Coral taxonomy and local stressors drive bleaching prevalence across the Hawaiian Archipelago in 2019.

The Hawaiian Archipelago experienced a moderate bleaching event in 2019-the third major bleaching event over a 6-year period to impact the islands. In response, the Hawai'i Coral Bleaching Collaborative (HCBC) conducted 2,177 coral bleaching surveys across the Hawaiian Archipelago. The HCBC was established to coordinate bleaching monitoring efforts across the state between academic institutions, non-governmental organizations, and governmental agencies to facilitate data sharing and provide management recommendations. In 2019, the goals of this unique partnership were to: 1) assess the spatial and temporal patterns of thermal stress; 2) examine taxa-level patterns in bleaching susceptibility; 3) quantify spatial variation in bleaching extent; 4) compare 2019 patterns to those of prior bleaching events; 5) identify predictors of bleaching in 2019; and 6) explore site-specific management strategies to mitigate future bleaching events. Both acute thermal stress and bleaching in 2019 were less severe overall compared to the last major marine heatwave events in 2014 and 2015. Bleaching observed was highly site- and taxon-specific, driven by the susceptibility of remaining coral assemblages whose structure was likely shaped by previous bleaching and subsequent mortality. A suite of environmental and anthropogenic predictors was significantly correlated with observed bleaching in 2019. Acute environmental stressors, such as temperature and surface light, were equally important as previous conditions (e.g. historical thermal stress and historical bleaching) in accounting for variation in bleaching during the 2019 event. We found little evidence for acclimation by reefs to thermal stress in the main Hawaiian Islands. Moreover, our findings illustrate how detrimental effects of local anthropogenic stressors, such as tourism and urban run-off, may be exacerbated under high thermal stress. In light of the forecasted increase in severity and frequency of bleaching events, future mitigation of both local and global stressors is a high priority for the future of corals in Hawai'i.

Low-level nutrient enrichment during thermal stress delays bleaching and ameliorates calcification in three Hawaiian reef coral species.

Terrestrial-based nutrient pollution has emerged as one of the most detrimental factors to coral health in many reef habitats. Recent studies have shown that excessive dissolved inorganic nutrients can reduce coral thermal tolerance thresholds and even exacerbate bleaching during thermal stress, yet the effects of minor nutrient enrichment under heat stress have not been extensively studied. In this study, Lobactis scutaria, Montipora capitata, and Pocillopora acuta colonies under heated conditions (~30.5 °C) were exposed to low and balanced nitrogen and phosphorous concentrations over a 31-day heating period. Coral colonies were collected from Kane'ohe Bay, O'ahu, which has a unique history of nutrient pollution, and held in mesocosms that allowed for environmental manipulation yet are also influenced by local field conditions. Principal findings included delays in the bleaching of nutrient-enriched heated colonies as compared to heated-only colonies, in addition to relatively greater calcification rates and lower proportions of early-stage paling. Species-specific outcomes were prevalent, with L. scutaria demonstrating no difference in calcification with enrichment under heat stress. By the end of the heating stage, however, many heated colonies were at least partially impacted by bleaching or mortality. Despite this, our findings suggest that low levels of balanced nutrient enrichment may serve as a mitigative force during thermal events. Further field-based studies will be required to assess these results in different reef habitats.

Stasis and diversity in living fossils: Species delimitation and evolution of lingulid brachiopods.

The Lingulidae are often considered living fossils, because they have shown little morphological change since the Paleozoic. Limited morphological variation has also made the taxonomic study of living lingulids challenging. We investigated species diversity and phylogenetic relationships of extant lingulids and show that they are substantially more diverse than realized, demonstrating that morphological stasis was commonly accompanied by speciation. Species delimitation based on cytochrome c oxidase subunit I (COI) gene sequences from 194 specimens sampled from East Asia, Australia, Oceania, and the Americas suggested 14-22 species in the lingulids (9-17 species in Lingula and 4-5 species in Glottidia), in contrast to the 11-12 species currently recognized globally in the family. Four-gene phylogenetic analyses supported the sister relationship between Lingula and Glottidia. Within Lingula, L. adamsi, which possesses large, brownish shells, was recovered as sister to all remaining Lingula species, which have more or less greenish shells. Within the greenish Lingula clade, the 'L. anatina' complex was sister to the clade that includes the 'L. reevei' complex. The 'L. anatina' complex was further separated into two major clades with partly separate ranges centered on (i) temperate East Asia, and (ii) the tropical west-central Pacific. Within Glottidia, Pacific species were nested within Atlantic species. Time-calibrated phylogenetic analyses suggested that Lingula likely originated in the early Cretaceous contrary to a previously proposed hypothesis advocating a Cenozoic origin. The separation of Lingula and Glottidia appears to date from the Mesozoic, not from the Carboniferous, contrary to a previous hypothesis. Overall, our results uncovered substantial cryptic diversity in lingulids, which will form the basis for conservation and further taxonomic revision.

Evidence of acclimatization or adaptation in Hawaiian corals to higher ocean temperatures.

Ocean temperatures have been accelerating at an alarming rate mainly due to anthropogenic fossil fuel emissions. This has led to an increase in the severity and duration of coral bleaching events. Predicted projections for the state of reefs do not take into account the rates of adaptation or acclimatization of corals as these have not as yet been fully documented. To determine any possible changes in thermal tolerances, manipulative experiments were conducted to precisely replicate the initial, pivotal research defining threshold temperatures of corals nearly five decades ago. Statistically higher calcification rates, survivorship, and lower mortality were observed in Montipora capitata, Pocillopora damicornis, and Lobactis scutaria in the present study at 31 °C compared to the original 1970 findings. First whole colony mortality was also observed to occur sooner in 1970 than in 2017 in M. capitata (3 d vs. 15 d respectively), L. scutaria (3 d vs. 17 d), and in P. damicornis (3 d vs. 13 d). Additionally, bleaching occurred sooner in 1970 compared to the 2017 experiment across species. Irradiance was an important factor during the recovery period for mortality but did not significantly alter calcification. Mortality was decreased by 17% with a 50% reduction in irradiance during the recovery period. These findings provide the first evidence of coral acclimatization or adaptation to increasing ocean temperatures for corals collected from the same location and using close replication of the experiment conducted nearly 50 years earlier. An important factor in this increased resistance to elevated temperature may be related to removal of the discharge of treated sewage into Kane'ohe Bay and resulting decrease in nitrification and eutrophication. However, this level of increased temperature tolerance may not be occurring rapidly enough to escape the projected increased intensity of bleaching events, as evidenced by the recent 2014 and 2015 high coral mortality in Hawai'i (34%) and in the tropics worldwide.

Effectiveness of coral relocation as a mitigation strategy in Kane'ohe Bay, Hawai'i.

Coral reef restoration and management techniques are in ever-increasing demand due to the global decline of coral reefs in the last several decades. Coral relocation has been established as an appropriate restoration technique in select cases, particularly where corals are scheduled for destruction. However, continued long-term monitoring of recovery of transplanted corals is seldom sustained. Removal of coral from a navigation channel and relocation to a similar nearby dredged site occurred in 2005. Coral recovery at the donor site and changes in fish populations at the receiving site were tracked periodically over the following decade. Coral regrowth at the donor site was rapid until a recent bleaching event reduced coral cover by more than half. The transplant of mature colonies increased spatial complexity at the receiving site, immediately increasing fish biomass, abundance, and species that was maintained throughout subsequent surveys. Our research indicates that unlike the majority of historical accounts of coral relocation in the Pacific, corals transplanted into wave-protected areas with similar conditions as the original site can have high survival rates. Data on long-term monitoring of coral transplants in diverse environments is central in developing management and mitigation strategies.

Patterns of bleaching and mortality following widespread warming events in 2014 and 2015 at the Hanauma Bay Nature Preserve, Hawai'i.

Drastic increases in global carbon emissions in the past century have led to elevated sea surface temperatures that negatively affect coral reef organisms. Worldwide coral bleaching-related mortality is increasing and data has shown even isolated and protected reefs are vulnerable to the effects of global climate change. In 2014 and 2015, coral reefs in the main Hawaiian Islands (MHI) suffered up to 90% bleaching, with higher than 50% subsequent mortality in some areas. The location and severity of bleaching and mortality was strongly influenced by the spatial and temporal patterns of elevated seawater temperatures. The main objective of this research was to understand the spatial extent of bleaching mortality in Hanauma Bay Nature Preserve (HBNP), O'ahu, Hawai'i to gain a baseline understanding of the physical processes that influence localized bleaching dynamics. Surveys at HBNP in October 2015 and January 2016 revealed extensive bleaching (47%) and high levels of coral mortality (9.8%). Bleaching was highly variable among the four HBNP sectors and ranged from a low of ∼31% in the central bay at Channel (CH) to a high of 57% in the area most frequented by visitors (Keyhole; KH). The highest levels of bleaching occurred in two sectors with different circulation patterns: KH experienced comparatively low circulation velocity and a low temperature increase while Witches Brew (WB) and Backdoors (BD) experienced higher circulation velocity and higher temperature increase. Cumulative mortality was highest at WB (5.0%) and at BD (2.9%) although WB circulation velocity is significantly higher. HBNP is minimally impacted by local factors that can lead to decline such as high fishing pressure or sedimentation although human use is high. Despite the lack of these influences, high coral mortality occurred. Visitor impacts are strikingly different in the two sectors that experienced the highest mortality evidenced by the differences in coral cover associated with visitor use however, coral mortality was similar. These results suggest that elevated temperature was more influential in coral bleaching and the associated mortality than high circulation or visitor use.

Coral-algae metabolism and diurnal changes in the CO2-carbonate system of bulk sea water.

Precise measurements were conducted in continuous flow seawater mesocosms located in full sunlight that compared metabolic response of coral, coral-macroalgae and macroalgae systems over a diurnal cycle. Irradiance controlled net photosynthesis (P net), which in turn drove net calcification (G net), and altered pH. P net exerted the dominant control on [CO3 (2-)] and aragonite saturation state (Ωarag) over the diel cycle. Dark calcification rate decreased after sunset, reaching zero near midnight followed by an increasing rate that peaked at 03:00 h. Changes in Ωarag and pH lagged behind G net throughout the daily cycle by two or more hours. The flux rate P net was the primary driver of calcification. Daytime coral metabolism rapidly removes dissolved inorganic carbon (DIC) from the bulk seawater and photosynthesis provides the energy that drives G net while increasing the bulk water pH. These relationships result in a correlation between G net and Ωarag, with Ωarag as the dependent variable. High rates of H(+) efflux continued for several hours following mid-day peak G net suggesting that corals have difficulty in shedding waste protons as described by the Proton Flux Hypothesis. DIC flux (uptake) followed P net and G net and dropped off rapidly following peak P net and peak G net indicating that corals can cope more effectively with the problem of limited DIC supply compared to the problem of eliminating H(+). Over a 24 h period the plot of total alkalinity (AT ) versus DIC as well as the plot of G net versus Ωarag revealed a circular hysteresis pattern over the diel cycle in the coral and coral-algae mesocosms, but not the macroalgae mesocosm. Presence of macroalgae did not change G net of the corals, but altered the relationship between Ωarag and G net. Predictive models of how future global changes will effect coral growth that are based on oceanic Ωarag must include the influence of future localized P net on G net and changes in rate of reef carbonate dissolution. The correlation between Ωarag and G net over the diel cycle is simply the response of the CO2-carbonate system to increased pH as photosynthesis shifts the equilibria and increases the [CO3 (2-)] relative to the other DIC components of [HCO3 (-)] and [CO2]. Therefore Ωarag closely tracked pH as an effect of changes in P net, which also drove changes in G net. Measurements of DIC flux and H(+) flux are far more useful than concentrations in describing coral metabolism dynamics. Coral reefs are systems that exist in constant disequilibrium with the water column.

Use of integrated landscape indicators to evaluate the health of linked watersheds and coral reef environments in the Hawaiian islands.

A linkage between the condition of watersheds and adjacent nearshore coral reef communities is an assumed paradigm in the concept of integrated coastal management. However, quantitative evidence for this "catchment to sea" or "ridge to reef" relationship on oceanic islands is lacking and would benefit from the use of appropriate marine and terrestrial landscape indicators to quantify and evaluate ecological status on a large spatial scale. To address this need, our study compared the Hawai'i Watershed Health Index (HI-WHI) and Reef Health Index (HI-RHI) derived independently of each other over the past decade. Comparisons were made across 170 coral reef stations at 52 reef sites adjacent to 42 watersheds throughout the main Hawaiian Islands. A significant positive relationship was shown between the health of watersheds and that of adjacent reef environments when all sites and depths were considered. This relationship was strongest for sites facing in a southerly direction, but diminished for north facing coasts exposed to persistent high surf. High surf conditions along the north shore increase local wave driven currents and flush watershed-derived materials away from nearshore waters. Consequently, reefs in these locales are less vulnerable to the deposition of land derived sediments, nutrients and pollutants transported from watersheds to ocean. Use of integrated landscape health indices can be applied to improve regional-scale conservation and resource management.

Effects of mechanical fracturing and experimental trampling on Hawaiian corals.

In situ trampling occurred under experimental conditions to quantify the differences in the responses to anthropogenic trampling in four dominant species of Hawaiian corals, Porites compressa, Porites lobata, Montipora capitata, and Pocillopora meandrina. Trampling was simulated daily for a period of nine days at which time further breakage was minimal. Forty treatment colonies produced 559 fragments. Trampling was followed by an 11-month recovery period. Coral colony and fragment mortality was low. All four species were highly tolerant of inflicted damage, suggesting that some species of corals can withstand limited pulse events that allow time for recovery. Growth rates following trampling were significantly lower in the treatment groups for three of the four species. This study demonstrated that very few trampling events can produce significant changes in growth even after a long recovery period. Survivorship of fragments is clearly size- and species-dependent in M. capitata and P. compressa. Smaller fragments (<5 cm) had higher mortality than larger fragments (>5 cm). High breakage rates for M. capitata and P. compressa are consistent with the near shore, low-energy regions they inhabit-the same environment frequented by skin divers and waders. Mechanical tests were conducted to determine tensile and compressive strengths. Pocillopora meandrina exhibited the strongest skeletal strength, followed in decreasing order by Porites lobata, Porites compressa, and Montipora capitata. The skeletal strength obtained from the experiments correlate with the wave energy present in the environments in the regions they inhabit, suggesting that structural strength of corals is an adaptive response to hydraulic stress.