Effects of coral reef benthic primary producers on dissolved organic carbon and microbial activity

Abstract

Benthic primary producers in marine ecosystems may significantly alter biogeochemical cycling and microbial processes in their surrounding environment. To examine these interactions, we studied dissolved organic matter release by dominant benthic taxa and subsequent microbial remineralization in the lagoonal reefs of Moorea, French Polynesia. Rates of photosynthesis, respiration, and dissolved organic carbon (DOC) release were assessed for several common benthic reef organisms from the backreef habitat. We assessed microbial community response to dissolved exudates of each benthic producer by measuring bacterioplankton growth, respiration, and DOC drawdown in two-day dark dilution culture incubations. Experiments were conducted for six benthic producers: three species of macroalgae (each representing a different algal phylum: Turbinaria ornata--Ochrophyta; Amansia rhodantha--Rhodophyta; Halimeda opuntia--Chlorophyta), a mixed assemblage of turf algae, a species of crustose coralline algae (Hydrolithon reinboldii) and a dominant hermatypic coral (Porites lobata). Our results show that all five types of algae, but not the coral, exuded significant amounts of labile DOC into their surrounding environment. In general, primary producers with the highest rates of photosynthesis released the most DOC and yielded the greatest bacterioplankton growth; turf algae produced nearly twice as much DOC per unit surface area than the other benthic producers (14.0±2.8 µmol h⁻¹ dm⁻²), stimulating rapid bacterioplankton growth (0.044±0.002 log10 cells h⁻¹) and concomitant oxygen drawdown (0.16±0.05 µmol L⁻¹ h⁻¹ dm⁻²). Our results demonstrate that benthic reef algae can release a significant fraction of their photosynthetically-fixed carbon as DOC, these release rates vary by species, and this DOC is available to and consumed by reef associated microbes. These data provide compelling evidence that benthic primary producers differentially influence reef microbial dynamics and biogeochemical parameters (i.e., DOC and oxygen availability, bacterial abundance and metabolism) in coral reef communities.

Figure 1. Experimental setup.

Primary producers were incubated in filtered backreef seawater in replicates of a minimum of five for each species. Following the 8.5 h daylight DOC release incubations specimen were removed and reference parameters were determined and unfiltered backreef seawater was amended to add a representative microbial community for subsequent dark incubations (48 h) of the exudates. Thick arrows indicate measurements of respective parameters. Abbreviations: PP = primary producer, ED = exudate dilution, TOC = total organic carbon, Bac = bacterial cell abundance.

Figure 2. Rates of DOC production and DO production and consumption, normalized to surface area of benthic primary producers.

Bars are means with standard error whiskers. Panels with grey background shading are dark incubations. A) Rates of DOC production during 8 h daylight incubation and B) oxygen production and consumption over a 24 hour light/dark cycle; treatments with the same letter are not significantly different at α = 0.05.

Figure 3. Relationships between oxygen and DOC release in Light incubations.

Panel A relates absolute rates of oxygen and carbon production in light incubations, with line representing constant ratio of release for reference. Panel B shows variation in ratios of oxygen and DOC production among the six treatments; treatments with the same letter are not significantly different at α = 0.05. Quantile box plots in Panel B (whiskers extend to 95% quantiles) are overlaid with raw replicate data points from each treatment color/symbol coded according to the legend in panel (A).

Figure 4. Quantiles of bacterioplankton growth and oxygen consumption in dilution culture incubations on different exudates.

Panels show rates of bacterial oxygen consumption (A), bacterial cell yield (B), and bacterial specific growth rate (C). Quantile box plots (whiskers extend to 95% quantiles) are overlaid with raw replicate data points from each treatment color/symbol coded according to the legend in panel (A) and Fig. 3; treatments with the same letter are not significantly different at α = 0.05. Note that there were no significant differences among treatments in specific growth rate.

Figure 5. Rates of A.) bacterial carbon yield and B.) DO consumption on exudates over ∼48 hour dilution culture incubations normalized to surface area of previously incubated primary producers.

Bars are means with standard error whiskers; treatments with the same letter are not significantly different at α = 0.05.

Figure 6. The predicted DOC release (red squares) and bacterial yield (blue circles) for varying coral reef benthic assemblages.

The six benthic species characterized in this study were separated into four functional groups: turf algae, macroalgae (Amansia rhodantha and Turbinaria ornata), calcifying algae (Halimeda opuntia and Hydrolithon reinboldii (CCA)), and hermatypic coral (Porites lobata). Different combinations of percent cover for the four benthic functional groups were calculated (N = 102), the bar charts represent eight examples of the possible benthic assemblages. The measurements for benthic cover from two of the Line Islands (Kingman and Kiritimati) and Moorea were taken from Sandin et al, 2008 and the LTER database (knb-lter-mcr.8, http://mcr.lternet.edu/data), respectively.