A novel obligate cultivation mutualism between damselfish and Polysiphonia algae

Abstract

In cultivation mutualisms, farming animals prepare fields for cultivars, enhance their growth and harvest them. For example, in terrestrial ecosystems, plant-herbivore cultivation mutualisms arose between humans and their crops only relatively recently. We discovered an obligate cultivation mutualism between a damselfish and an alga in a coral reef ecosystem. The damselfish, Stegastes nigricans, manages algal farms through territorial defence against the invading grazers and through weeding of unpalatable algae. As a result, the algal farms of S. nigricans are dominated by one species, Polysiphonia sp. We performed an exhaustive survey of algal assemblages inside and outside the territories of five damselfish species around the Ryukyu Islands, Japan, using molecular and morphological characteristics. Polysiphonia sp. 1 grew exclusively inside the farms of S. nigricans, and never elsewhere. Since only Polysiphonia sp. 1 is harvested and consumed by the damselfish as a staple food, this interdependent relationship is an obligate cultivation mutualism. This is the first record of an obligate plant-herbivore cultivation mutualism in a marine ecosystem. Our data also suggest that three other Polysiphonia species are facultatively mutual with, commensal with, or parasitic on other damselfish species.

Figure 1

Percent occurrence of four Polysiphonia spp. algae inside and outside the territories of the damselfishes (a) Stegastes nigricans, (b) S. lividus, (c) Plectroglyphidodon lacrymatus, (d) Hemiglyphidodon plagiometopon and (e) Dischistodus prosopotaenia. The probability of occurrence of each algal species among these sites was analysed using Fisher's exact test. ^***p<0.001.

Figure 2

Phylogeny of Polysiphonia spp. algae found inside and outside the territories of the damselfishes Stegastes nigricans, S. lividus, Plectroglyphidodon lacrymatus, Hemiglyphidodon plagiometopon and Dischistodus prosopotaenia. The association of each alga is denoted by the abbreviation and colour of its damselfish host species and by collection site. An asterisk denotes the dominance of the alga in samples (representing more than 50% of the biomass). Numbers in parentheses indicate the number of DNA samples. Data for unshaded species denote citations from the NCBI GenBank. The tree was obtained using ML method, with a log-likelihood score of 4971.063. Branches that collapse in MP, ML and/or BI trees are presented as dotted lines. Nodal support is assessed by bootstrap values of MP and posterior probabilities of BI (above branches, MP/BI, respectively). Solid and broken arrows indicate obligate and facultative associations, respectively.