Comparing the Behavioral Impacts of Heavy Metals and Rare Earth Elements on Black Soldier Fly (Hermetia illucens) Larvae

Heavy metals (HMs) and rare earth elements (REEs) increasingly co-occur in environmental waste streams and soils, yet their comparative neurotoxic mechanisms and sublethal effects on invertebrate decomposers remain poorly understood. This study used black soldier fly larvae (BSFL, Hermetia illucens) to perform a comparative behavioral and transcriptomic assessment of 23 HMs and 16 REEs across two acute exposure concentrations. High-throughput video tracking and phenomic analysis showed HMs produced broader disruption than REEs, with low-concentration HMs inducing locomotor suppression, thigmotaxis, reduced fractal dimension and entropy, progressing to severe motor inhibition and rigid low-entropy states. In contrast, REEs showed a biphasic profile, shifting from selective locomotor suppression with preserved organization at low concentrations to hyperactive, fragmented, high-entropy movement with increased thigmotaxis at high concentrations. PCA and hierarchical clustering integrated endpoints into four neurobehavioral fingerprints segregating metal class and concentration, with partial overlap of high-concentration REEs with HMs along a shared high-toxicity axis. Transcriptomic profiling showed that cobalt as a representative HM activated DNA damage and cell-cycle pathways, perturbed energy signaling, and suppressed neuroactive ligand–receptor interaction, whereas samarium as a representative REE downregulated xenobiotic metabolism, oxidative phosphorylation, glutathione metabolism, and synaptic vesicle cycling. These findings demonstrate distinct concentration-dependent neurotoxic modes of action for HMs and REEs and establish BSFL behavioral phenomics integrated with transcriptomics as a mechanistically informative platform for ecological risk assessment in contaminated waste systems.