Trophic transfer of polylactic acid microplastics induces multisystemic dysfunction in Tenebrio molitor and challenges the perceived safety of biodegradable plastics

Abstract

The trophic transfer of microplastics (MPs) in terrestrial food webs, particularly involving biodegradable polymers such as polylactic acid (PLA), remains poorly understood. In this study, we simulated a detritivore-based experimental food chain to investigate the transfer of PLA-MPs from Musca domestica to Tenebrio molitor and the resulting ecotoxicological effects. M. domestica larvae were exposed to PLA-MPs incorporated into the rearing substrate (4.2 mg kg⁻¹), and the presence of MPs was confirmed in newly emerged adults. These adults were then offered as prey to T. molitor larvae for five days, with subsequent confirmation of trophic transfer of PLA-MPs. Indirect exposure led to pronounced behavioral alterations, including locomotor rigidity, exploratory hesitation, and heightened phototactic response, with metrics such as immobility time, direction reversals, and spatial recurrence emerging as key discriminators in multivariate analysis. Growth and developmental impairments were also evident, characterized by ontogenetic delay, reduced biomass gain, and shifts in metabolic conversion. At the biochemical level, exposure induced marked disruptions in energy reserves (reduced protein and carbohydrate levels and elevated triglycerides), intensified digestive enzyme activity, and a pronounced redox imbalance – evidenced by increased reactive oxygen species, malondialdehyde, and nitrite, along with decreased superoxide dismutase and catalase activity. Neurochemical dysfunctions were also observed, including alterations in dopamine and serotonin levels and changes in acetylcholinesterase activity. Furthermore, functional network analysis revealed connectivity losses, reduced topological resilience, and a reconfiguration of biochemical co-activity patterns in response to PLA-MP exposure. Finally, integrative modeling via sparse partial least squares discriminant analysis demonstrated clear segregation between experimental groups, consolidating the evidence for multisystemic effects induced by trophic PLA-MP transfer. Collectively, these findings expand our understanding of the ecotoxicological risks posed by biodegradable polymers in terrestrial ecosystems, challenging the perceived environmental safety of materials labeled as biodegradable.