Risk assessment of persistent exposure to artificial light at night revealed altered behavior and metabolic patterns of marine nocturnal shellfish

The evolvement of urbanization has caused artificial light at night (ALAN) to be one of the major pollution sources in major cities, resulting in numerous environmental concerns. In view of the increasing intensity and range of ALAN, this study aims to evaluate the influence of ALAN on the physiology and behavior of the Pacific abalone Haliotis discus hannai, a typical nocturnal marine shellfish. Street lighting at night (SL6, lights on from 18:00 until 00:00; SL12, lights on from 18:00 until 06:00 the next morning) and car lighting (CL, lights were turned once every hour for 30 s and then turned off) were simulated indoors, with the natural light cycle group (lights on from 06:00 to 18:00) treated as the control group (CTR). The significantly higher cumulative distance covered along with the duration of abalone movement was observed in Group SL12 upon comparison with other groups (P < 0.05). Cosine rhythm analysis revealed that the peak phase of abalone's movement duration and cumulative distance moved in Group SL6 was shifted to ZT16:25 and ZT15:32, respectively, relative to Group CTR (ZT12:53 and ZT13:07). Correlation analysis affirmed that melatonin concentrations in all groups were significantly and negatively correlated with the abalone's movement duration and cumulative distance moved. Transcriptome sequencing analysis revealed 1599, 2142, 1507, 1676, 2355, and 1922 differentially expressed genes in the CTR vs. SL12, SL6 vs. CL, CTR vs. CL, SL12 vs. CL, CTR vs. SL6, and SL12 vs. SL6 comparisons, respectively. Based on the significantly enriched Kyoto Encyclopedia of Genes and Genomes pathways and weighted geneco-expression network analysis, quantitative real-time PCR was conducted for the validation of expression levels of 12 key genes in different groups. Amino acid catabolism and protein processing were the primary pathways used by abalone to acquire energy under the impact of ALAN. The targeted metabonomics analysis revealed that the concentrations of 20 of 23 amino acids were up-regulated in Group SL6. These results reveal the physiological adaptation and behavioral mechanisms of nocturnal marine shellfish under the impact of ALAN, and they also provide guidance for the conservation of nearshore benthic biodiversity and the optimization of urban night lighting schemes.