Malcolm T. McCulloch

• Professor (Full) at The University of Western Australia

The future of coral reef ecosystems is under threat because vital reef-accreting species such as coralline algae are highly susceptible to ocean acidification. Although ocean acidification is known to reduce coralline algal growth rates, its direct effects on the development of coralline algal reproductive structures (conceptacles) is largely unkno...

Crustose coralline algae play a crucial role in the building of reefs in the photic zones of nearshore ecosystems globally, and are highly susceptible to ocean acidification1–3. Nevertheless, the extent to which ecologically important crustose coralline algae can gain tolerance to ocean acidification over multiple generations of exposure is unknown...

Natural variability in pH in the diffusive boundary layer (DBL), the discrete layer of seawater between bulk seawater and the outer surface of organisms, could be an important factor determining the response of corals and coralline algae to ocean acidification (OA). Here, two corals with different morphologies and one coralline alga were maintained...

Ocean acidification (OA) is a major threat to coral reefs, which are built by calcareous species. However, long-term assessments of the impacts of OA are scarce, limiting the understanding of the capacity of corals and coralline algae to acclimatize to high partial pressure of carbon dioxide (pCO2) levels. Species-specific sensitivities to OA are i...

Ocean acidification poses a serious threat to marine calcifying organisms, yet experimental and field studies have found highly diverse responses among species and environments. Our understanding of the underlying drivers of differential responses to ocean acidification is currently limited by difficulties in directly observing and quantifying the...

Reef-building corals are surrounded by complex microenvironments (i.e. concentration boundary layers) that partially isolate them from the ambient seawater. Although the presence of such concentration boundary layers (CBLs) could potentially play a role in mitigating the negative impacts of climate change stressors, their role is poorly understood....

Ocean acidification is a threat to the continued accretion of coral reefs, though some undergo daily fluctuations in pH exceeding declines predicted by 2100. We test whether exposure to greater pH variability enhances resistance to ocean acidification for the coral Goniopora sp. and coralline alga Hydrolithon reinboldii from two sites: one with low...

The Perth Canyon is a prominent submarine valley system in the southeast Indian Ocean that incises the southwest Australian continental shelf. It is characterised by two main steep-sided valleys forming a V-shaped configuration that extend from a depth of ~600m to the abyssal plain at ~4000m. Despite its prominence and location of only ~27 nautical...

Trace element abundances in corals can potentially provide high-resolution seasonally resolved constraints on past sea-surface temperatures, much needed to improve our understanding of climate variability on interannual to centennial time scales. A major limitation to the general application of trace element (TE) paleo-thermometers to coral fossil...

Ocean acidification (OA) is a major threat to marine ecosystems, particularly coral reefs which are heavily reliant on calcareous species. OA decreases seawater pH and calcium carbonate saturation state (Ω), and increases the concentration of dissolved inorganic carbon (DIC). Intense scientific effort has attempted to determine the mechanisms via w...

High-latitude coral reefs provide natural laboratories for investigating themechanisms andlimits of coral calcification. While the calcification processes of tropical corals have been studied intensively, little is known about how their temperate counterparts grow under much lower temperature and light conditions. Here, we report the results of a l...

The isotopic and elemental systematics of boron in aragonitic coral skeletons have recently been developed as a proxy for the carbonate chemistry of the coral extracellular calcifying fluid. With knowledge of the boron isotopic fractionation in seawater and the B/Ca partition coefficient (KD) between aragonite and seawater, measurements of coral sk...

Ocean acidification threatens the persistence of biogenic calcium carbonate (CaCO3) production on coral reefs. However, some coral genera show resistance to declines in seawater pH, potentially achieved by modulating the chemistry of the fluid where calcification occurs.We use two novel geochemical techniques based on boron systematics and Raman sp...

The isotopic and elemental systematics of boron in aragonitic coral skeletons have recently been developed as a proxy for the carbonate chemistry of the coral extracellular calcifying fluid. With knowledge of the boron isotopic fractionation in seawater and the B / Ca partition coefficient (KD) between aragonite and seawater, measurements of coral...

Tropical reef systems are transitioning to a new era in which the interval between recurrent bouts of coral bleaching is too short for a full recovery of mature assemblages. We analyzed bleaching records at 100 globally distributed reef locations from 1980 to 2016. The median return time between pairs of severe bleaching events has diminished stead...

The boron isotopic composition (δ¹¹B) of scleractinian corals has been used to track changes in seawater pH and more recently as a probe into the processes controlling bio-calcification. For corals that precipitate aragonite skeletons, up-regulation of pH appears to be a general characteristic, typically being ~0.3 to ~0.6 pH units higher than ambi...

Ocean acidification (OA) is a pressing threat to reef-building corals, but it remains poorly understood how coral calcification is inhibited by OA and whether corals could acclimatize and/or adapt toOA. Using a novel geochemical approach, we reconstructed the carbonate chemistry of the calcifying fluid in two coral species using both a pH and disso...

Evaluating the factors responsible for differing species-specific sensitivities to declining seawater pH is central to understanding the mechanisms via which ocean acidification (OA) affects coral calcification. We report here the results of an experiment comparing the responses of the coral Acropora yongei and Pocillopora damicornis to differing p...

The concentrations and δ³⁴S values of thioaromatic compounds of a suite of oils from several major oil fields in Kurdistan and their corresponding regional Type II-S source rocks have been measured to investigate their source relationship. The oils of three fields (Khabbaz, Jambur, Ajeel) and the bitumen extracted from specific rock formations (Ala...

Quantifying the saturation state of aragonite (ΩAr) within the calcifying fluid of corals is critical for understanding their biomineralisation process and sensitivity to environmental changes including ocean acidification. Recent advances in microscopy, microprobes, and isotope geochemistry allow determination of calcifying fluid pH and [CO32−], b...

Quantifying the saturation state of aragonite (ΩAr) within the calcifying fluid of corals is critical for understanding their biomineralization process and sensitivity to environmental changes including ocean acidification. Recent advances in microscopy, microprobes, and isotope geochemistry enable the determination of calcifying fluid pH and [CO32...

In 2015/16, a marine heatwave associated with a record El Niño led to the third global mass bleaching event documented to date. This event impacted coral reefs around the world, including in Western Australia (WA), although WA reefs had largely escaped bleaching during previous strong El Niño years. Coral health surveys were conducted during the au...

Coral calcification is dependent on both the supply of dissolved inorganic carbon (DIC) and the up-regulation of pH in the calcifying fluid (cf). Using geochemical proxies (δ 11 B, B/Ca, Sr/Ca, Li/Mg), we show seasonal changes in the pH cf and DIC cf for Acropora yongei and Pocillopora damicornis growing in-situ at Rottnest Island (32°S) in Western...

In contrast to Li/Ca and Mg/Ca, Li/Mg is strongly anticorrelated with temperature in aragonites precipitated by the benthic foraminifer Hoeglundina elegansand a wide range of scleractinian coral taxa. We propose a simple conceptual model of biomineralization that explains this pattern and is consistent with available abiotic aragonite partition coe...

The ~251 Ma ago Permian/Triassic (P-Tr) extinction was the most severe of the Phanerozoic extinctions, with a disappearance of 95 % of marine species (e.g. Erwin et al., 2002) over a relatively short time interval (~60 ± 48 kyr; Burgess et al., 2014). Still, no consensus about the causes exists, with the most popular explanations including i) massi...

Molluscs incorporate negligible uranium into their skeleton while they are living, with any uranium uptake occurring post-mortem. As such, closed-system U-series dating of molluscs is unlikely to provide reliable age constraints for marine deposits. Even the application of open-system U-series modelling is challenging, because uranium uptake and lo...

Coral calcification is dependent on the mutualistic partnership between endosymbiotic zooxanthellae and the coral host. Here, using newly developed geochemical proxies (λ¹¹B and B/Ca), we show that Porites corals from natural reef environments exhibit a close (r² ~0.9) antithetic relationship between dissolved inorganic carbon (DIC) and pH of the c...

Seawater (blue) and coral calcifying fluid parameters (orange). DIC = Dissolved Inorganic Carbon. pH*cf and G* are expected calcifying fluid (cf) pH and calcification rates (G) from fixed condition experimental calibrations (pH*cf = 0.32pHsw + 5.2). See manuscript for more details.

Severe, global-scale thermal stress events like those of 1998 and 2016, are becoming more frequent and intense, potentially compromising the future of coral reefs. Here we report the effects of the 1998 bleaching event on coral calcification as well as the composition of the calcifying fluid (cf) from which corals precipitate their calcium carbonat...

Hydropyrolysis (HyPy) of S-containing oil mature rock samples from two geologic settings each produced much higher concentrations of organosulfur compounds (OSCs) compared to their free occurrence in the bitumen. The δ³⁴S values of the most abundant OSCs from the kerogen and in the bitumen, were measured by gas chromatography inductively coupled pl...

Coralline algae provide important ecosystem services but are susceptible to the impacts of ocean acidification. However, the mechanisms are uncertain, and the magnitude is species specific. Here, we assess whether species-specific responses to ocean acidification of coralline algae are related to differences in pH at the site of calcification withi...

During 2015-2016, record temperatures triggered a pan-tropical episode of coral bleaching, the third global-scale event since mass bleaching was first documented in the 1980s. Here we examine how and why the severity of recurrent major bleaching events has varied at multiple scales, using aerial and underwater surveys of Australian reefs combined w...

During the summer of 2010/11, a regional marine heat wave resulted in coral bleaching of variable severity along much of the western coastline of Australia. At Ningaloo Reef, a 300km long fringing reef system and World Heritage site, highly contrasting coral bleaching was observed between two morphologically distinct nearshore reef communities loca...

We present high precision (TIMS double spike) stable isotope measurements of both δ44/40Ca and δ88/86Sr together with radiogenic ⁸⁷Sr/⁸⁶Sr ratios determined from conodont apatite. These data represent five intervals ranging from the early Ordovician to late Triassic. The conodont δ44/40Ca values (relative to NIST 915a) range from − 0.47‰ to + 0.15‰...

High-latitude cold-water coral (CWC) reefs are particularly susceptible due to enhanced CO2 uptake in these regions. Using precisely dated (U/Th) CWCs (Lophelia pertusa) retrieved during research cruise POS 391 (Lopphavet 70.6°N, Oslofjord 59°N) we applied boron isotopes (δ11B), Ba/Ca, Li/Mg and U/Ca ratios to reconstruct the environmental boundary...

The Ca isotopic composition (δ44/40Ca) in a Porites spp. coral from the Great Barrier Reef was analyzed at monthly intervals for two consecutive years. It was found that variations in skeletal δ44/40Ca values over the 2-year period are slightly greater than the analytical precision of the measurements, although other coralline geochemical records (...

Rising atmospheric CO2 is causing the oceans to both warm and acidify, which could reduce the calcification rates of corals globally. Successful coral recruitment and high rates of juvenile calcification are critical to the replenishment and ultimate viability of coral reef ecosystems. Although elevated PCO2 (partial pressure of CO2) has been shown...

This study investigated the impacts of acidified seawater (pCO2 900 µatm) and elevated water temperature (+3 °C) on the early life history stages of Acropora spicifera from the subtropical Houtman Abrolhos Islands (28°S) in Western Australia. Settlement rates were unaffected by high temperature (27 °C, 250 µatm), high pCO2 (24 °C, 900 µatm), or a c...

Naturally extreme temperature environments can provide important insights into the processes underlying coral thermal tolerance. We determined the bleaching resistance of Acropora aspera and Dipsastraea sp. from both intertidal and subtidal environments of the naturally extreme Kimberley region in northwest Australia. Here tides of up to 10 m can c...

Marine Isotope Stage 11 (MIS 11) from ∼424,000 to 374,000 yrs ago included one of the longest and warmest interglacials of the last 800,000 yrs, and is a potential analogue for the Holocene due to the similarity of Earth's orbital configuration at this time. The question of how the El Niño–Southern Oscillation (ENSO) responds to warmer background c...

Increasing intensity of marine heatwaves has caused widespread mass coral bleaching events, threatening the integrity and functional diversity of coral reefs. Here we demonstrate the role of inter-ocean coupling in amplifying thermal stress on reefs in the poorly studied southeast Indian Ocean (SEIO), through a robust 215-year (1795–2010) geochemic...

Supplementary Figures 1-16, Supplementary Tables 1-9 and Supplementary References.

Significance In situ free ocean CO 2 enrichment (FOCE) experiments and geochemical analyses (δ ¹¹ B, Sr/Ca) conducted on corals ( Porites cylindrica ) from the highly dynamic Heron Island reef flat of the Great Barrier Reef show that this species exerts strong physiological controls on the pH of their calcifying fluid (pH cf ). Over an ∼6-mo period...

This study investigated the impacts of acidified seawater (pCO2 ~900 \muatm) and elevated water temperature (+3\circC) on the early life history stages of Acropora spicifera from the sub-tropical Houtman Abrolhos Islands (28\circS), in Western Australia. Settlement rates were unaffected by high temperature (27\circC, ~250 \muatm), high pCO2 (24\cir...

We report seasonal changes in coral calcification within the highly dynamic intertidal and subtidal zones of Cygnet Bay (16.5°S, 123.0°E) in the Kimberley region of northwest Australia, where the tidal range can reach nearly 8 m and the temperature of nearshore waters ranges seasonally by ~9 °C from a minimum monthly mean of ~22 °C to a maximum of...

Waters south of the Polar Front in the high latitude Southern Ocean become undersaturated with respect to aragonite and calcite, strongly limiting carbonate accumulation and preservation. Cold-water corals are among the few calcifying organisms that can cope with this corrosive environment and can, therefore, represent good candidates for the recon...

palaeo‑environmental reconstructions from coral archives, relevant for understanding Australian climate extremes. The key issues for advancing this field are the need for high-resolution marine paleoclimate records to place the present in the context of past natural climate and sea level change, and to understand the impact of those changes on mari...

The response of Acropora digitifera to ocean acidification is determined using geochemical proxy measurements of the skeletal composition of A. digitifera cultured under a range of pH levels. We show that the chemical composition (δ11B, Sr/Ca, Mg/Ca, and Ba/Ca) of the coral skeletons can provide quantitative constraints on the effects of seawater p...

The boron isotopic (δ11Bcarb) compositions of long-lived Porites coral are used to reconstruct reef-water pH across the central Great Barrier Reef (GBR) and assess the impact of river runoff on inshore reefs. For the period from 1940 to 2009, corals from both inner- and mid-shelf sites exhibit the same overall decrease in δ11Bcarb of 0.086 ± 0.033‰...

To assess the viability of high latitude environments as coral refugia, we report measurements of seasonal changes in seawater parameters (temperature, light, and carbonate chemistry) together with calcification rates for two coral species, Acrop-ora yongei and Pocillopora damicornis from the southernmost geographical limit of these species at Salm...

The boron isotopic (δ11Bcarb) compositions of long-lived Porites coral are used to reconstruct reef-water pH across the central Great Barrier Reef (GBR) and assess the impact of river runoff on inshore reefs. For the period from 1940 to 2009, corals from both inner- and mid-shelf sites exhibit the same overall decrease in δ11Bcarb of 0.086 ± 0.033‰...

Scleractinian or 'reef building' corals represent an interesting case of a biomineral with remarkable mechanical properties accreting a tough exoskeleton composed of biopolymers and an aragonite mineral phase. Understanding the origins of this toughness from a materials science perspective is of great interest in the context of current efforts in t...

Palaeoclimate research relevant to marine systems in Australia includes the collection and analysis of: (a) shallow-water and deep-sea corals, which provide highresolution archives, (b) deep-sea sediment and ice cores, which span longer time scales, and (c) palaeoclimate modelling, which gives us insights into mechanisms, dynamics and thresholds un...

The pace of revolution in analytical chemistry in the field of Geosciences has been dramatic over the recent decades and includes fundamental developments that have become common place in many related and unrelated disciplines. The analytical tools (nano to macro-scale from stable to radioactive isotopes to synchrotron imaging) used have been appli...

Rationale: The isotopic composition and elemental abundance of boron (B) in marine carbonates provide a powerful tool for tracking changes in seawater pH and carbonate chemistry. Progress in this field has, however, been hampered by the volatile nature of B, its persistent memory, and other uncertainties associated with conventional chemical extra...

Coral skeletal boron isotopes have been established as a proxy for seawater pH, yet it remains unclear if and how this proxy is affected by seawater temperature. Specifically, it has never been directly tested whether coral bleaching caused by high water temperatures influences coral boron isotopes. Here we report the results from a controlled blea...

It is always difficult to write about the premature departure of a brilliant colleague and a generous friend as such was Sergio to all of us. Driven by an insatiable curiosity for the sea and its infinite mysteries, Sergio graduated in geological sciences in 1995 with a PhD from the University La Sapienza of Rome, with a dissertation on geomorpholo...

Sampling of annually banded massive coral skeletons at annual (or higher) resolutions is increasingly being used to obtain replicate long-term time series of changing seawater conditions. However, few of these studies have compared and calibrated the lower annual resolution records based on coral geochemical tracers with the corresponding instrumen...

Compound-specific isotope analysis (CSIA) has been extended to the ^(32)S and ^(34)S stable isotopes of sulfur (δ^(34)S) through the combination of gas chromatography (GC) and multi-collector inductively coupled mass spectrometry (ICPMS). The molecular level resolution of sulfur-CSIA is greatly expanding the biogeochemical applications of existing...

The pace of revolution in analytical chemistry in the field of Geosciences has been dramatic over the recent decades and includes fundamental developments that have become common place in many related and unrelated disciplines. The analytical tools (nano to macro-scale from stable to radioactive isotopes to synchrotron imaging) used have been appli...

We examined the seasonal and spatial variability in the temperatures of nearshore reef waters over 19 months across Coral Bay at Ningaloo Reef, Western Australia. Local deviations in the mean daily temperature of nearshore reef waters from offshore values (dT) were a linear function of the combined effect of net atmospheric heating (Qnet) and offsh...

Ocean acidification driven by rising levels of CO2 impairs calcification, threatening coral reef growth. Predicting how corals respond to CO2 requires a better understanding of how calcification is controlled. Here we show how spatial variations in the pH of the internal calcifying fluid (pHcf) in coral (Stylophora pistillata) colonies correlates w...

We show that the Li/Mg systematics of a large suite of aragonitic coral skeletons, representing a wide range of species inhabiting disparate environments, provides a robust proxy for ambient seawater temperature. The corals encompass both zooxanthellate and azooxanthellate species (Acropora sp., Porites sp., Cladocora caespitosa, Lophelia pertusa,...

Variability of the Leeuwin current (LC) off Western Australia is a footprint of interannual and decadal climate variations in the tropical Indo-Pacific. La Niña events often result in a strengthened LC, high coastal sea levels and unusually warm sea surface temperatures (SSTs), termed Ningaloo Niño. The rarity of such extreme events and the respons...

Ocean acidification driven by rising levels of CO2 impairs calcification, threatening coral reef growth. Predicting how corals respond to CO2 requires a better understanding of how calcification is controlled. Here we show how spatial variations in the pH of the internal calcifying fluid (pHcf) in coral (Stylophora pistillata) colonies correlates w...

Calcification rates are reported for 41 long-lived Porites corals from 7 reefs, in an inshore to offshore transect across the central Great Barrier Reef (GBR). Over multi-decadal timescales, corals in the mid-shelf (1947–2008) and outer reef (1952–2004) regions of the GBR exhibit a significant increase in calcification of 10.9 ± 1.1 % (1.4 ± 0.2 %...

The biogenic structures of stationary organisms can be effective recorders of environmental fluctuations. These proxy records of environmental change are preserved as geochemical signals in the carbonate skeletons of scleractinian corals and are useful for reconstructions of temporal and spatial fluctuations in the physical and chemical environment...

We investigate how local atmospheric conditions and hydrodynamic forcing contributed to local variations in water temperature within a fringing coral reef-lagoon system during the peak of a marine heat wave in 2010-2011 that caused mass coral bleaching across Western Australia. A three-dimensional circulation model ROMS (Regional Ocean Modeling Sys...

Pacific Ocean sea surface temperatures (SST) influence rainfall variability on multidecadal and interdecadal timescales in concert with the Pacific Decadal Oscillation (PDO) and Interdecadal Pacific Oscillation (IPO). Rainfall variations in locations such as Australia and North America are therefore linked to phase changes in the PDO. Furthermore,...

We present a three-dimensional hydrodynamic-biogeochemical model of a wave-driven coral-reef lagoon system using the circulation model ROMS (Regional Ocean Modeling System) coupled with the wave transformation model SWAN (Simulating WAves Nearshore). Simulations were used to explore the sensitivity of water column carbonate chemistry across the ree...

Derivation of wave setup formulation. (DOC)