Several long-term studies have monitored populations of algal symbionts, Symbiodinium sp., in coral hosts over different temporal and spatial scales, and among multiple host species. The extension of these studies to include environmental pools of algal symbionts from sources such as the water column, sediments, free-floating mucus mats and those settling on biofilms has only been studied by a few, yet has the potential to enhance our understanding of the dynamics and controls on symbiont populations. Adaptive changes in the coral symbiont complement rely either on the uptake of new strains from the environment or population expansion of rarer strains in the existing symbiont population. The relative scope for these alternative pathways of uptake is unknown. This study therefore examined spatial changes in Symbiodinium clades within the water column at two different time periods and compared these with other environmental pools (biofilms, sediments, and mucus mats) and those within the dominant reef-building species at the study site, Acropora muricata. A diversity of algal symbiont clades were detected in environmental pools, with specific clades associated with different habitats. At an island scale, there was significant variation in clade composition between sites separated by 0.5–7 km, a result which was repeated for both sample periods encompassing different seasons (March 2009 and August 2010). Although no single environmental pool contained a Symbiodinium complement comparable to that of the host coral species investigated, the dominant coral Symbiodinium were available in combinations of the environmental pools, indicating that the coral has the potential to obtain its symbionts from a variety of environmental sources.