Quantifying interconnected performances of the modules in a colonial organism (feeding, sexual reproduction, rejuvenation, dormancy) into an integral picture enables studying functional dynamics and resource allocation at different levels – from module to population. Testing this approach on the common boreal-Arctic bryozoan Cribrilina annulata in the White Sea, we describe its life history, comparing colonies on two algal substrates with contrasting size and lifespan. Colonies living on kelps were much larger and had a higher proportion of dormant zooids, whereas the percentage of reproducing, feeding and rejuvenating zooids was higher in colonies on red algae (with the colonies also exhibiting longer reproductive period). Colony lifespan was dependent both on substrate type and on time of colony establishment, lasting from 4–5 to up to 17 months on kelps and 14–18 months on red algae. During the reproductive season (May–September) the C. annulata population consisted of colonies of three cohorts on both substrata: overwintered and two summer generations that behaved differently. Whereas overwintered and summer colonies established in June–early August produced larvae, most of the colonies established after mid-summer were preparing for hibernation and postponed reproduction until next spring. Moreover, young reproducing colonies formed brooding hermaphrodite zooids of ordinary size, whereas overwintered colonies budded smaller-sized basal and frontal (dwarf) hermaphrodites. Finally, overall zooidal performance in co-existing colonies of the overwintered and young generations was different on kelps, but similar on red algae. Altogether our findings indicate that the life histories of colonial epibionts are much more complex and evolutionarily flexible than generally acknowledged.