Assessing coral reefs on a Pacific-wide scale using the microbialization score

Abstract

The majority of the world's coral reefs are in various stages of decline. While a suite of disturbances (overfishing, eutrophication, and global climate change) have been identified, the mechanism(s) of reef system decline remain elusive. Increased microbial and viral loading with higher percentages of opportunistic and specific microbial pathogens have been identified as potentially unifying features of coral reefs in decline. Due to their relative size and high per cell activity, a small change in microbial biomass may signal a large reallocation of available energy in an ecosystem; that is the microbialization of the coral reef. Our hypothesis was that human activities alter the energy budget of the reef system, specifically by altering the allocation of metabolic energy between microbes and macrobes. To determine if this is occurring on a regional scale, we calculated the basal metabolic rates for the fish and microbial communities at 99 sites on twenty-nine coral islands throughout the Pacific Ocean using previously established scaling relationships. From these metabolic rate predictions, we derived a new metric for assessing and comparing reef health called the microbialization score. The microbialization score represents the percentage of the combined fish and microbial predicted metabolic rate that is microbial. Our results demonstrate a strong positive correlation between reef microbialization scores and human impact. In contrast, microbialization scores did not significantly correlate with ocean net primary production, local chla concentrations, or the combined metabolic rate of the fish and microbial communities. These findings support the hypothesis that human activities are shifting energy to the microbes, at the expense of the macrobes. Regardless of oceanographic context, the microbialization score is a powerful metric for assessing the level of human impact a reef system is experiencing.

Figure 1. Location of the 29 islands surveyed.

Color scale indicates oceanic net primary production derived from satellite data using the Vertically Generalized Production Model (VGPM). Circles indicate the relative NCEAS cumulative human impact score for each island. For island abbreviations see Table 1.

Figure 2. Linear regression analysis of microbialization scores versus NCEAS cumulative human impact values (y = 8.19 x – 26.10; r² = 0.68).

The microbialization score is the percentage of the combined fish and microbial predicted metabolic rate that is microbial. Color denotes oceanographic region: Guam and the Mariana Islands (orange circles), the Main Hawaiian Islands (blue circles), Pacific Remote Islands and Atolls (pink circles), and the Samoa region (green circles). For island abbreviations see Table 1.

Figure 3. Microbialization scores plotted against the combined fish + microbes predicted metabolic rates for each of the 29 islands surveyed.

Colors are as in Fig. 2. For island abbreviations see Table 1.

Figure 4. Measures of energy use versus metrics of primary production.

(a) Non-linear regression analysis of the combined fish + microbes predicted metabolic rate versus net primary production (NPP) for the 29 surveyed islands. NPP was derived from satellite data using the Vertically Generalized Production Model (VGPM). (y = 0.00008x+0.0012; R² = 0.21) (b) Non-linear regression analysis of the combined fish + microbes predicted metabolic rate versus nearshore chla concentrations at the 29 surveyed islands (y = 0.54x+0.01; R² = 0.08) (c) Microbialization scores versus NPP derived from satellite data using the VGPM for the 29 surveyed islands. (d) Microbialization scores versus nearshore chla concentrations at the 29 surveyed islands (y = 171.5x+29.7; R² = 0.22). Colors are as in Fig. 2. For island abbreviations see Table 1.