Overcoming Detection Lag in a Cryptic Panzootic: Chytrid Invasion Linked to Historically Enigmatic Amphibian Declines in the Brazilian Atlantic Forest

Abstract

As human activity accelerates the spread of pathogens and other invasive species, reconstructing the cryptic early dynamics of undetected invasions has become a central challenge in disease ecology and invasion biology. Here, we leverage museum specimens to reconstruct the invasion of Batrachochytrium dendrobatidis (Bd), a fungal panzootic driving global amphibian biodiversity loss, across historically enigmatic declines in the Brazilian Atlantic Forest. Two hypotheses have been proposed to explain Bd's historical dynamics in this region: long-term enzootic persistence versus recent epizootic invasion coinciding with declines. Using molecular screening, histopathology, and genotyping of museum and modern specimens, we find no evidence of Bd infection prior to the decline, followed by widespread infection immediately thereafter. Only the global panzootic lineage (Bd-GPL) was detected during the first year of post-decline sampling, implicating its invasion in driving regional losses. Infection prevalence varied among species following the decline, likely reflecting species-specific interactions between baseline susceptibility and ecological exposure risk. Contemporary host populations exhibit more uniform prevalence regardless of decline history, consistent with the evolution of pathogen tolerance under enzootic conditions. Together, these results provide the first site-specific evidence linking Bd-GPL invasion to enigmatic amphibian declines in Brazil and demonstrate the power of museum collections for resolving detection lag dynamics in emerging infectious diseases.