Response of seagrasses to aquaculture effluents and the filtering capacity of seagrass meadows for anthropogenic nitrogen in Hainan, China

Abstract

Seagrasses are marine flowering plants that inhabit coastal waters. Due to their high productivity, seagrass meadows provide important ecosystem services at the boundary between land and the ocean. At this position, they are impacted by local and global influences from land and sea. Especially human-caused nutrient and organic matter input from land into coastal waters threaten seagrasses globally. Excess nutrients and organic material cause eutrophication in coastal waters. During the process of eutrophication, nutrients induce algal growth, which results in light limitation for the benthic community. The microbial degradation of the algal biomass consumes oxygen. Thus, oxygen may become limiting, further harming the benthic community. Globally, the intensive use of the coastal zone through urbanisation and agriculture alters the hydrology and biogeochemistry of watersheds which increases the nutrient runoff into the coastal zone. An emerging but previously underestimated source of nutrients in the coastal zone is the aquaculture industry. As overfishing progressively threatens wild fish stocks, aquaculture is considered an alternative source for animal protein to feed the world’s population. Globally, aquaculture production is steadily increasing; in 2018, aquaculture production was already similar to the global capture fisheries production. There is a strong concentration of aquaculture production in Asia, where 80% of the global yield is produced. Effluents, rich in nutrients and organic matter, are often directly discharged into the environment without prior treatment, inducing eutrophication and thus threatening coastal ecosystems. One ecosystem service of seagrass meadows is filtering nutrients from the water column, therefore mitigating eutrophication. Even though it is known that eutrophication causes seagrass loss, the trajectory and mechanisms involved in this process remain poorly understood. Furthermore, tropical seagrasses are understudied compared to temperate seagrasses, even though seagrass species diversity is highest in the tropical Indo-Pacific. This dissertation aimed to investigate the effect of aquaculture effluent induced eutrophication on tropical multispecies seagrass meadows and their inorganic nitrogen filter function in the short-term and the long-term. These effects were studied in NE of the tropical island Hainan, China. On land, a vast area is covered by coastal aquaculture ponds, while in the coastal back-reef area, multispecies seagrass meadows grow. Different seagrass meadows are subjected to different intensities and histories of aquaculture effluent input; therefore, these sites represent a natural laboratory to investigate the long-term effects of aquaculture effluents. Three back-reef areas with different exposure to aquaculture effluent input were chosen to follow the long-term impact of eutrophication on seagrass meadows for nearly a decade. Overall, the aboveground seagrass biomass in the study area declined by 87% during this period. At sites directly and chronically affected by eutrophication, seagrass meadows nearly or completely disappeared. Furthermore, species diversity was lower at these sites. In meadows only remotely and periodically affected by eutrophication, seagrass diversity remained stable. I modelled the empirical relationship between seagrass biomass and the dissolved inorganic nitrogen (DIN) concentration in the coastal water as a proxy for eutrophication. I found that above a threshold of 8 µM DIN concentration, seagrass meadows will disappear in the long-term. The large seagrass species Enhalus acoroides and Thalassia hemprichii seem to be more resistant to eutrophication as they were the last species found at sites chronically affected by aquaculture effluents. At the same time, the species Cyomdocea rotundata, Cymodocea serrulata, Halophila ovalis, Halodule uninervis, and Syringodium isoetifolium had already disappeared. To understand how eutrophication drives seagrass declines, I investigated the immediate responses of different seagrass species to eutrophication. Therefore, I artificially fertilized in an in situ experiment a part of a periodically eutrophied seagrass meadow in dry and wet season. After four weeks, I measured the morphological and physiological adaptions of different seagrass species to fertilization. In the dry season, seagrasses were nutrient-limited, as fertilization caused higher growth rates and larger leaf areas. In the wet season, the plants had lower growth rates and smaller leaf areas than in the dry season, probably induced by eutrophic conditions, including light limitation and high nitrogen concentrations in the water column caused by heavy rainfall. Since nutrient concentrations were already high in wet season, the artificial fertilization had little effect on the plant’s physiology and morphology. Only T. hemprichii morphologically further adapted to the additional nutrient enrichment. To sustain their high productivity, seagrasses need to take up nutrients from their environment. Seagrasses can mitigate eutrophication by taking up inorganic nutrients from the water column through their leaves. The same in situ experiment was conducted to investigate the impact of eutrophication on the inorganic nitrogen filter function of seagrasses. Inorganic nitrogen uptake rates of different seagrass species were quantified under different trophic conditions. Furthermore, the nitrogen demand for leaf growth was calculated from the leaf growth rates and the nitrogen content in the leaves. All species preferred ammonium over nitrate, but at low nitrogen availabilities, also nitrate was an important nitrogen source. The daily inorganic nitrogen uptake and the nitrogen demand normalised by leaf area did not differ between seasons, experimental treatments, and species. However, T. hemprichii covered less of its nitrogen demand by uptake through leaves. Conceivably, this species internally recycles nitrogen more efficiently than other species. This implies that eutrophication has a strong negative effect on the nitrogen filter function of seagrass meadows because it affects seagrass leaf growth and leaf biomass and, therefore, their nitrogen demand and uptake. Furthermore, the species composition shifted towards a species that covers less of its nitrogen demand by uptake from the water column. Finally, the impact of eutrophication on the nitrogen retention time and nitrogen cycling in the ecosystem is discussed. Nitrogen bound in biomass is only temporarily retained and remains in the system. It can be remineralised and released again into the water. The retention time depends on biochemical and physical parameters, and eutrophication can accelerate nitrogen remineralisation. Therefore, once the nitrogen filter function of a seagrass meadow is surpassed, eutrophication is a self-reinforcing process at multiple levels. In the short-term, it reduces seagrass growth and, therefore, the nitrogen demand. In long-term, it causes seagrass loss and a species shift towards a species with a less effective nitrogen filter function. Furthermore, it accelerates nitrogen cycling. To conclude, eutrophication caused by aquaculture effluents is a severe threat to seagrass meadows and, therefore, the release of nutrients into coastal waters needs to be reduced to conserve this important coastal ecosystem.

This dissertation aimed to investigate the effect of aquaculture effluent induced eutrophication on tropical multispecies seagrass meadows and their inorganic nitrogen filter function in the short-term and the long-term. These effects were studied in NE of the tropical island Hainan, China. In the short-term, eutrophication from aquaculture effluents reduced seagrass growth and, therefore, the seagrass’ nitrogen demand. In the long-term, eutrophication caused seagrass loss and a species shift towards a species with a less effective nitrogen filter function. To conclude, eutrophication caused by aquaculture effluents is a severe threat to seagrass meadows. Therefore, the release of nutrients into coastal waters needs to be reduced to conserve this important coastal ecosystem.