Intergenerational effects of macroalgae on a reef coral: major declines in larval survival but subtle changes in microbiomes

Abstract

Tropical reefs are shifting from coral to macroalgal dominance, with macroalgae suppressing coral recovery, potentially via effects on coral microbiomes. Understanding how macroalgae affect corals and their microbiomes requires comparing algae- versus coral-dominated reefs without confounding aspects of time and geography. We compared survival, settlement, and post-settlement survival of larvae, as well as the microbiomes of larvae and adults, of the Pacific coral Pocillopora damicornis between an Marine Protected Area (MPA) dominated by corals versus an adjacent fished area dominated by macroalgae. Microbiome composition in adult coral, larval coral, and seawater did not differ between the MPA and fished area. However, microbiomes of adult coral were more variable in the fished area and Vibrionaceae bacteria, including strains most closely related to the pathogen Vibrio shilonii, were significantly enriched, but rare, in adult and larval coral from the fished area. Larvae from the macroalgae-dominated area exhibited higher pre-settlement mortality and reduced settlement compared to those from the coral-dominated area. Juveniles planted into a coral-dominated area survived better than those placed into a fished area dominated by macroalgae. Differential survival depended on whether macroalgae were immediately adjacent to juvenile coral rather than on traits of the areas per se. Contrary to our expectations, coral microbiomes were relatively uniform at the community level despite dramatic differences in macroalgal cover between the MPA (~2% cover) and fished (~90%) area. Reducing macroalgae may elicit declines in rare but potentially harmful microbes in coral and their larvae, as well as positive intergenerational effects on offspring survival.

Keywords: Pocillopora damicornis; coral larvae; coral microbiome; coral-algae interactions; marine protected areas.

Figure 1

A) PCO and PERMANOVA analysis of Bray Curtis dissimilarity matrix of coral larvae, coral adults, and water microbiomes from the MPA and fished area. B) Diversity of OTUs in coral and water samples. C) Shannon Diversity Index for coral and water samples. OTUs and Shannon Diversity were analyzed by a two-factor ANOVA with Tukey post-hoc analysis. D) Taxonomic groups that contribute to 2% or greater of the microbial community composition of coral adults, coral larvae, and water are depicted at the level of family with the exception of Chromatiales (order). Low abundance taxa, contributing less than 2% of community composition were pooled to generate ‘Low Abundance Bacteria’ and ‘Low Abundance Archaea’ groups. For analyses in A–D above, each coral larva, and coral adult data point represents the mean community composition for a single replicate.

Figure 2

Abundances and two-factor ANOVA analyses of Vibrio shilonii (A) and taxa within the family Vibrionaceae (B) in corals (adults and larvae) from the MPA and fished area.

Figure 3

A) Survival and two-factor ANOVA analysis of larvae (mean ± SE) from the MPA and fished area maintained in MPA or fished area water for six days (n = 10 per level of each factor). Letters above bars indicate significant groupings by Tukey HSD post-hoc analysis. B) PCO and PERMANOVA analysis of Bray Curtis dissimilarity matrix of microbiomes from surviving larvae from the MPA or fished area maintained in MPA or fished area water for six days. C) PCO and PERMANOVA analysis of Bray Curtis dissimilarity matrix of water microbiomes from the MPA and fished area, used to maintain larvae in the lab from the MPA or fished area for six days.

Figure 4

A) Settlement (mean ± SE) of MPA and fished area larvae on rubble from the MPA without macroalgae and from the fished area with macroalgae at 24 and 48 h (n = 20 per level of each factor; absolute percentages provided). See Table 1A for statistical analyses of repeated measures ANOVA on square root transformed proportion data. B) Survival (mean ± SE) of newly settled MPA and fished area juvenile corals on MPA versus fished area substrates that were out-planted to their corresponding reef (MPA rubble planted in the MPA and fished area rubble planted in the fished area) when corals were four and 26 days old (n = 13 – 18 per level of each factor due to loss of zip-tied rubble on the reef over time). See Table 1B for statistical analyses of repeated measures ANOVA on proportion data.

Figure 5

A) Percent settlement (mean ± SE) of MPA larvae on rubble from the MPA without macroalgae, the fished area without macroalgae, and the fished area with macroalgae at 24 and 48 hours (n = 15 with the exception of one lost replicate due to sloughing of macroalgae during the settlement experiment; absolute percentages provided). Repeated measures ANOVA was performed on square root transformed proportion data. B) Percent survival (mean ± SE) of newly settled juvenile corals on rubble from the MPA without macroalgae, the fished area without macroalgae, and the fished area with macroalgae that were out-planted to their corresponding reef (MPA rubble planted in the MPA and fished area rubble planted in the fished area) when the juvenile corals were four days old. Repeated measures ANOVA was performed on proportion data (n = 11 – 15 due to loss of replicates planted on the reef over time).