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Cultures in humans and other species are maintained through interactions among conspecifics. Declines in population density could be exacerbated by culture loss, thereby linking culture to conservation. We combined historical recordings, citizen science and breeding data to assess the impact of severe population decline on song culture, song complexity and individual fitness in critically endangered regent honeyeaters (Anthochaera phrygia). Song production in the remaining wild males varied dramatically, with 27% singing songs that differed from the regional cultural norm. Twelve per cent of males, occurring in areas of particularly low population density, completely failed to sing any species-specific songs and instead sang other species' songs. Atypical song production was associated with reduced individual fitness, as males singing atypical songs were less likely to pair or nest than males that sang the …