Benjamin Mueller

Natural diet of coral-excavating sponges consists mainly of dissolved organic carbon (DOC).

Coral-excavating sponges are the most important bioeroders on Caribbean reefs and increase in abundance throughout the region. This increase is commonly attributed to a concomitant increase in food availability due to eutrophication and pollution. We therefore investigated the uptake of organic matter by the two coral-excavating sponges Siphonodictyon sp. and Cliona delitrix and tested whether they are capable of consuming dissolved organic carbon (DOC) as part of their diet. A device for simultaneous sampling of water inhaled and exhaled by the sponges was used to directly measure the removal of DOC and bacteria in situ. During a single passage through their filtration system 14% and 13% respectively of the total organic carbon (TOC) in the inhaled water was removed by the sponges. 82% (Siphonodictyon sp.; mean±SD; 13±17 μmol L−1) and 76% (C. delitrix; 10±12 μmol L−1) of the carbon removed was taken up in form of DOC, whereas the remainder was taken up in the form of particulate organic carbon (POC; bacteria and phytoplankton) despite high bacteria retention efficiency (72±15% and 87±10%). Siphonodictyon sp. and C. delitrix removed DOC at a rate of 461±773 and 354±562 μmol C h−1 respectively. Bacteria removal was 1.8±0.9×1010 and 1.7±0.6×1010 cells h−1, which equals a carbon uptake of 46.0±21.2 and 42.5±14.0 μmol C h−1 respectively. Therefore, DOC represents 83 and 81% of the TOC taken up by Siphonodictyon sp. and C. delitrix per hour. These findings suggest that similar to various reef sponges coral-excavating sponges also mainly rely on DOC to meet their carbon demand. We hypothesize that excavating sponges may also benefit from an increasing production of more labile algal-derived DOC (as compared to coral-derived DOC) on reefs as a result of the ongoing coral-algal phase shift.

High dissolved organic carbon release by benthic cyanobacterial mats in a Caribbean reef ecosystem

Benthic cyanobacterial mats (BCMs) are increasing in abundance on coral reefs worldwide. However, their impacts on biogeochemical cycling in the surrounding water and sediment are virtually unknown. By measuring chemical fluxes in benthic chambers placed over sediment covered by BCMs and sediment with BCMs removed on coral reefs in Curaçao, Southern Caribbean, we found that sediment covered by BCMs released 1.4 and 3.5 mmol C m−2 h−1 of dissolved organic carbon (DOC) during day and night, respectively. Conversely, sediment with BCMs removed took up DOC, with day and night uptake rates of 0.9 and 0.6 mmol C m−2 h−1. DOC release by BCMs was higher than reported rates for benthic algae (turf and macroalgae) and was estimated to represent 79% of the total DOC released over a 24 h diel cycle at our study site. The high nocturnal release of DOC by BCMs is most likely the result of anaerobic metabolism and degradation processes, as shown by high respiration rates at the mat surface during nighttime. We conclude that BCMs are significant sources of DOC. Their increased abundance on coral reefs will lead to increased DOC release into the water column, which is likely to have negative implications for reef health.

Effect of light and nutrient availability on the release of dissolved organic carbon (DOC) by Caribbean turf algae

Turf algae increasingly dominate benthic communities on coral reefs. Given their abundance and high dissolved organic carbon (DOC) release rates, turf algae are considered important contributors to the DOC pool on modern reefs. The release of photosynthetically fixed carbon as DOC generally, but not always, increases with increased light availability. Nutrient availability was proposed as an additional factor to explain these conflicting observations. To address this proposed but untested hypothesis, we documented the interactive contributions of light and nutrient availability on the release of DOC by turf algae. DOC release rates and oxygen production were quantified in incubation experiments at two light levels (full and reduced light) and two nutrient treatments (natural seawater and enriched seawater). In natural seawater, DOC release at full light was four times higher than at reduced light. When nutrients were added, DOC release rates at both light levels were similar to the natural seawater treatment at full light. Our results therefore show that low light in combination with low nutrient availability reduces the release of DOC by turf algae and that light and nutrient availability interactively determine DOC release rates by this important component of Caribbean reef communities.

Biofouling of inlet pipes affects water quality in running seawater aquaria and compromises sponge cell proliferation.

Marine organism are often kept, cultured, and experimented on in running seawater aquaria. However, surprisingly little attention is given to the nutrient composition of the water flowing through these systems, which is generally assumed to equal in situ conditions, but may change due to the presence of biofouling organisms. Significantly lower bacterial abundances and higher inorganic nitrogen species (nitrate, nitrite, and ammonium) were measured in aquarium water when biofouling organisms were present within a 7-year old inlet pipe feeding a tropical reef running seawater aquaria system, compared with aquarium water fed by a new, biofouling-free inlet pipe. These water quality changes are indicative of the feeding activity and waste production of the suspension- and filter-feeding communities found in the old pipe, which included sponges, bivalves, barnacles, and ascidians. To illustrate the physiological consequences of these water quality changes on a model organism kept in the aquaria system, we investigated the influence of the presence and absence of the biofouling community on the functioning of the filter-feeding sponge Halisarca caerulea, by determining its choanocyte (filter cell) proliferation rates. We found a 34% increase in choanocyte proliferation rates following the replacement of the inlet pipe (i.e., removal of the biofouling community). This indicates that the physiological functioning of the sponge was compromised due to suboptimal food conditions within the aquarium resulting from the presence of the biofouling organisms in the inlet pipe. This study has implications for the husbandry and performance of experiments with marine organisms in running seawater aquaria systems. Inlet pipes should be checked regularly, and replaced if necessary, in order to avoid excessive biofouling and to approach in situ water quality.

Size at maturation, sex differences, and pair density during the mating season of the Indo-Pacific beach star Archaster typicus (Echinodermata: Asteroidea) in the Philippines

Mating of the relatively common sea star, Archaster typicus, provides an excellent opportunity to study maturation processes and behavioral differences between males and females, since monomorphism does not allow separation under normal conditions. The present study determined biological and behavioral features of males and females during the mating season in the Davao Gulf (Philippines). Thousands of pairs were observed in September and October 2008 with a mean density of 3 pairs m−2. Around full moon, mean density reached 7 pairs m−2, whereas during new moon very few pairs were found. Specimens reached maturity at a radius (R) of 29 mm, while mating specimens had a mean R of 35 mm. Two-thirds of the population were adults and about 35% participated in mating during each observation. Mean R of mating adults was constant throughout the mating season, but within pairs, males were significantly larger in September than in October. The locomotion rate increased with R from 40 to 60 cm min−1 and there was no significant difference between males and females. The role of the lunar cycle as a trigger for reproduction and the significance of large males mating before small males are discussed.

Caribbean free-living coral species co-occurring deep off the windward coast of Curaçao

We document the co-occurrence of two Caribbean species of free-living zooxanthellate corals, Meandrina danae (Milne-Edwards and Haime 1848) (Fig. 1a) and Manicina areolata (Linnaeus 1758) (Fig. 1b), in a previously not well-documented environment. The two species were encountered at three locations (ranging from 30 to 50 m depth) on the windward side of the island of Curaçao, southern Caribbean. Corals are present beyond the reef base on substrate consisting of coarse coral sand, small rubble, and fragments of shells and calcareous algae (Fig. 1c). Colony sizes (mean length) were 58 mm (SD 18, n = 133) for M. areolata and 67 mm (SD 19, n = 32) for M. danae. Maximum colony density of both species together was 30 individuals per m 2 with M. areolata colonies being 9 times as abundant. None of these species has been reported from such a deep habitat. M. danae has never previously been recorded on the island while M. areolata has been described in shallow sandy areas in Curaçao by Roos (1971). It was reported in seagrass beds and on sandy and rubble areas on the reef down to 20 m in Jamaica (Goreau and Goreau 1960) and in seagrass flats and mangrove-associated communities in the San Blas Archipelago, northern Panama (Johnson 1992). Furthermore, free-living scleractinian corals can form dense and species-rich assemblages on sandy habitats of Indo-Pacific reef systems (Hoeksema 2012). To our knowledge, this is the first documented multi-species assemblage of free-living zooxanthellate corals in the Caribbean.

Relevance of coral geometry in the outcomes of the coral-algal benthic war

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.

Spatio–temporal variation in stable isotope signatures (δ 13 C and δ 15 N) of sponges on the Saba Bank

Sponges are ubiquitous on coral reefs, mostly long lived and therefore adaptive to changing environmental conditions. They feed on organic matter withdrawn from the passing water and they may harbor microorganisms (endosymbionts), which contribute to their nutrition. Their diets and stable isotope (SI) fractionation determine the SI signature of the sponge holobiont. Little is known of spatio–temporal variations in SI signatures of δ13C and δ15N in tropical sponges and whether they reflect variations in the environment. We investigated the SI signatures of seven common sponge species with different functional traits and their potential food sources between 15 and 32 m depth along the S-SE and E-NE side of the Saba Bank, Eastern Caribbean, in October 2011 and October 2013. SI signatures differed significantly between most sponge species, both in mean values and in variation, indicating different food preferences and/or fractionation, inferring sponge species-specific isotopic niche spaces. In 2011, all sponge species at the S-SE side were enriched in d13C compared to the E-NE side. In 2013, SI signatures of sponges did not differ between the two sides and were overall lighter in δ13C and δ15N than in 2011. Observed spatio–temporal changes in SI in sponges could not be attributed to changes in the SI signatures of their potential food sources, which remained stable with different SI signatures of pelagic (particulate organic matter (POM): δ13C −24.9‰, δ15N +4.3‰) and benthic-derived food (macroalgae: δ13C −15.4‰, δ15N +0.8‰). Enriched δ13C signatures in sponges at the S-SE side in 2011 are proposed to be attributed to predominantly feeding on benthic-derived C. This interpretation was supported by significant differences in water mass constituents between sides in October 2011. Elevated NO3 and dissolved organic matter concentrations point toward a stronger reef signal in reef overlying water at the S-SE than N-NE side of the Bank in 2011. The depletions of δ13C and δ15N in sponges in October 2013 compared to October 2011 concurred with significantly elevated POM concentrations. The contemporaneous decrease in δ15N suggests that sponges obtain their N mostly from benthic-derived food with a lower δ15N than pelagic food. Average proportional feeding on available sources varied between sponge species and ranged from 20% to 50% for benthic and 50% to 80% for pelagic-derived food, assuming trophic enrichment factors of 0.5‰ ± sd 0.5 for δ13C and 3‰ ± sd 0.5 for δ15N for sponges. We suggest that observed variation of SI in sponges between sides and years were the result of shifts in the proportion of ingested benthic- and pelagic-derived organic matter driven by environmental changes. We show that sponge SI signatures reflect environmental variability in space and time on the Saba Bank and that SI of sponges irrespective of their species-specific traits move in a similar direction in response to these environmental changes.

DOC concentrations across a depth-dependent light gradient on a Caribbean coral reef

Photosynthates released by benthic primary producers (BPP), such as reef algae and scleractinian corals, fuel the dissolved organic carbon (DOC) production on tropical coral reefs. DOC concentrations near BPP have repeatedly been observed to be elevated compared to those in the surrounding water column. As the DOC release of BPP increases with increasing light availability, elevated DOC concentrations near them will, in part, also depend on light availability. Consequently, DOC concentrations are likely to be higher on the shallow, well-lit reef terrace than in deeper sections on the fore reef slope. We measured in situ DOC concentrations and light intensity in close proximity to the reef alga Dictyota sp. and the scleractinian coral Orbicella faveolata along a depth-dependent light gradient from 5 to 20 m depth and compared these to background concentrations in the water column. At 10 m (intermediate light), DOC concentrations near Dictyota sp. were elevated by 15 µmol C L−1 compared to background concentrations in the water column, but not at 5 and 20 m (high and low light, respectively), or near O. faveolata at any of the tested depths. DOC concentrations did not differ between depths and thereby light environments for any of the tested water types. However, water type and depth appear to jointly affect in situ DOC concentrations across the tested depth-dependent light gradient. Corroborative ex situ measurements of excitation pressure on photosystem II suggest that photoinhibition in Dictyota sp. is likely to occur at light intensities that are commonly present on Curaçaoan coral reefs under high light levels at 5 m depth during midday. Photoinhibition may have thereby reduced the DOC release of Dictyota sp. and DOC concentrations in its close proximity. Our results indicate that the occurrence of elevated DOC concentrations did not follow a natural light gradient across depth. Instead, a combination of multiple factors, such as water type, light availability (including the restriction by photoinhibition), and water movement are proposed to interactively determine the DOC concentrations in the close vicinity of BPP.