Experimental coral reef communities transform yet persist under mitigated future ocean warming and acidification.

Coral reefs are among the most sensitive ecosystems affected by ocean warming and acidification, and are predicted to collapse over the next few decades. Reefs are predicted to shift from net accreting calcifier-dominated systems with exceptionally high biodiversity to net eroding algal-dominated systems with dramatically reduced biodiversity. Here, we present a two-year experimental study examining the responses of entire mesocosm coral reef communities to warming (+2 °C), acidification (-0.2 pH units), and combined future ocean (+2 °C, -0.2 pH) treatments. Contrary to modeled projections, we show that under future ocean conditions, these communities shift structure and composition yet persist as novel calcifying ecosystems with high biodiversity. Our results suggest that if climate change is limited to Paris Climate Agreement targets, coral reefs could persist in an altered state rather than collapse.

Biodiversity of coral reef cryptobiota shuffles but does not decline under the combined stressors of ocean warming and acidification.

Ocean-warming and acidification are predicted to reduce coral reef biodiversity, but the combined effects of these stressors on overall biodiversity are largely unmeasured. Here, we examined the individual and combined effects of elevated temperature (+2 °C) and reduced pH (-0.2 units) on the biodiversity of coral reef communities that developed on standardized sampling units over a 2-y mesocosm experiment. Biodiversity and species composition were measured using amplicon sequencing libraries targeting the cytochrome oxidase I (COI) barcoding gene. Ocean-warming significantly increased species richness relative to present-day control conditions, whereas acidification significantly reduced richness. Contrary to expectations, species richness in the combined future ocean treatment with both warming and acidification was not significantly different from the present-day control treatment. Rather than the predicted collapse of biodiversity under the dual stressors, we find significant changes in the relative abundance but not in the occurrence of species, resulting in a shuffling of coral reef community structure among the highly species-rich cryptobenthic community. The ultimate outcome of altered community structure for coral reef ecosystems will depend on species-specific ecological functions and community interactions. Given that most species on coral reefs are members of the understudied cryptobenthos, holistic research on reef communities is needed to accurately predict diversity-function relationships and ecosystem responses to future climate conditions.

Ecological succession of the sponge cryptofauna in Hawaiian reefs add new insights to detritus production by pioneering species.

Successional theory proposes that fast growing and well dispersed opportunistic species are the first to occupy available space. However, these pioneering species have relatively short life cycles and are eventually outcompeted by species that tend to be longer-lived and have lower dispersal capabilities. Using Autonomous Reef Monitoring Structures (ARMS) as standardized habitats, we examine the assembly and stages of ecological succession among sponge species with distinctive life history traits and physiologies found on cryptic coral reef habitats of Kane'ohe Bay, Hawai'i. Sponge recruitment was monitored bimonthly over 2 years on ARMS deployed within a natural coral reef habitat resembling the surrounding climax community and on ARMS placed in unestablished mesocosms receiving unfiltered seawater directly from the natural reef deployment site. Fast growing haplosclerid and calcareous sponges initially recruited to and dominated the mesocosm ARMS. In contrast, only slow growing long-lived species initially recruited to the reef ARMS, suggesting that despite available space, the stage of ecological succession in the surrounding habitat influences sponge community development in uninhabited space. Sponge composition and diversity between early summer and winter months within mesocosm ARMS shifted significantly as the initially recruited short-lived calcareous and haplosclerid species initially recruit and then died off. The particulate organic carbon contribution of dead sponge tissue from this high degree of competition-free community turnover suggests a possible new component to the sponge loop hypothesis which remains to be tested among these pioneering species. This source of detritus could be significant in early community development of young coastal habitats but less so on established coral reefs where the community is dominated by long-lived colonial sponges.

Abundance, size, and survival of recruits of the reef coral Pocillopora acuta under ocean warming and acidification.

Ocean warming and acidification are among the greatest threats to coral reefs. Massive coral bleaching events are becoming increasingly common and are predicted to be more severe and frequent in the near future, putting corals reefs in danger of ecological collapse. This study quantified the abundance, size, and survival of the coral Pocillopora acuta under future projections of ocean warming and acidification. Flow-through mesocosms were exposed to current and future projections of ocean warming and acidification in a factorial design for 22 months. Neither ocean warming or acidification, nor their combination, influenced the size or abundance of P. acuta recruits, but heating impacted subsequent health and survival of the recruits. During annual maximum temperatures, coral recruits in heated tanks experienced higher levels of bleaching and subsequent mortality. Results of this study indicate that P. acuta is able to recruit under projected levels of ocean warming and acidification but are susceptible to bleaching and mortality during the warmest months.

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.

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.

The unnatural history of Kane'ohe Bay: coral reef resilience in the face of centuries of anthropogenic impacts.

Kane'ohe Bay, which is located on the on the NE coast of O'ahu, Hawai'i, represents one of the most intensively studied estuarine coral reef ecosystems in the world. Despite a long history of anthropogenic disturbance, from early settlement to post European contact, the coral reef ecosystem of Kane'ohe Bay appears to be in better condition in comparison to other reefs around the world. The island of Moku o Lo'e (Coconut Island) in the southern region of the bay became home to the Hawai'i Institute of Marine Biology in 1947, where researchers have since documented the various aspects of the unique physical, chemical, and biological features of this coral reef ecosystem. The first human contact by voyaging Polynesians occurred at least 700 years ago. By A.D. 1250 Polynesians voyagers had settled inhabitable islands in the region which led to development of an intensive agricultural, fish pond and ocean resource system that supported a large human population. Anthropogenic disturbance initially involved clearing of land for agriculture, intentional or accidental introduction of alien species, modification of streams to supply water for taro culture, and construction of massive shoreline fish pond enclosures and extensive terraces in the valleys that were used for taro culture. The arrival by the first Europeans in 1778 led to further introductions of plants and animals that radically changed the landscape. Subsequent development of a plantation agricultural system led to increased human immigration, population growth and an end to traditional land and water management practices. The reefs were devastated by extensive dredge and fill operations as well as rapid growth of human population, which led to extensive urbanization of the watershed. By the 1960's the bay was severely impacted by increased sewage discharge along with increased sedimentation due to improper grading practices and stream channelization, resulting in extensive loss of coral cover. The reefs of Kane'ohe Bay developed under estuarine conditions and thus have been subjected to multiple natural stresses. These include storm floods, a more extreme temperature range than more oceanic reefs, high rates of sedimentation, and exposure at extreme low tides. Deposition and degradation of organic materials carried into the bay from the watershed results in low pH conditions such that according to some ocean acidification projections the rich coral reefs in the bay should not exist. Increased global temperature due to anthropogenic fossil fuel emmisions is now impacting these reefs with the first "bleaching event" in 1996 and a second more severe event in 2014. The reefs of Kane'ohe Bay have developed and persist under rather severe natural and anthropogenic perturbations. To date, these reefs have proved to be very resilient once the stressor has been removed. A major question remains to be answered concerning the limits of Kane'ohe Bay reef resilience in the face of global climate change.

The 2014 coral bleaching and freshwater flood events in Kane'ohe Bay, Hawai'i.

Until recently, subtropical Hawai'i escaped the major bleaching events that have devastated many tropical regions, but the continued increases in global long-term mean temperatures and the apparent ending of the Pacific Decadal Oscillation (PDO) cool phase have increased the risk of bleaching events. Climate models and observations predict that bleaching in Hawai'i will occur with increasing frequency and increasing severity over future decades. A freshwater "kill" event occurred during July 2014 in the northern part of Kane'ohe Bay that reduced coral cover by 22.5% in the area directly impacted by flooding. A subsequent major bleaching event during September 2014 caused extensive coral bleaching and mortality throughout the bay and further reduced coral cover in the freshwater kill area by 60.0%. The high temperature bleaching event only caused a 1.0% reduction in live coral throughout the portion of the bay not directly impacted by the freshwater event. Thus, the combined impact of the low salinity event and the thermal bleaching event appears to be more than simply additive. The temperature regime during the September 2014 bleaching event was analogous in duration and intensity to that of the large bleaching event that occurred previously during August 1996, but resulted in a much larger area of bleaching and coral mortality. Apparently seasonal timing as well as duration and magnitude of heating is important. Coral spawning in the dominant coral species occurs early in the summer, so reservoirs of stored lipid in the corals had been depleted by spawning prior to the September 2014 event. Warm months above 27 °C result in lower coral growth and presumably could further decrease lipid reserves, leading to a bleaching event that was more severe than would have happened if the high temperatures occurred earlier in the summer. Hawaiian reef corals decrease skeletal growth at temperatures above 27 °C, so perhaps the "stress period" actually started long before the bleaching threshold of 29 °C was reached. Hawai'i is directly influenced by the PDO which may become a factor influencing bleaching events in subtropical Hawai'i in much the same manner as variations in the El Niño Southern Oscillation (ENSO) influences bleaching events at low latitudes in the tropical Pacific. Records show that offshore temperatures measured by satellite will not always predict inshore bleaching because other factors (high cloud cover, high wind and wave action, tidal exchange rate) can limit inshore heating and prevent temperatures in the bay from reaching the bleaching threshold. Low light levels due to cloud cover or high turbidity can also serve to prevent bleaching.