Metal bioaccumulation and transfer in benthic species based on isotopic signatures of individual amino acids in South China Sea cold seep environments

Abstract

Cold seeps are deep-sea ‘oases’ with dense and dominant coexisting populations of large mussels and tubeworms under extreme environments. Under such natural source of high metal concentrations, the present study investigated the metal bioaccumulation and transfer with trophic positions in six benthic species by the isotopic δ15N and δ13C signatures in the active Haima cold seep, South China Sea. Comparing the isotopic signatures of bulk-tissue and amino acids by compound-specific isotopic analysis (CSIA-AA), we found that the bulk trophic (TPB) values in the benthos except mussels were significantly higher than those of CSIA-based TPGlu-Phe values. The estimated CSIA-based TPGlu-Phe values showed a relatively compressed food chain with much changeable and unique amino acid isotopic heterogeneity, followed slim tubeworms (1.20)<mussels (1.38)<clams (1.52)<brittle stars (1.82)<giant tubeworms (2.16)<shrimps (2.31). All species accumulated relatively high concentrations of Fe, Zn, Cu, and Cr, especially for Zn in clams. Pearson correlation analysis showed that most metals had no significant relationship between their bioaccumulation and trophic positions, whereas Hg showed a significantly positive bioaccumulation through trophic transfer in such a compressed food chain. Water exposure was a major metal source rather than bacterial assimilation for most metals in the cold seep higher consumers. Hyperaccumulation of specific metals in some tissues of different benthos indicated different metal overflows in the Haima cold seep (As and Ni for tubeworms, Zn and Cd for clam gills, Ag and Cu for mussel gills). This study demonstrated high metal adaptations in different species and stable isotopic characteristics of amino acid metabolism in a natural high metal source of an active deep-sea cold seep, which is important for deep-sea development and environmental protection.