Regenerative responses and structural plasticity of gills in Atlantic salmon

Abstract

Introduction: Gill regeneration in teleosts represents a key adaptive mechanism for maintaining respiratory efficiency under environmental stress. This study provides the first detailed histological characterization of branchial regeneration in Atlantic salmon (Salmo salar) smolts reared under freshwater hatchery conditions. Material and methods: Fifty clinically healthy smolts were analyzed through anatomical, histological, and microcomputed tomography (micro-CT) approaches. Results: We observed that the regenerative blastema first gave rise to primary filaments with developing lamellae; subsequently, from this same structure, a second generation of filaments emerged, demonstrating the capacity of the blastema to produce multiple waves of filament outgrowth. Unlike zebrafish, where branchial regeneration after filament resection has been widely described, regeneration in Atlantic salmon occurs more slowly and has been poorly characterized despite its relevance for aquaculture. Quantitative morphometry showed that the blastema occupied 8–19% (mean 14%) of total gill area and correlated positively with the number of regenerated filaments (ρ = 0.5; p ≈ 0.011). PCNA immunostaining revealed active cell proliferation within filament cartilage (mean index: 38.9 ± 13.5%), confirming its role as a substrate for regeneration. Newly formed tissues exhibited differentiation into hyaline cartilage, smooth and striated muscle, and vascular structures. Lamellar density remained lower in regenerating filaments (33.8 ± 15.9 per 0.5 mm²) compared to healthy ones (48.6 ± 19.3 per 0.5 mm²; p = 0.013), indicating incomplete maturation during smoltification. Discussion: These findings demonstrate that branchial regeneration in S. salar occurs naturally, without amputation, likely as an adaptive response to transient hypoxia. Recognizing these histological patterns allows distinguishing physiological regeneration from pathology and offers new criteria for welfare and smolt-readiness assessment in aquaculture.