypothesis that the observed linear correlation between L. orbiculatus and Z. noltii in this continent-wide study result from a generic facultative mutualistic feedback. These findings support previous experimental laboratory studies that found a positive effect of L. orbiculatus on seagrass biomass (van der Heide et al 2012, de Fouw et al 2022. Based on the logistic regression analysis on the presence-absence of the bivalves, we expected a negative effect of mud content on L. orbiculatus density in our SEM.…”

“…4a). The nature and strength of this association is in line with experimental mesocosm results from other studies showing a positive effect on seagrass growth due to sulphide detoxification by the lucinids (van der Heide et al 2012, Chin et al 2021, de Fouw et al 2022. In addition, we found a positive effect of higher temperatures (i.e.…”

“…Apart from a positive effect, seagrass may also increase mud content potentially negatively influencing lucinid bivalve densities (Anderson 2008, Ellis et al 2017, Douglas et al 2019). In turn, we expect the lucinids positively affect seagrass health due to sulphide detoxification (van der Heide et al 2012, de Fouw et al 2022). However, as we do not have data of porewater sulphide levels and such measurements typically only reflect recent conditions, we used biomass and SSI as long‐term proxy for seagrass health for Z. noltii and Z. marina , respectively.…”

“…To mitigate sulphide accumulation, however, seagrasses can engage in a facultative mutualistic interaction with lucinid bivalves and their gill‐inhabiting, sulphide‐oxidizing bacteria. In return, the bivalves and their endosymbionts profit not only from sulphide that is indirectly provided by the seagrasses, but also from oxygen released by seagrass roots and protection from predation due it's complex root and rhizome network (van der Heide et al 2012, de Fouw et al 2016b, de Fouw et al 2018, van der Geest et al 2020, Chin et al 2021, de Fouw et al 2022).…”