Daily budgets of photosynthetically fixed carbon were constructed for Pteraeolidia ianthina with high and low densities of zooxanthellae, for irradiances typical of latitude 34° S in winter, spring and summer. Whereas nudibranchs with high densities of zooxanthellae were potentially phototrophic with respect to carbon, animals with densities of zooxanthellae less than 0.5 x 10 6 cells mg -1 protein were not. The proportion of dividing zooxanthellae (mitotic index) in P. ianthina was followed over 48 hours. The diel pattern of mitotic index was asynchronous; the indices were higher in animals with low densities of zooxanthellae (20.1±6.2%) than in animals with high densities of zooxanthellae (4.7±1.8%). Specific growth rates of zooxanthellae, calculated from mitotic indices, ranged between 0.100 and 0.399 d -1 , indicating that zooxanthellae in P . ianthina have the potential to grow at rates comparable to those found in free-living and other symbiotic dinoflagellates. Zooxanthellae in the host photosynthesized at similar rates, irrespective of their density in P . ianthina . Because of the greater amount of newly synthesized carbon dedicated to the population growth of zooxanthellae, low-density populations did not have excess organic carbon available for host respiration. High density populations, however, were able to supply 79% of the animal’s respiratory carbon demand in winter, 121% in spring and 173% in summer. These results demonstrate that the metabolic relationship of zooxanthellae and their invertebrate hosts may change during the establishment of a symbiotic association.