Does ecotype matter? The influence of ecophysiology on benzo[a]pyrene and cadmium accumulation and distribution in earthworms

Abstract

Benzo[a]pyrene (BaP) and cadmium (Cd) are soil pollutants that persist in the environment and impacting soil health. Earthworms are selective consumers, yet little is known about how their feeding and burrowing habits translate into species-specific differences in pollution accumulation and distribution. Here, we exposed three ecophysiologically distinct earthworm species, Eisenia fetida (epigeic), Pheretima guillelmi (endogeic), and Metaphire guillelmi (anecic) to different concentrations (0, 1, 10, 30, 60, 100, 300, 500 mg/kg) of BaP or Cd in natural fluvo–aquic soil for 14 days. BaP and Cd accumulation and distribution patterns were analyzed at the individual and organ levels. The results showed that the adsorption behavior of BaP or Cd in earthworms and the organs fit the Langmuir adsorption model well (R2 > 0.8, p < 0.001). E. fetida and M. guillelmi accumulated more BaP than Cd, with the respectively higher predicted maximum internal concentration (Cmax) of BaP (1946.27 ± 306.29 mg/kg, 2046.61 ± 90.64 mg/kg) and the lower Cmax of Cd (279.75 ± 49.57 mg/kg, 318.11 ± 60.64 mg/kg), while P. guillelmi showed the opposite trend with 927.10 mg/kg of Cd Cmax and 358.82 ± 68.35 mg/kg of BaP Cmax. The low mobility of endogeic worms may reduce their BaP accumulation, and lead to a lower BaP bioaccumulation factor (BAF) than that observed for the other two earthworms; P. guillelmi had a BAF of 8.64 ± 1.79, which was far less than that of E. fetida (106.93 ± 11.84) and M. guillelmi (350.16 ± 67.15). Whereas the higher Cd accumulation in P. guillelmi may be due to their highly efficient geophagous feeding strategy, at the same time the highest Cd BAF achieved (e.g. 203.54 ± 19.96 under 1 mg/kg Cd exposure). BaP distributed mainly in the body walls of all three earthworms (average 60.78%), as its high hydrophobicity increased its dermal uptake. More BaP than Cd accumulated in the reproductive organs, and Cmax of BaP in E. fetida, P. guillelmi, and M. guillelmi in the reproductive organs was 4031.08 ± 1237.38 mg/kg, 490.76 ± 79.88 mg/kg, and 3675.24 ± 794.68 mg/kg, respectively. However, Cd was more abundant in the gizzard and gut, as its hydrophilic nature meant Cd was mainly ingested orally, and the Cmax of Cd in E. fetida, P. guillelmi, and M. guillelmi in the gizzard and gut, respectively, was 452.43 ± 48.33 and 360.83 ± 44.36 mg/kg, 996.03 and 809.11 mg/kg, and 93.37 and 109.19 mg/kg. By contrast, for E. fetida, more Cd was distributed in the body wall (average 50.16%), possibly due to its high affinity for this organ (the average logKL for the body wall was −3.60) predicted by the Langmuir adsorption model, also the worm ingested less soil. These data suggest that ecotype influences the accumulation and distribution of pollutants in earthworms, as their ecophysiological properties (e.g., motility, food choices, and feeding efficiency) affect their exposure to and ingestion of pollutants. The distinct chemical properties of BaP and Cd also appear to affect their accumulation and distribution in earthworms. These factors should be considered when using earthworms as bioindicators in environmental risk assessments.