Geographic variation in the damselfish-red alga cultivation mutualism in the Indo-West Pacific

Abstract

Abstract Background On coral reefs, damselfish defend their territories from invading herbivores and maintain algal turfs, from which they harvest filamentous algae. In southern Japan, intensive weeding of indigestible algae by Stegastes nigricans results in overgrowth by one filamentous alga, Polysiphonia sp. 1. Because this alga is highly susceptible to grazing and is competitively inferior to other algae, it survives only within the protective territories of this fish species, suggesting an obligate mutualism between damselfish and their cultivated alga. The wide distribution of damselfish species through the Indo-Central Pacific raises the question of whether this species-specific mutualism is maintained throughout the geographic range of the fish. To address this question, from all 18 damselfish species we conducted comprehensive surveys of algal flora within their territories throughout the Indo-West Pacific, and identified species of Polysiphonia using morphological examination and gene sequencing data. Results Several species of the genus Polysiphonia were observed as a major crop in territories throughout the geographic range of S. nigricans. Polysiphonia sp. 1 occurred only in territories of S. nigricans in central areas of the Indo-Pacific. However, its occurrence was low from the Great Barrier Reef and Mauritius. In contrast, other indigenous Polysiphonia species, which formed a clade with Polysiphonia sp. 1, occurred in the territories of fishes from Egypt, Kenya, and the Maldives. The other Polysiphonia species in the clade only inhabited damselfish territories and were never found elsewhere. Conclusions Cultivation mutualism between the damselfish S. nigricans and algae of Polysiphonia was maintained throughout the Indo-West Pacific, although algal crop species and the mode of cultivation (e.g., presence/absence of selective weeding, the species composition of algal turfs) varied among localities. This finding implies that damselfish utilize indigenous Polysiphonia species in newly colonized habitats in different ways, and therefore the algal composition and means of cultivation have diverged.