Ecosystem metabolism regulates seasonal bioaccumulation of metals in atyid shrimp (Neocaridina denticulata) in a tropical brackish wetland

Abstract

Natural dissolved organic matter (DOM) forms the base of aquatic food webs and is a key environmental factor that affects the bioavailability of metals for aquatic organisms. Aquatic communities are naturally exposed simultaneously to environments containing a mixture of metals and varying DOM levels and compositions. However, the exact effect of DOM on metal bioaccumulation is difficult to predict due to temporal and spatial variations in sources, production, and consumption of DOM, and to interactions between DOM and metals. Ecosystem metabolism describes the process of organic carbon production and consumption and, therefore, the trophic status of ecosystems. However, whether and how ecosystem metabolism determines the seasonality of metal bioaccumulation remains unclear. The present study used in-situ water quality sondes and discrete field samplings to establish the relationship between the seasonality of ecosystem metabolism; related environmental and limnological regulators; the metal speciation and concentration in bulk water and sediments; and their metal bioaccumulation. The target population consisted of atyid shrimp (Neocaridina denticulata) in a brackish constructed wetland in tropical Taiwan was sampled between August 2014 and November 2015. Metal bioaccumulation displayed distinct seasonal patterns that peaked in summer (Cu, Cd, Cr, Zn, Mn, and Se) or winter (Pb and Ni). The in situ production (gross primary production) and heterotrophic consumption (ecosystem respiration) of organic matter significantly decreased with increasing waterborne DOM levels in this heterotrophic wetland. Both dissolved free metals bioavailable for respiratory surfaces (As, Zn, Cu, and Cr) and insoluble metals available for dietary intake (Mn and Ni) decreased with increasing DOM, as well as with decreasing gross primary production and ecosystem respiration. Seasonal variations of metal bioaccumulation also paralleled the transition in wetland trophic status, which reflected the effect of potential qualitative changes in the wetland DOM pool. Bioaccumulation of most metals displayed strong correlations with gross primary production, ecosystem respiration, and wetland trophic status. Our findings demonstrated that ecosystem metabolism can play a key mediating role in the seasonality of metal bioaccumulation in atyid shrimp, as it links the variation and interaction between DOM level/source, the speciation/bioavailability, and the uptake efficiency for metals by aquatic organisms. This study contributes to the temporal-specific risk assessment of aquatic metal exposure in regional environmental settings. It also reveals ecosystem-specific spectra in the context of changes in climate and environment.

Keywords: Allochthony; Dissolved organic matter; Ecosystem respiration; Gross primary production; Neocaridina denticulate; Trophic status.