Microbial colonisation of low grade sulphidic ores and subsequent growth in heap bioleaching systems has not been quantified rigorously. In this study, an experimental system simulating the sub-processes that occur at the agglomerate scale was used to quantify the colonisation, growth and propagation of Acidithiobacillus ferrooxidans in an unsaturated bed of crushed and agglomerated low grade chalcopyrite ore. The relative distribution of the microorganisms in the flowing leachate solution ('PLS'), the stagnant interstitial liquid and weakly and strongly attached to the mineral surfaces was determined at various time points during the leach. There was a distinct difference in population dynamics in each of these discrete phases. The microbial cells present in the interstitial phase dominated the microbial population in the ore bed. Particularly, the microbial concentration in the free flowing PLS was found to be a poor representation of the ore-associated microbial population. The calculated growth rate of At. ferrooxidans in the PLS was unreasonably high when modelled as a continuous system, indicating that change in cell concentration in the PLS was dominated by transfer from the mineral ore associated population. However, the transfer rate was not correlated directly to changes in either the interstitial or attached population sizes. Therefore, unless transfer rates can be accounted for, PLS population dynamics do not accurately represent those in the column as a whole. Growth rates of microorganisms in the interstitial, weakly mineral-attached and strongly mineral-attached phases better predicted growth of At. ferrooxidans on the whole ore system owing to the dominance of the microbial location in these phases.