Craig Humphrey

Natural volcanic CO2 seeps reveal future trajectories for host-microbial associations in corals and sponges

Atmospheric carbon dioxide (CO2) levels are rapidly rising causing an increase in the partial pressure of CO2 (pCO2) in the ocean and a reduction in pH known as ocean acidification (OA). Natural volcanic seeps in Papua New Guinea expel 99% pure CO2 and thereby offer a unique opportunity to explore the effects of OA in situ. The corals Acropora millepora and Porites cylindrica were less abundant and hosted significantly different microbial communities at the CO2 seep than at nearby control sites <500 m away. A primary driver of microbial differences in A. millepora was a 50% reduction of symbiotic Endozoicomonas. This loss of symbiotic taxa from corals at the CO2 seep highlights a potential hurdle for corals to overcome if they are to adapt to and survive OA. In contrast, the two sponges Coelocarteria singaporensis and Cinachyra sp. were ∼40-fold more abundant at the seep and hosted a significantly higher relative abundance of Synechococcus than sponges at control sites. The increase in photosynthetic microbes at the seep potentially provides these species with a nutritional benefit and enhanced scope for growth under future climate scenarios (thus, flexibility in symbiosis may lead to a larger niche breadth). The microbial community in the apparently pCO2-sensitive sponge species S. massa was not significantly different between sites. These data show that responses to elevated pCO2 are species-specific and that the stability and flexibility of microbial partnerships may have an important role in shaping and contributing to the fitness and success of some hosts.

A bioindicator system for water quality on inshore coral reefs of the Great Barrier Reef

Responses of bioindicator candidates for water quality were quantified in two studies on inshore coral reefs of the Great Barrier Reef (GBR). In Study 1, 33 of the 38 investigated candidate indicators (including coral physiology, benthos composition, coral recruitment, macrobioeroder densities and FORAM index) showed significant relationships with a composite index of 13 water quality variables. These relationships were confirmed in Study 2 along four other water quality gradients (turbidity and chlorophyll). Changes in water quality led to multi-faceted shifts from phototrophic to heterotrophic benthic communities, and from diverse coral dominated communities to low-diversity communities dominated by macroalgae. Turbidity was the best predictor of biota; hence turbidity measurements remain essential to directly monitor water quality on the GBR, potentially complemented by our final calibrated 12 bioindicators. In combination, this bioindicator system may be used to assess changes in water quality, especially where direct water quality data are unavailable.

Temporal dynamics in coral bioindicators for water quality on coastal coral reefs of the Great Barrier Reef

There is a need to identify effective coral bioindicators that provide quantifiable links between changes in water quality and the condition of coastal coral reefs. Temporal variation in a range of coral bioindicators including symbiont density, concentration of chlorophyll a, skeletal density and colony brightness of Pocillopora damicornis, as well as colony brightness and density of macro-bioeroders of massive Porites spp. was examined for 2 years on a coastal coral reef of the Great Barrier Reef. The specificity to changes in water quality varied among bioindicators. For example, a 2.5-fold variation in symbiont density of P. damicornis was related strongly to mean 14-day sea surface temperature and seasonal changes in water quality, suggesting medium specificity to changes in water quality. In contrast, the density of macro-bioeroders in Porites did not vary seasonally but there were consistently more macro-bioeroders at the coastal than mid-shelf reference locations, suggesting high specificity of spatial differences in water quality. In situ measurements of benthic irradiance and turbidity allowed the quantification of potential stress thresholds for coastal corals. Our data suggest long-term turbidity >3 NTU leads to sublethal stress, whereas long-term turbidity >5 NTU corresponds to severe stress effects on corals at shallow depths.

Near‐future ocean acidification causes differences in microbial associations within diverse coral reef taxa

Microorganisms form symbiotic partnerships with a diverse range of marine organisms and can be critical to the health and survival of their hosts. Despite the importance of these relationships, the sensitivity of symbiotic microbes to ocean acidification (OA) is largely unknown and this needs to be redressed to adequately predict marine ecosystem resilience in a changing climate. We adopted a profiling approach to explore the sensitivity of microbes associated with coral reef biofilms and representatives of three ecologically important calcifying invertebrate phyla [corals, foraminifera and crustose coralline algae (CCA)] to OA. The experimental design for this study comprised four pHs consistent with current IPCC predictions for the next few centuries (pHNIST 8.1, 7.9, 7.7, 7.5); these pH/pCO₂ conditions were produced in flow-through aquaria using CO₂ bubbling. All reduced pH/increased pCO₂ treatments caused clear differences in the microbial communities associated with coral, foraminifera, CCA and reef biofilms over 6 weeks, while no visible signs of host stress were detected over this period. The microbial communities of coral, foraminifera, CCA and biofilms were significantly different between pH 8.1 (pCO₂ = 464 μatm) and pH 7.9 (pCO₂ = 822 μatm), a concentration likely to be exceeded by the end of the present century. This trend continued at lower pHs/higher pCO₂. 16S rRNA gene sequencing revealed variable and species-specific changes in the microbial communities with no microbial taxa consistently present or absent from specific pH treatments. The high sensitivity of coral, foraminifera, CCA and biofilm microbes to OA conditions projected to occur by 2100 is a concern for reef ecosystems and highlights the need for urgent research to assess the implications of microbial shifts for host health and coral reef processes.

Chemical and physical environmental conditions underneath mat- and canopy-forming macroalgae, and their effects on understorey corals.

Disturbed coral reefs are often dominated by dense mat- or canopy-forming assemblages of macroalgae. This study investigated how such dense macroalgal assemblages change the chemical and physical microenvironment for understorey corals, and how the altered environmental conditions affect the physiological performance of corals. Field measurements were conducted on macroalgal-dominated inshore reefs in the Great Barrier Reef in quadrats with macroalgal biomass ranging from 235 to 1029 g DW m−2 dry weight. Underneath mat-forming assemblages, the mean concentration of dissolved oxygen was reduced by 26% and irradiance by 96% compared with conditions above the mat, while concentrations of dissolved organic carbon and soluble reactive phosphorous increased by 26% and 267%, respectively. The difference was significant but less pronounced under canopy-forming assemblages. Dissolved oxygen declined and dissolved inorganic carbon and alkalinity increased with increasing algal biomass underneath mat-forming but not under canopy-forming assemblages. The responses of corals to conditions similar to those found underneath algal assemblages were investigated in an aquarium experiment. Coral nubbins of the species Acropora millepora showed reduced photosynthetic yields and increased RNA/DNA ratios when exposed to conditions simulating those underneath assemblages (pre-incubating seawater with macroalgae, and shading). The magnitude of these stress responses increased with increasing proportion of pre-incubated algal water. Our study shows that mat-forming and, to a lesser extent, canopy-forming macroalgal assemblages alter the physical and chemical microenvironment sufficiently to directly and detrimentally affect the metabolism of corals, potentially impeding reef recovery from algal to coral-dominated states after disturbance. Macroalgal dominance on coral reefs therefore simultaneously represents a consequence and cause of coral reef degradation.

Does Trophic Status Enhance or Reduce the Thermal Tolerance of Scleractinian Corals? A Review, Experiment and Conceptual Framework

Global warming, and nutrient and sediment runoff from coastal development, both exert increasing pressures on coastal coral reefs. The objective of this study was to resolve the question of whether coastal eutrophication may protect corals from thermal stress by improving their nutritional status, or rather diminish their thermal tolerance through the synergy of dual stressors. A review of previous studies on the topic of combined trophic status and heat exposure on the thermal tolerance of corals reveals a broad range of outcomes, including synergistic, additive and antagonistic effects. We conducted a 90-day long experiment exposing corals to realistic levels of elevated nutrients and sediments, and heat stress. Colonies of two common scleractinian corals (Acropora millepora and Montipora tuberculosa) were kept in coastal seawater, or coastal seawater that was further organically and nutrient enriched (OE), and/or enriched with nitrate. Batches of OE were created daily, facilitating nutrient uptake, plankton succession and organic enrichment as observed in coastal waters. After 10 days of acclimation, 67% of the colonies had their temperature gradually increased from 27° to 31.2°C. After 3–7 weeks of heat stress, colonies of both species had significantly greater reductions in fluorescence yields and lower survival in OE than without addition of OE. Furthermore, photophysiological recovery was incomplete 31–38 days after ending the heat stress only in the OE treatments. Nitrate alone had no measurable effect on survival, bleaching and recovery in either species. Skeletal growth rates were reduced by 45% in heat-stressed A. millepora and by 24% in OE-exposed M. tuberculosa. We propose a conceptual trophic framework that resolves some of the apparently contradictory outcomes revealed by the review. Our study shows that management actions to reduce coastal eutrophication can improve the resistance and resilience of vulnerable coastal coral reefs to warming temperatures.

Investigation of the mud crab (Scylla serrata) as a potential bio-monitoring species for tropical coastal marine environments of Australia

Mud crabs, Scylla serrata, were sampled from four estuaries (the Normanby, Herbert, Burdekin and Fitzroy Rivers) along the coast of northern Queensland, Australia, representing a pollution gradient from low to high contamination based upon previous chemical monitoring. Four biomarkers; glutathione-S-transferase (GST) activity, cholinesterase (ChE) inhibition and the urinary metabolite concentrations of naphthalene (NPH) and benzo-a-pyrene (BaP) were evaluated in S. serrata hepatopancreas, haemolymph and urine. Site-specific evidence of elevated GST activity and BaP metabolite concentrations and significant ChE inhibition was detected. Biomarker responses from this field study provide evidence of contaminant exposure of S. serrata from river estuaries along the coast of northern Queensland and indicate that further investigation is warranted. Based on the current results, and with further work on characterising the dose-response and seasonal variation in this species, mud crabs have great potential as indicator species for water quality and ecosystem monitoring programs across tropical coastal regions of Australia.

Early development and growth of the eastern rainbowfish, Melanotaenia splendida splendida (Peters). I. Morphogenesis and ontogeny

This paper describes the ontogeny and morphogenesis of the eastern rainbowfish, Melanotaenia splendida splendida, including details on reproduction and the conditions required for laboratory breeding and rearing. M. s. splendida is easily bred under standard laboratory conditions using readily available commercial foods. Aquaria with two males and three females can produce between 40 and 200 eggs daily. They can be induced to spawn daily throughout the year through manipulation of light and temperature conditions. The eggs, which ranged in size from 0.93 to 1.20 mm, had a homogeneous yolk and a clear, uniform chorion, making observation of developmental stages possible. Development was telolecithical and division was meroblastic. Development of M. s. splendida was similar to that of other Melanotaenia species. At 28°C, hatching occurred between 4 and 8 days, with an average larval length of 3.7 mm standard length. Growth was rapid and the fish reached sexual maturity within approximately 90 days. Knowledge of the developmental stages of M. s. splendida is important in enabling further work, such as bioassays and environmental monitoring, to be carried out, investigating the ways in which changes in the environment, such as pollution, will impact on Australias freshwater fishes. Melanotaenia splendida splendida is an ideal species for this purpose in the north-eastern tropics of Australia.

Early development and growth of the eastern rainbowfish, Melanotaenia splendida splendida (Peters). II. Otolith development, increment validation and larval growth

A method of preparing and interpreting the microstructure of otoliths of the eastern rainbowfish, Melanotaenia splendida splendida, was developed and used to validate the periodicity of increment formation. Otoliths were collected from laboratory-reared M. s. splendida of known age. The sagittal otolith was preferred for ageing because resolving the earliest increments was easier than in the lapillus during an early slow-growth period, up to 15 days after hatching. Increments formed in the sagittae before hatching, and a distinct discontinuity was visible in the otolith sections at a time corresponding to hatching. Another discontinuity occurred at the time of yolk-sac absorption, when larvae became completely reliant on exogenous feeding. After this, increments were clear, regularly spaced and easily resolved. Linear relationships were found between fish size and sagittal length, breadth and perimeter. Observations of the otolith sections confirmed that the increments in sagittae of M. s. splendida were laid down daily. The information provided here enables growth and mortality rates of M. s. splendida to be measured, providing a useful tool for monitoring the impacts of contaminants in tropical Australian waters.

Expression of calcification and metabolism-related genes in response to elevated pCO2 and temperature in the reef-building coral Acropora millepora.

Declining health of scleractinian corals in response to deteriorating environmental conditions is widely acknowledged, however links between physiological and functional genomic responses of corals are less well understood. Here we explore growth and the expression of 20 target genes with putative roles in metabolism and calcification in the branching coral, Acropora millepora, in two separate experiments: 1) elevated pCO2 (464, 822, 1187 and 1638 μatm) and ambient temperature (27°C), and 2) elevated pCO2 (490 and 822 μatm) and temperature (28 and 31 °C). After 14 days of exposure to elevated pCO2 and ambient temperatures, no evidence of differential expression of either calcification or metabolism genes was detected between control and elevated pCO2 treatments. After 37 days of exposure to control and elevated pCO2, Ubiquinol-Cytochrome-C Reductase Subunit 2 gene (QCR2; a gene involved in complex III of the electron chain transport within the mitochondria and critical for generation of ATP) was significantly down-regulated in the elevated pCO2 treatment in both ambient and elevated temperature treatments. Overall, the general absence of a strong response to elevated pCO2 and temperature by the other 19 targeted calcification and metabolism genes suggests that corals may not be affected by these stressors on longer time scales (37 days). These results also highlight the potential for QCR2 to act as a biomarker of coral genomic responses to changing environments.