Climate change promotes parasitism in a coral symbiosis

Abstract

Coastal oceans are increasingly eutrophic, warm and acidic through the addition of anthropogenic nitrogen and carbon, respectively. Among the most sensitive taxa to these changes are scleractinian corals, which engineer the most biodiverse ecosystems on Earth. Corals' sensitivity is a consequence of their evolutionary investment in symbiosis with the dinoflagellate alga, Symbiodinium. Together, the coral holobiont has dominated oligotrophic tropical marine habitats. However, warming destabilizes this association and reduces coral fitness. It has been theorized that, when reefs become warm and eutrophic, mutualistic Symbiodinium sequester more resources for their own growth, thus parasitizing their hosts of nutrition. Here, we tested the hypothesis that sub-bleaching temperature and excess nitrogen promotes symbiont parasitism by measuring respiration (costs) and the assimilation and translocation of both carbon (energy) and nitrogen (growth; both benefits) within Orbicella faveolata hosting one of two Symbiodinium phylotypes using a dual stable isotope tracer incubation at ambient (26 °C) and sub-bleaching (31 °C) temperatures under elevated nitrate. Warming to 31 °C reduced holobiont net primary productivity (NPP) by 60% due to increased respiration which decreased host %carbon by 15% with no apparent cost to the symbiont. Concurrently, Symbiodinium carbon and nitrogen assimilation increased by 14 and 32%, respectively while increasing their mitotic index by 15%, whereas hosts did not gain a proportional increase in translocated photosynthates. We conclude that the disparity in benefits and costs to both partners is evidence of symbiont parasitism in the coral symbiosis and has major implications for the resilience of coral reefs under threat of global change.

Fig. 1

Atom %¹³C (a, b) and %¹⁵N enrichment (c, d) of Orbicella faveolata (right) and their Symbiodinium (left) after a 10 h pulse of ¹⁵NO₃⁻ and H¹³CO₃⁻ following a 10-day incubation at ambient (26 °C) and elevated (31 °C) temperature. Points represent the mean +/− standard error of 10 replicate samples collected from the shallow (1 m; dominated by ITS2 phylotype A3) and deep (15 m; dominated by ITS2 phylotype C7) fore-reef at Carrie Bow Cay, Belize. Initial samples reflect the natural abundance isotope composition prior to tracer incubation. * indicates a significant difference between the temperature treatments within a depth fraction. ‡ indicates a significant difference between shallow and deep samples

Fig. 2

The mean difference between atom % enrichment of carbon (a, b) and nitrogen (c, d) observed between Symbiodinium and their Orbicella faveolata hosts after 10 h exposure to H¹³CO₃⁻ and ¹⁵NO₃⁻ and following a 10 day incubation at ambient (26 °C) and elevated (31 °C) temperature. Points represent the mean +/− standard error of 10 replicate samples collected from the shallow (1 m; dominated by ITS2 phylotype A3) and deep (15 m; dominated by ITS2 phylotype C7) fore-reef at Carrie Bow Cay, Belize pooled from 2 replicated experiments. * indicates a significant difference between the temperature treatments as determined by Student’s t test

Fig. 3

Hypothetical growth curves of Symbiodinium density based on initial cell densities and final mitotic index (MI) values following 10 days of incubation at elevated temperature and nutrients, for corals adapted to the deep and shallow forereef environment. The ‘high symbiont burden’ threshold is derived from Kemp et al. [38]. For model equations and assumptions, please refer to Supplemental Materials.