Variation in susceptibility among three Caribbean coral species and their algal symbionts indicates the threatened staghorn coral, Acropora cervicornis, is particularly susceptible to elevated nutrients and heat stress

Abstract

Coral cover is declining worldwide due to multiple interacting threats. We compared the effects of elevated nutrients and temperature on three Caribbean corals: Acropora cervicornis, Orbicella faveolata, and Siderastrea siderea. Colonies hosting different algal symbionts were exposed to either ambient nutrients (A), elevated NH 4 (N), or elevated NH 4 ? PO 4 (N ? P) at control temperatures (26 °C) for [ 2 months, followed by a 3-week thermal challenge (31.5 °C). A. cervicornis hosted Symbiodinium (S. fitti) and was highly susceptible to the combination of elevated nutrients and temperature. During heat stress, A. cervicornis pre-exposed to elevated nutrients experienced 84%-100% mortality and photochemical efficiency (F v / F m ) declines of 41-50%. In comparison, no mortality and lower F v /F m declines (11-20%) occurred in A. cervicornis that were heat-stressed but not pre-exposed to nutrients. O. faveolata and S. siderea response to heat stress was determined by their algal symbiont community and was not affected by nutrients. O. faveolata predominantly hosted Durusdinium trenchii or Breviolum, but only corals hosting Breviolum were susceptible to heat, experiencing 100% mortality, regardless of nutrient treatment. S. siderea colonies predominantly hosted Cladocopium C1 (C. goreaui), Cladocopium C3, D. trenchii, or variable proportions of Cladocopium C1 and D. trenchii. This species was resilient to elevated nutrients and temperature, with no significant mortality in any of the treatments. However, during heat stress, S. siderea hosting Cladocopium C3 suffered higher reductions in F v /F m (41-56%) compared to S. siderea hosting Cladocopium C1 and D. trenchii (17-26% and 10-16%, respectively). These differences in holobiont susceptibility to elevated nutrients and heat may help explain historical declines in A. cervicornis starting decades earlier than other Caribbean corals. Our results suggest that tackling only warming temperatures may be insufficient to ensure the continued persistence of Caribbean corals, especially A. cervicornis. Reducing nutrient inputs to reefs may also be necessary for these iconic coral species to survive.

Microbiome signatures in Acropora cervicornis are associated with genotypic resistance to elevated nutrients and heat stress

“…In a companion study, we found that A. cervicornis is particularly sensitive to the combined effects of elevated nutrients and temperature (Palacio-Castro et al 2021). Here we investigated genotypic variation in sensitivity by comparing the performance (growth, survivorship, and photochemical efficiency), and prokaryotic community (bacteria and archaea) of six A. cervicornis genotypes that are used in coral restoration in South Florida.…”

“…Thirty-nine fragments were sacrificed during the experiment (28 at the end of phase 1, and 11 at the end of phase 3; Fig. 1) for a companion study (Palacio-Castro et al 2021), and their removal was recorded as "censored" events to adjust the survivorship curves. These events account for the incomplete information about the survivorship outcome of the removed fragments since it is unknown if they would die or survive if left longer in the experiment.…”

“…Nutrients have been also reported to increase disease prevalence (Vega Thurber et al 2013), and disrupt corals' associated microbial communities, altering the cycling of nutrients among the coral host and their symbionts (Rädecker et al 2015) and promoting the proliferation of opportunistic or pathogenic microbes (Vega Thurber et al 2009). However, the effects of nutrient enrichment on corals are not always negative and can vary by coral species (Fox et al 2021;Palacio-Castro et al 2021), nutrient levels (D'Angelo et al 2014;Dobson et al 2021), nutrient source (Burkepile et al 2019), exposure time (Fabricius 2005), and the ratio of nitrogen to phosphorus availability (Ferrier-Pagès et al 2000;Rosset et al 2017).…”

Microbiome signatures inAcropora cervicornisare associated with genotypic resistance to elevated nutrients and heat stress

“…Nutrients have been also reported to increase disease prevalence (Vega Thurber et al 2013), and disrupt corals’ associated microbial communities, altering the cycling of nutrients among the coral host and their symbionts (Rädecker et al 2015) and promoting the proliferation of opportunistic or pathogenic microbes (Vega Thurber et al 2009). However, the effects of nutrient enrichment on corals are not always negative and can vary by coral species (Fox et al 2021; Palacio-Castro et al 2021), nutrient levels (D’Angelo et al 2014; Dobson et al 2021), nutrient source (Burkepile et al 2019), exposure time (Fabricius 2005), and the ratio of nitrogen to phosphorus availability (Ferrier-Pagès et al 2000; Rosset et al 2017).…”

Endosymbiont strategic shifts inhibit cooperation during coral bleaching recovery

“…Corals with these thermotolerant algae are more likely to survive heat stress events (e.g. [23,24]; but see [25]); however, these thermotolerant algae often provide less photosynthate to their hosts under ambient conditions, limiting host growth (e.g. [26][27][28][29][30][31]; but see [32,33]).…”