Farming behaviour of reef fishes increases the prevalence of coral disease associated microbes and the occurrence of black band disease

Background/Question/Methods

Microbial community structure on coral reefs is strongly influenced by coral-algae interactions; however, the extent to which this influence is mediated by fishes is unknown. By excluding fleshy macroalgae, cultivating palatable filamentous algae and engaging in frequent aggression to protect resources, territorial damselfish (f. Pomacentridae) mediate macro-benthic dynamics on coral reefs and may significantly influence microbial communities. Intensive territorial grazers in the genus Stegastes have a particularly large role in benthic systems due to their high abundances, propagation of thick algal turfs and heightened aggressive responses to intruders. Previously, benthic turf algae have been shown to harbour pathogens that are associated with coral disease, yet the microbial communities of damselfish territories are virtually unexplored. To elucidate how Stegastes apicalis and Stegastes nigricans may alter benthic microbial assemblages, we determined the prokaryotic community composition of the epilithic algal matrix (EAM) and Acropora muricata, a common staghorn coral, inside and outside of damselfish territories around Lizard Island, the Great Barrier Reef, Australia. To further determine how territorial grazers may engineer microbial communities, we transplanted nubbins of A. muricata inside and outside of Stegastes’ territories and used 16S sequencing to analyze the microbial assemblages associated with coral fragments over one year.

Results/Conclusions

16S sequencing of the EAM revealed distinct bacterial communities associated with damselfish territories and a two to three times greater relative abundance of phylotypes with high sequence similarity to coral pathogens associated with black band disease inside Stegastes’ territories. The relative abundance of coral disease associated pathogens in transplanted coral nubbins increased both inside and outside Stegastes’ territories, which may be a result of exposure to the EAM rather than a factor of the presence or absence of territorial damselfish. However, black band disease (BBD) surveys showed a significantly higher occurrence (P = 0.035) of BBD in A. muricata outcrops occupied by S. nigricans’ territories as opposed to A. muricata outcrops with territorial damselfish absent. Thus, intensive grazers’ cultivation of thick turfs and exclusion of intruders appears to create a benthic assemblage that harbours microbial genera associated with coral disease, which may be responsible for the higher prevalence of BBD. These findings demonstrate a potential link between fish behaviour, reservoirs of coral disease pathogens and the manifestation of coral disease. If the recently hypothesized positive relationship between fishing pressure and damselfish abundance is valid, a damselfish-pathogen link would have important implications for the management of coral health in reef systems.