Photoreceptor currents of the multicellular green alga Volvox carteri were analyzed using a dissolver mutant. The photocurrents are restricted to the eyespot region of somatic cells. Photocurrents are detectable from intact cells and excised eyes. The rhodopsin action spectrum suggests that the currents are induced by Volvox rhodopsin. Flash-induced photocurrents are a composition of a fast Ca2+-carried current (PF) and a slower current (PS), which is carried by H+. PF is a high-intensity response that appears with a delay of less than 50 micros after flash. The stimulus-response curve of its initial rise is fit by a single exponential and parallels the rhodopsin bleaching. These two observations suggest that the responsible channel is closely connected to the rhodopsin, both forming a tight complex. At low flash energies PS is dominating. The current delay increases up to 10 ms, and the PS amplitude saturates when only a few percent of the rhodopsin is bleached. The data are in favor of a second signaling system, which includes a signal transducer mediating between rhodopsin and the channel. We present a model of how different modes of signal transduction are accomplished in this alga under different light conditions.