Benjamin Mueller

Sponges are important ecological and functional components of coral reefs. Recently, a new hypothesis about the functional ecology of sponges in organic matter recycling pathways, the sponge-loop hypothesis, in which dissolved and particulate organic matter is taken up by sponges and shunted to higher trophic levels as detritus, has been proposed and demonstrated for shallow (< 30 m) cryptic species. However, support for this hypothesis at mesophotic depths (∼ 30–150 m) is lacking. Here, we examined detritus production, a prerequisite of the sponge loop pathway, in a reciprocal transplant experiment, using Halisarca caerulea from water depths of 10 and 50 m. Detritus production was significantly lower in mesophotic sponges compared to shallow samples of H. caerulea. Additionally, detritus production rates in transplanted sponges moved in the direction of rates observed for resident conspecifics. The microbiome of these sponge populations was also significantly different between shallow and mesophotic depths, and the microbial communities of the transplanted sponges also shifted in the direction of their new depth in 10 d largely driven by changes in Oxyphotobacteria, Acidimicrobiia, Nitrososphaeria, Nitrospira, Deltaproteobacteria, and Dadabacteriia. This occurred in an environment where the availability of both dissolved and particulate trophic resources changed significantly across the shallow to mesophotic depth gradient where these sponge populations were found. These results suggest that changes in sponge detritus production are primarily driven by differential quality and quantity of trophic resources, as well as their utilization by the sponge host, and its microbiome, along the shallow to mesophotic depth gradient.

Corals have built reefs on the benthos for millennia, becoming an essential element in marine ecosystems. Climate change and human impact, however, are favoring the invasion of non-calcifying benthic algae and reducing coral coverage. Corals rely on energy derived from photosynthesis and heterotrophic feeding, which depends on their surface area, to defend their outer perimeter. But the relation between geometric properties of corals and the outcome of competitive coral-algal interactions is not well known. To address this, 50 coral colonies interacting with algae were sampled in the Caribbean island of Curaçao. 3D and 2D digital models of corals were reconstructed to measure their surface area, perimeter, and polyp sizes. A box counting algorithm was applied to calculate their fractal dimension. The perimeter and surface dimensions were statistically non-fractal, but differences in the mean surface fractal dimension captured relevant features in the structure of corals. The mean fractal dimension and surface area were negatively correlated with the percentage of losing perimeter and positively correlated with the percentage of winning perimeter. The combination of coral perimeter, mean surface fractal dimension, and coral species explained 19% of the variability of losing regions, while the surface area, perimeter, and perimeter-to-surface area ratio explained 27% of the variability of winning regions. Corals with surface fractal dimensions smaller than two and small perimeters displayed the highest percentage of losing perimeter, while corals with large surface areas and low perimeter-to-surface ratios displayed the largest percentage of winning perimeter. This study confirms the importance of fractal surface dimension, surface area, and perimeter of corals in coral-algal interactions. In combination with non-geometrical measurements such as microbial composition, this approach could facilitate environmental conservation and restoration efforts on coral reefs.

One mechanism giving fleshy algae a competitive advantage over corals during reef degradation is algal-induced and microbially-mediated hypoxia (typically less than 69.5 µmol oxygen L⁻¹). During hypoxic conditions oxygen availability becomes insufficient to sustain aerobic respiration in most metazoans. Algae are more tolerant of low oxygen conditions and may outcompete corals weakened by hypoxia. A key question on the ecological importance of this mechanism remains unanswered: How extensive are local hypoxic zones in highly turbulent aquatic environments, continuously flushed by currents and wave surge? To better understand the concert of biological, chemical, and physical factors that determine the abundance and distribution of oxygen in this environment, we combined 3D imagery, flow measurements, macro- and micro-organismal abundance estimates, and experimentally determined biogenic oxygen and carbon fluxes as input values for a 3D bio-physical model. The model was first developed and verified for controlled flume experiments containing coral and algal colonies in direct interaction. We then developed a three-dimensional numerical model of an existing coral reef plot off the coast of Curaçao where oxygen concentrations for comparison were collected in a small-scale grid using fiberoptic oxygen optodes. Oxygen distribution patterns given by the model were a good predictor for in situ concentrations and indicate widespread localized differences exceeding 50 µmol L^-1 over distances less than a decimeter. This suggests that small-scale hypoxic zones can persist for an extended period of time in the turbulent environment of a wave- and surge- exposed coral reef. This work highlights how the combination of three-dimensional imagery, biogenic fluxes, and fluid dynamic modeling can provide a powerful tool to illustrate and predict the distribution of analytes (e.g., oxygen or other bioactive substances) in a highly complex system.

Abstract

A paramount challenge in coral reef ecology is to estimate the abundance and composition of the communities residing in such complex ecosystems. Traditional 2D projected surface cover estimates neglect the 3D structure of reefs and reef organisms, overlook communities residing in cryptic reef habitats (e.g., overhangs, cavities), and thus may fail to represent biomass estimates needed to assess trophic ecology and reef function. Here, we surveyed the 3D surface cover, biovolume, and biomass (i.e., ash-free dry weight) of all major benthic taxa on 12 coral reef stations on the island of Curaçao (Southern Caribbean) using structure-from-motion photogrammetry, coral point counts, in situ measurements, and elemental analysis. We then compared our 3D benthic community estimates to corresponding estimates of traditional 2D projected surface cover to explore the differences in benthic community composition using different metrics. Overall, 2D cover was dominated (52 ± 2%, mean ± SE) by non-calcifying phototrophs (macroalgae, turf algae, benthic cyanobacterial mats), but their contribution to total reef biomass was minor (3.2 ± 0.6%). In contrast, coral cover (32 ± 2%) more closely resembled coral biomass (27 ± 6%). The relative contribution of erect organisms, such as gorgonians and massive sponges, to 2D cover was twofold and 11-fold lower, respectively, than their contribution to reef biomass. Cryptic surface area (3.3 ± 0.2 m2 m−2planar reef) comprised half of the total reef substrate, rendering two thirds of coralline algae and almost all encrusting sponges (99.8%) undetected in traditional assessments. Yet, encrusting sponges dominated reef biomass (35 ± 18%). Based on our quantification of exposed and cryptic reef communities using different metrics, we suggest adjustments to current monitoring approaches and highlight ramifications for evaluating the ecological contributions of different taxa to overall reef function. To this end, our metric conversions can complement other benthic assessments to generate non-invasive estimates of the biovolume, biomass, and elemental composition (i.e., standing stocks of organic carbon and nitrogen) of Caribbean coral reef communities.

Abstract

Reef-building corals are ecosystem engineers that compete with other benthic organisms for space and resources. Corals harvest energy through their surface by photosynthesis and heterotrophic feeding, and they divert part of this energy to defend their outer colony perimeter against competitors. Here, we hypothesized that corals with a larger space-filling surface and smaller perimeters increase energy gain while reducing the exposure to competitors. This predicted an association between these two geometric properties of corals and the competitive outcome against other benthic organisms. To test the prediction, fifty coral colonies from the Caribbean island of Curaçao were rendered using digital 3D and 2D reconstructions. The surface areas, perimeters, box-counting dimensions (as a proxy of surface and perimeter space-filling), and other geometric properties were extracted and analyzed with respect to the percentage of the perimeter losing or winning against competitors based on the coral tissue apparent growth or damage. The increase in surface space-filling dimension was the only significant single indicator of coral winning outcomes, but the combination of surface space-filling dimension with perimeter length increased the statistical prediction of coral competition outcomes. Corals with larger surface space-filling dimensions (Ds > 2) and smaller perimeters displayed more winning outcomes, confirming the initial hypothesis. We propose that the space-filling property of coral surfaces complemented with other proxies of coral competitiveness, such as life history traits, will provide a more accurate quantitative characterization of coral competition outcomes on coral reefs. This framework also applies to other organisms or ecological systems that rely on complex surfaces to obtain energy for competition.