Light responses in Drosophila photoreceptors are mediated by two Ca 2+ permeable cation channels, transient receptor potential (TRP) and TRP-like (TRPL). Although Ca2+ influx via these channels is critical for amplification, inactivation, and light adaptation, the fractional contribution of Ca2+ to the currents (Pf) has not been measured. We describe a slow (τ ∼ 350 ms) tail current in voltage-clamped light responses and show that it is mediated by electrogenic Na+/Ca2+ exchange. Assuming a 3Na:1Ca stoichiometry, we derive empirical estimates of Pf by comparing the charge integrals of the exchanger and light-induced currents. For TRPL channels, Pf was ∼17% as predicted by Goldman-Hodgkin-Katz (GHK) theory. Pf for TRP (29%) and wild-type flies (26%) was higher, but lower than the GHK prediction (45% and 42%). As predicted by GHK theory, Pf for both channels increased with extracellular [Ca2+], and was largely independent of voltage between -100 and -30 mV. A model incorporating intra- and extracellular geometry, ion permeation, diffusion, extrusion, and buffering suggested that the deviation from GHK predictions was largely accounted for by extracellular ionic depletion during the light-induced currents, and the time course of the Na+/Ca2+ exchange current could be used to obtain estimates of cellular Ca2+ buffering capacities.