Bats are recognized as reservoirs for diverse paramyxoviruses, some of which are closely related to known human pathogens or directly implicated in zoonotic transmission. The emergence of the zoonotic Sosuga virus (SOSV) from Egyptian rousette bats (ERBs), which caused an acute febrile illness in a reported human case in Africa, has increased the focus on the zoonotic potential of the Rubulavirinae subfamily. Previous studies identified human parainfluenza virus 2 (HPIV2)- and mumps (MuV)-related viruses in ERBs from South Africa, with HPIV2-related viruses restricted to gastrointestinal samples, an underexplored target for rubulavirus biosurveillance, suggesting that sample-type bias may have led to their oversight. To address this, we performed a longitudinal analysis of population-level fecal samples from an ERB maternity roost for rubulavirus RNA, employing a broadly reactive hemi-nested RT-PCR assay targeting the polymerase gene. We detected HPIV2- and MuV-related viruses in addition to numerous pararubulaviruses, highlighting significant viral diversity. Temporal analysis of three major clades revealed peaks in rubulavirus shedding that correlated with seasonal environmental changes and host reproductive cycles, although shedding patterns varied between clades. These findings identify specific periods of increased risk for the spillover of bat-associated rubulaviruses to humans, providing critical information for developing targeted mitigation strategies to minimize zoonotic transmission risk within the local community.