Toward a New Era of Coral Reef Monitoring.

Coral reefs host some of the highest concentrations of biodiversity and economic value in the oceans, yet these ecosystems are under threat due to climate change and other human impacts. Reef monitoring is routinely used to help prioritize reefs for conservation and evaluate the success of intervention efforts. Reef status and health are most frequently characterized using diver-based surveys, but the inherent limitations of these methods mean there is a growing need for advanced, standardized, and automated reef techniques that capture the complex nature of the ecosystem. Here we draw on experiences from our own interdisciplinary research programs to describe advances in in situ diver-based and autonomous reef monitoring. We present our vision for integrating interdisciplinary measurements for select "case-study" reefs worldwide and for learning patterns within the biological, physical, and chemical reef components and their interactions. Ultimately, these efforts could support the development of a scalable and standardized suite of sensors that capture and relay key data to assist in categorizing reef health. This framework has the potential to provide stakeholders with the information necessary to assess reef health during an unprecedented time of reef change as well as restoration and intervention activities.

Significance of Perylene for Source Allocation of Terrigenous Organic Matter in Aquatic Sediments.

Perylene is a frequently abundant, and sometimes the only polycyclic aromatic hydrocarbon (PAH) in aquatic sediments, but its origin has been subject of a longstanding debate in geochemical research and pollutant forensics because its historical record differs markedly from typical anthropogenic PAHs. Here we investigate whether perylene serves as a source-specific molecular marker of fungal activity in forest soils. We use a well-characterized sedimentary record (1735-1999) from the anoxic-bottom waters of the Pettaquamscutt River basin, RI to examine mass accumulation rates and isotope records of perylene, and compare them with total organic carbon and the anthropogenic PAH fluoranthene. We support our arguments with radiocarbon (14C) data of higher plant leaf-wax n-alkanoic acids. Isotope-mass balance-calculations of perylene and n-alkanoic acids indicate that ∼40% of sedimentary organic matter is of terrestrial origin. Further, both terrestrial markers are pre-aged on millennial time-scales prior to burial in sediments and are insensitive to elevated 14C concentrations following nuclear weapons testing in the mid-20th Century. Instead, changes coincide with enhanced erosional flux during urban sprawl. These findings suggest that perylene is definitely a product of soil-derived fungi, and a powerful chemical tracer to study the spatial and temporal connectivity between terrestrial and aquatic environments.

Genetically divergent Symbiodinium sp. display distinct molecular responses to pathogenic Vibrio and thermal stress.

Global climate change and anthropogenic activities are threatening the future survival of coral reef ecosystems. The ability of reef-building zooxanthellate coral to survive these stressors may be determined through fundamental differences within their symbiotic dinoflagellates (Symbiodinium sp.). We define the in vitro apoptotic response of 2 evolutionarily distant Symbiodinium sp., subtypes B2 and C1, to determine the synergistic effects of disease and temperature on cell viability using flow cytometry. The putative yellow band disease (YBD) consortium of Vibrio spp. bacteria and temperature (33°C) had a positive synergistic effect on C1 apoptosis, while B2 displayed increased apoptosis to elevated temperature (29 and 33°C), the Vibrio consortium, and a lone virulent strain of V. alginolyticus, but no synergistic effects. Additionally, heat shock protein 60 expression revealed differential cell-mediated temperature sensitivity between subtypes via western blotting. This result marks the first evidence of Symbiodinium sp. apoptotic variations to YBD pathogens and emphasizes the potential impact of synergistic stress on globally distributed coral-Symbiodinium symbioses.

Major similarities in the bacterial communities associated with lesioned and healthy Fungiidae corals.

Cultivation-based studies have demonstrated that yellow-band disease (YBD), a lesion-producing ailment affecting diverse species of coral, is caused by a consortium of Vibrio spp. This study takes the first cultivation-independent approach to examine the whole bacterial community associated with YBD-like lesioned corals. Two species of Fungiidae corals, Ctenactis crassa and Herpolitha limax, displaying YBD-like lesions were examined across diverse reefs throughout the Red Sea. Using a pyrosequencing approach targeting the V1-V3 regions of the SSU rRNA gene, no major differences in bacterial community composition or diversity were identified between healthy and lesioned corals of either species. Indicator species analysis did not find Vibrio significantly associated with the lesioned corals. However, operational taxonomic units belonging to the Ruegeria genus of Alphaproteobacteria and NS9 marine group of Flavobacteria were significantly associated with the lesioned corals. The most striking trend of this dataset was that reef location was found to be the most significant influence on the coral-bacterial community. It is possible that more pronounced lesion-specific bacterial signatures might have been concealed by the strong influence of environmental conditions on coral-bacteria. Overall, this study demonstrates inconsistencies between cultivation-independent and cultivation-based studies regarding the role of specific bacteria in coral diseases.

The microbiome of the Red Sea coral Stylophora pistillata is dominated by tissue-associated Endozoicomonas bacteria.

Endozoicomonas bacteria were found highly associated with the coral Stylophora pistillata, and these bacteria are also ubiquitously associated with diverse corals worldwide. Novel Endozoicomonas-specific probes revealed that Endozoicomonas bacteria were abundant in the endodermal tissues of S. pistillata and appear to have an intimate relationship with the coral.

Ulcerated yellow spot syndrome: implications of aquaculture-related pathogens associated with soft coral Sarcophyton ehrenbergi tissue lesions.

We introduce a new marine syndrome called ulcerated yellow spot, affecting the soft coral Sarcophyton ehrenbergi. To identify bacteria associated with tissue lesions, tissue and mucus samples were taken during a 2009 Indo-Pacific research expedition near the Wakatobi Island chain, Indonesia. Polymerase chain reaction targeting the 16S rDNA gene indicated associations with the known fish-disease-causing bacterium Photobacterium damselae, as well as multiple Vibrio species. Results indicate a shift toward decreasing diversity of bacteria in lesioned samples. Photobacterium damselae ssp. piscicida, formerly known as Pasteurella piscicida, is known as the causative agent of fish pasteurellosis and in this study, was isolated solely in lesioned tissues. Globally, fish pasteurellosis is one of the most damaging fish diseases in marine aquaculture. Vibrio alginolyticus, a putative pathogen associated with yellow band disease in scleractinian coral, was also isolated from lesioned tissues. Lesions appear to be inflicting damage on symbiotic zooxanthellae (Symbiodinium sp.), measurable by decreases in mitotic index, cell density and photosynthetic efficiency. Mitotic index of zooxanthellae within infected tissue samples was decreased by ~80%, while zooxanthellae densities were decreased by ~40% in lesioned tissue samples compared with healthy coral. These results provide evidence for the presence of known aquaculture pathogens in lesioned soft coral and may be a concern with respect to cross-species epizootics in the tropics.

Response to Comment on "A global environmental crisis 42,000 years ago".

Our study on the exact timing and the potential climatic, environmental, and evolutionary consequences of the Laschamps Geomagnetic Excursion has generated the hypothesis that geomagnetism represents an unrecognized driver in environmental and evolutionary change. It is important for this hypothesis to be tested with new data, and encouragingly, none of the studies presented by Picin et al. undermine our model.

Response to Comment on "A global environmental crisis 42,000 years ago".

Our paper about the impacts of the Laschamps Geomagnetic Excursion 42,000 years ago has provoked considerable scientific and public interest, particularly in the so-called Adams Event associated with the initial transition of the magnetic poles. Although we welcome the opportunity to discuss our new ideas, Hawks' assertions of misrepresentation are especially disappointing given his limited examination of the material.

A global environmental crisis 42,000 years ago.

Geological archives record multiple reversals of Earth's magnetic poles, but the global impacts of these events, if any, remain unclear. Uncertain radiocarbon calibration has limited investigation of the potential effects of the last major magnetic inversion, known as the Laschamps Excursion [41 to 42 thousand years ago (ka)]. We use ancient New Zealand kauri trees (Agathis australis) to develop a detailed record of atmospheric radiocarbon levels across the Laschamps Excursion. We precisely characterize the geomagnetic reversal and perform global chemistry-climate modeling and detailed radiocarbon dating of paleoenvironmental records to investigate impacts. We find that geomagnetic field minima ~42 ka, in combination with Grand Solar Minima, caused substantial changes in atmospheric ozone concentration and circulation, driving synchronous global climate shifts that caused major environmental changes, extinction events, and transformations in the archaeological record.

Consistently dated Atlantic sediment cores over the last 40 thousand years.

Rapid changes in ocean circulation and climate have been observed in marine-sediment and ice cores over the last glacial period and deglaciation, highlighting the non-linear character of the climate system and underlining the possibility of rapid climate shifts in response to anthropogenic greenhouse gas forcing. To date, these rapid changes in climate and ocean circulation are still not fully explained. One obstacle hindering progress in our understanding of the interactions between past ocean circulation and climate changes is the difficulty of accurately dating marine cores. Here, we present a set of 92 marine sediment cores from the Atlantic Ocean for which we have established age-depth models that are consistent with the Greenland GICC05 ice core chronology, and computed the associated dating uncertainties, using a new deposition modeling technique. This is the first set of consistently dated marine sediment cores enabling paleoclimate scientists to evaluate leads/lags between circulation and climate changes over vast regions of the Atlantic Ocean. Moreover, this data set is of direct use in paleoclimate modeling studies.

Rapid global ocean-atmosphere response to Southern Ocean freshening during the last glacial.

Contrasting Greenland and Antarctic temperatures during the last glacial period (115,000 to 11,650 years ago) are thought to have been driven by imbalances in the rates of formation of North Atlantic and Antarctic Deep Water (the 'bipolar seesaw'). Here we exploit a bidecadally resolved 14C data set obtained from New Zealand kauri (Agathis australis) to undertake high-precision alignment of key climate data sets spanning iceberg-rafted debris event Heinrich 3 and Greenland Interstadial (GI) 5.1 in the North Atlantic (~30,400 to 28,400 years ago). We observe no divergence between the kauri and Atlantic marine sediment 14C data sets, implying limited changes in deep water formation. However, a Southern Ocean (Atlantic-sector) iceberg rafted debris event appears to have occurred synchronously with GI-5.1 warming and decreased precipitation over the western equatorial Pacific and Atlantic. An ensemble of transient meltwater simulations shows that Antarctic-sourced salinity anomalies can generate climate changes that are propagated globally via an atmospheric Rossby wave train.A challenge for testing mechanisms of past climate change is the precise correlation of palaeoclimate records. Here, through climate modelling and the alignment of terrestrial, ice and marine 14C and 10Be records, the authors show that Southern Ocean freshwater hosing can trigger global change.

Response to Comment on "Abrupt warming events drove Late Pleistocene Holarctic megafaunal turnover".

Rasmussen and Svensson correctly point out that there is currently no satisfactory method to fully align the Greenland and Cariaco Basin records of climate change. However, our approach using interstadial onsets as tie-points allows direct comparison between radiocarbon dates and Greenland climate records. Crucially, both the standard Greenland and the merged Greenland-Cariaco time scales show that interstadial warming was associated with megafaunal genetic transitions.

CO2 and fire influence tropical ecosystem stability in response to climate change.

Interactions between climate, fire and CO2 are believed to play a crucial role in controlling the distributions of tropical woodlands and savannas, but our understanding of these processes is limited by the paucity of data from undisturbed tropical ecosystems. Here we use a 28,000-year integrated record of vegetation, climate and fire from West Africa to examine the role of these interactions on tropical ecosystem stability. We find that increased aridity between 28-15 kyr B.P. led to the widespread expansion of tropical grasslands, but that frequent fires and low CO2 played a crucial role in stabilizing these ecosystems, even as humidity changed. This resulted in an unstable ecosystem state, which transitioned abruptly from grassland to woodlands as gradual changes in CO2 and fire shifted the balance in favor of woody plants. Since then, high atmospheric CO2 has stabilized tropical forests by promoting woody plant growth, despite increased aridity. Our results indicate that the interactions between climate, CO2 and fire can make tropical ecosystems more resilient to change, but that these systems are dynamically unstable and potentially susceptible to abrupt shifts between woodland and grassland dominated states in the future.

Punctuated Shutdown of Atlantic Meridional Overturning Circulation during Greenland Stadial 1.

The Greenland Stadial 1 (GS-1; ~12.9 to 11.65 kyr cal BP) was a period of North Atlantic cooling, thought to have been initiated by North America fresh water runoff that caused a sustained reduction of North Atlantic Meridional Overturning Circulation (AMOC), resulting in an antiphase temperature response between the hemispheres (the 'bipolar seesaw'). Here we exploit sub-fossil New Zealand kauri trees to report the first securely dated, decadally-resolved atmospheric radiocarbon ((14)C) record spanning GS-1. By precisely aligning Southern and Northern Hemisphere tree-ring (14)C records with marine (14)C sequences we document two relatively short periods of AMOC collapse during the stadial, at ~12,920-12,640 cal BP and 12,050-11,900 cal BP. In addition, our data show that the interhemispheric atmospheric (14)C offset was close to zero prior to GS-1, before reaching 'near-modern' values at ~12,660 cal BP, consistent with synchronous recovery of overturning in both hemispheres and increased Southern Ocean ventilation. Hence, sustained North Atlantic cooling across GS-1 was not driven by a prolonged AMOC reduction but probably due to an equatorward migration of the Polar Front, reducing the advection of southwesterly air masses to high latitudes. Our findings suggest opposing hemispheric temperature trends were driven by atmospheric teleconnections, rather than AMOC changes.

PALEOECOLOGY. Abrupt warming events drove Late Pleistocene Holarctic megafaunal turnover.

The mechanisms of Late Pleistocene megafauna extinctions remain fiercely contested, with human impact or climate change cited as principal drivers. We compared ancient DNA and radiocarbon data from 31 detailed time series of regional megafaunal extinctions and replacements over the past 56,000 years with standard and new combined records of Northern Hemisphere climate in the Late Pleistocene. Unexpectedly, rapid climate changes associated with interstadial warming events are strongly associated with the regional replacement or extinction of major genetic clades or species of megafauna. The presence of many cryptic biotic transitions before the Pleistocene/Holocene boundary revealed by ancient DNA confirms the importance of climate change in megafaunal population extinctions and suggests that metapopulation structures necessary to survive such repeated and rapid climatic shifts were susceptible to human impacts.

Two centuries of limited variability in subtropical North Atlantic thermocline ventilation.

Ventilation and mixing of oceanic gyres is important to ocean-atmosphere heat and gas transfer, and to mid-latitude nutrient supply. The rates of mode water formation are believed to impact climate and carbon exchange between the surface and mid-depth water over decadal periods. Here, a record of (14)C/(12)C (1780-1940), which is a proxy for vertical ocean mixing, from an annually banded coral from Bermuda, shows limited inter-annual variability and a substantial Suess Effect (the decrease in (14)C/(12)C since 1900). The Sargasso Sea mixing rates between the surface and thermocline varied minimally over the past two centuries, despite changes to mean-hemispheric climate, including the Little Ice Age and variability in the North Atlantic Oscillation. This result indicates that regional formation rates of sub-tropical mode water are stable over decades, and that anthropogenic carbon absorbed by the ocean does not return to the surface at a variable rate.

Temporal distributions of anthropogenic Al, Zn and Pb in Hong Kong Porites coral during the last two centuries.

A 182-year long record of trace metal concentrations of aluminum, zinc and lead was reconstructed from a massive Porites coral skeleton from southeastern Hong Kong to evaluate the impacts of anthropogenic activity on the marine environment. Zn/Ca and Pb/Ca ratios fluctuate synchronously from the early 19th century to the present, indicating that the marine environment has been anthropogenically influenced since industrialization. Additionally, land reclamation, mining, and ship building activities are recorded by elevated Al/Ca ratios from 1900 to 1950. The coral record indicates that high levels of Zn, Pb and Al occur coincidentally with local wars, and may have contributed to partial colony mortality. Pb/Ca does not correlate well with hemispheric proxy records after 1950, indicating that coastal corals may be recording local rather than hemispheric contamination. Pb/Ca levels in Hong Kong, Guangdong and Hainan corals imply a continuous supply of Pb-based contamination to southern China not reflected in hemispheric signals.

Century-scale records of land-based activities recorded in Mesoamerican coral cores.

The Mesoamerican Reef, the second-largest barrier reef in the world, is located in the western Caribbean Sea off the coasts of Mexico, Belize, Guatemala, and Honduras. Particularly in the south, the surrounding watersheds are steep and the climate is extremely wet. With development and agricultural expansion, the potential for negative impacts to the reef from land-based runoff becomes high. We constructed annually resolved century-scale records of metal/calcium ratios in coral skeletons collected from four sites experiencing a gradient of land-based runoff. Our proxy data indicate that runoff onto the reef has increased relatively steadily over time at all sites, consistent with land use trends from historical records. Sediment supply to the reef is greater in the south, and these more exposed reefs will probably benefit most immediately from management that targets runoff reduction. However, because runoff at all sites is steadily increasing, even distal sites will benefit from watershed management.

Abrupt tropical vegetation response to rapid climate changes.

Identifying leads and lags between high- and low-latitude abrupt climate shifts is needed to understand where and how such events were triggered. Vascular plant biomarkers preserved in Cariaco basin sediments reveal rapid vegetation changes in northern South America during the last deglaciation, 15,000 to 10,000 years ago. Comparing the biomarker records to climate proxies from the same sediment core provides a precise measure of the relative timing of changes in different regions. Abrupt deglacial climate shifts in tropical and high-latitude North Atlantic regions were synchronous, whereas changes in tropical vegetation consistently lagged climate shifts by several decades.

Synchroneity of tropical and high-latitude Atlantic temperatures over the last glacial termination.

A high-resolution western tropical Atlantic sea surface temperature (SST) record from the Cariaco Basin on the northern Venezuelan shelf, based on Mg/Ca values in surface-dwelling planktonic foraminifera, reveals that changes in SST over the last glacial termination are synchronous, within +/-30 to +/-90 years, with the Greenland Ice Sheet Project 2 air temperature proxy record and atmospheric methane record. The most prominent deglacial event in the Cariaco record occurred during the Younger Dryas time interval, when SSTs dropped by 3 degrees to 4 degrees C. A rapid southward shift in the atmospheric intertropical convergence zone could account for the synchroneity of tropical temperature, atmospheric methane, and high-latitude changes during the Younger Dryas.