Coral reefs in transition: Temporal photoquadrat analyses and validation of underwater hyperspectral imaging for resource-efficient monitoring in Guam.

The island of Guam in the west Pacific has seen a significant decrease in coral cover since 2013. Lafac Bay, a marine protected area in northeast Guam, served as a reference site for benthic communities typical of forereefs on the windward side of the island. The staghorn coral Acropora abrotanoides is a dominant and characteristic ecosystem engineer of forereef communities on exposed shorelines. Photoquadrat surveys were conducted in 2015, 2017, and 2019, and a diver-operated hyperspectral imager (i.e., DiveRay) was used to survey the same transects in 2019. Machine learning algorithms were used to develop an automated pipeline to assess the benthic cover of 10 biotic and abiotic categories in 2019 based on hyperspectral imagery. The cover of scleractinian corals did not differ between 2015 and 2017 despite being subjected to a series of environmental disturbances in these years. Surveys in 2019 documented the almost complete decline of the habitat-defining staghorn coral Acropora abrotanoides (a practically complete disappearance from about 10% cover), a significant decrease (~75%) in the cover of other scleractinian corals, and a significant increase (~55%) in the combined cover of bare substrate, turf algae, and cyanobacteria. The drastic change in community composition suggests that the reef at Lafac Bay is transitioning to a turf algae-dominated community. However, the capacity of this reef to recover from previous disturbances suggests that this transition could be reversed, making Lafac Bay an excellent candidate for long-term monitoring. Community analyses showed no significant difference between automatically classified benthic cover estimates derived from the hyperspectral scans in 2019 and those derived from photoquadrats. These findings suggest that underwater hyperspectral imagers can be efficient and effective tools for fast, frequent, and accurate monitoring of dynamic reef communities.

Assessment of the utility of underwater hyperspectral imaging for surveying and monitoring coral reef ecosystems.

Technological innovations that improve the speed, scale, reproducibility, and accuracy of monitoring surveys will allow for a better understanding of the global decline in tropical reef health. The DiveRay, a diver-operated hyperspectral imager, and a complementary machine learning pipeline to automate the analysis of hyperspectral imagery were developed for this purpose. To evaluate the use of a hyperspectral imager underwater, the automated classification of benthic taxa in reef communities was tested. Eight reefs in Guam were surveyed and two approaches for benthic classification were employed: high taxonomic resolution categories and broad benthic categories. The results from the DiveRay surveys were validated against data from concurrently conducted photoquadrat surveys to determine their accuracy and utility as a proxy for reef surveys. The high taxonomic resolution classifications did not reliably predict benthic communities when compared to those obtained by standard photoquadrat analysis. At the level of broad benthic categories, however, the hyperspectral results were comparable to those of the photoquadrat analysis. This was particularly true when estimating scleractinian coral cover, which was accurately predicted for six out of the eight sites. The annotation libraries generated for this study were insufficient to train the model to fully account for the high biodiversity on Guam's reefs. As such, prediction accuracy is expected to improve with additional surveying and image annotation. This study is the first to directly compare the results from underwater hyperspectral scanning with those from traditional photoquadrat survey techniques across multiple sites with two levels of identification resolution and different degrees of certainty. Our findings show that dependent on a well-annotated library, underwater hyperspectral imaging can be used to quickly, repeatedly, and accurately monitor and map dynamic benthic communities on tropical reefs using broad benthic categories.

Nitrogen and phosphorus uptake rates of different species from a coral reef community after a nutrient pulse.

Terrestrial runoff after heavy rainfall can increase nutrient concentrations in waters overlying coral reefs that otherwise experience low nutrient levels. Field measurements during a runoff event showed a sharp increase in nitrate (75-fold), phosphate (31-fold) and ammonium concentrations (3-fold) in waters overlying a fringing reef at the island of Curaçao (Southern Caribbean). To understand how benthic reef organisms make use of such nutrient pulses, we determined ammonium, nitrate and phosphate uptake rates for one abundant coral species, turf algae, six macroalgal and two benthic cyanobacterial species in a series of laboratory experiments. Nutrient uptake rates differed among benthic functional groups. The filamentous macroalga Cladophora spp., turf algae and the benthic cyanobacterium Lyngbya majuscula had the highest uptake rates per unit biomass, whereas the coral Madracis mirabilis had the lowest. Combining nutrient uptake rates with the standing biomass of each functional group on the reef, we estimated that the ammonium and phosphate delivered during runoff events is mostly taken up by turf algae and the two macroalgae Lobophora variegata and Dictyota pulchella. Our results support the often proposed, but rarely tested, assumption that turf algae and opportunistic macroalgae primarily benefit from episodic inputs of nutrients to coral reefs.

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.

Fast detection of nutrient limitation in macroalgae and seagrass with nutrient-induced fluorescence.

BACKGROUND: Rapid determination of which nutrients limit the primary production of macroalgae and seagrasses is vital for understanding the impacts of eutrophication on marine and freshwater ecosystems. However, current methods to assess nutrient limitation are often cumbersome and time consuming. For phytoplankton, a rapid method has been described based on short-term changes in chlorophyll fluorescence upon nutrient addition, also known as Nutrient-Induced Fluorescence Transients (NIFTs). Thus far, though, the NIFT technique was not well suited for macroalgae and seagrasses. METHODOLOGY & PRINCIPAL FINDINGS: We developed a new experimental setup so that the NIFT technique can be used to assess nutrient limitation of benthic macroalgae and seagrasses. We first tested the applicability of the technique on sea lettuce (Ulva lactuca) cultured in the laboratory on nutrient-enriched medium without either nitrogen or phosphorus. Addition of the limiting nutrient resulted in a characteristic change in the fluorescence signal, whereas addition of non-limiting nutrients did not yield a response. Next, we applied the NIFT technique to field samples of the encrusting fan-leaf alga Lobophora variegata, one of the key algal species often involved in the degradation of coral reef ecosystems. The results pointed at co-limitation of L. variegata by phosphorus and nitrogen, although it responded more strongly to phosphate than to nitrate and ammonium addition. For turtle grass (Thalassia testudinum) we found the opposite result, with a stronger NIFT response to nitrate and ammonium than to phosphate. CONCLUSIONS & SIGNIFICANCE: Our extension of the NIFT technique offers an easy and fast method (30-60 min per sample) to determine nutrient limitation of macroalgae and seagrasses. We successfully applied this technique to macroalgae on coral reef ecosystems and to seagrass in a tropical inner bay, and foresee wider application to other aquatic plants, and to other marine and freshwater ecosystems.