First report of marine leech Limnotrachelobdella okae infestation in miiuy croaker (Miichthys miiuy): An emerging threat to Chinese mariculture.

Abstract

From January to April 2025, an unprecedented epizootic outbreak of Limnotrachelobdella okae infested Miichthys miiuy in China, reducing survival rates to 7.69 % and causing massive economic losses. Clinical manifestations included ulcerative lesions, gill filament pallor, and anorexia. The present study aimed to characterize this emerging parasitic threat and the involved pathogenic mechanisms. Leeches collected from infected fish were morphologically and phylogenetically identified. Although first documented to induce mortality in M. miiuy, L. okae exhibited broad host plasticity. Pathological impacts were assessed via hematological profiling and histopathology. The pathological effects of the infestation included a cascade of hemorrhagic anemia (40 % decrease in red blood cells and 39 % decrease in hemoglobin), systemic immunosuppression (69 % decrease in white blood cells), and anemia-induced multiple organ dysfunction (liver, spleen, head kidney, and trunk kidney). Furthermore, field data confirmed temperature (>20 °C) as the dominant driver of epidemic termination (Pearson's r = -0.717, p = 0.045). Environmental tolerance assays of L. okae demonstrated strict cryohalophilic dependence, with optimal viability at 5-15°C and 15-25 ‰ salinity, and complete mortality was observed at 25 °C. The present study identified L. okae as an emerging threat to mariculture diversification. The present findings expand the spectrum of high-risk parasites jeopardizing marine aquaculture. Elucidation of the behavioral ecology and pathogenesis of L. okae will advance targeted surveillance and mitigation strategies.