The oxygen dynamics and pumping behavior in Dysidea avara and Chondrosia reniformis (Porifera, Demospongiae) were investigated using oxygen microelectrodes and heated thermistor flow sensors. Both field and laboratory experiments showed the common occurrence of low oxygenation approaching anoxia in both species, lasting up to 1 h. Strong temporal and spatial heterogeneity of oxygen concentrations were observed with replicate oxygen profile series across the sponge surface, though tissue close to an osculum was generally better oxygenated than deeper in the sponge body. Because of observed lag times between a pumping event and the respective oxygenation response, the state of oxygenation of sponge tissue could only be partially attributed to its pumping activity. Ambient flow also influenced oxygenation patterns of sponges. Larger individuals possessing a functional aquiferous system regulated their pumping activity according to the ambient flow regime, whereas a small D. avara sponge, yet to possess its first osculum, was passively oxygenated by ambient flow and became anoxic approximately 30 min after ambient flow was stopped in its laboratory tank. These studies showed (1) sponge tissue metabolism switched frequently from aerobic to anaerobic, (2) temporally and spatially dynamic oxygen-depleted regions were commonly found within those sponges, both in captivity and in the field, and (3) tissue oxygenation was regulated both by active behavior (pumping) and passive environmental events (ambient water flow). We concluded that the metabolism of both sponge cells and sponge microbes will be influenced by the sponges' ability to control oxygen concentrations in different regions of its body at any particular time. In addition, when a sponge is actively pumping in a particular region of its body, higher oxygen concentrations will favor aerobic symbionts and aerobic metabolism, whereas when active pumping ceases, anaerobic symbionts and anaerobic tissue metabolism will be favored.