Coral recruits are highly sensitive to heavy fuel oil exposure both in the presence and absence of UV light

Oil pollution remains a prominent local hazard to coral reefs, but the sensitivity of some coral life stages to oil exposure remains unstudied. Exposure to ultraviolet radiation (UVR), ubiquitous on coral reefs, may significantly increase oil toxicity towards these critical habitat-forming taxa. Here we present the first data on the sensitivity of two distinct post-settlement life stages of the model coral species Acropora millepora to a heavy fuel oil (HFO) water accommodated fraction (WAF) in the absence and presence of UVR. Assessment of lethal and sublethal endpoints indicates that both 1-week-old and 2-month-old recruits (1-wo and 2-mo) were negatively affected by chronic exposures to HFO (7 and 14 days, respectively). Relative growth (1-wo and 2-mo recruits) and survival (1-wo recruits) at end of exposure were the most sensitive endpoints in the absence of UVR, with no effect concentrations (NEC) of 34.3, 5.7 and 29.3 μg L-1 total aromatic hydrocarbons (TAH; ∑39 monocyclic- and polycyclic aromatic hydrocarbons), respectively. On average, UVR increased the negative effects by 10% for affected endpoints, and latent effects of exposure were evident for relative growth and symbiont uptake of recruits. Other sublethal endpoints, including maximum quantum yield and tissue colour score, were unaffected by chronic HFO exposure. A comparison of putative species-specific sensitivity constants for these ecologically relevant endpoints, indicates A. millepora recruits may be as sensitive as the most sensitive species currently included in oil toxicity databases. While the low intensity UVR only significantly increased the negative effects of the oil for one endpoint, the majority of endpoints showed trends towards increased toxicity in the presence of UVR. Therefore, the data presented here further support the standard incorporation of UVR in oil toxicity testing for tropical corals

Thermal and herbicide tolerances of chromerid algae and their ability to form a symbiosis with corals

Reef-building corals form an obligate symbiosis with photosynthetic microalgae in the family Symbiodiniaceae that meet most of their energy requirements. This symbiosis is under threat from the unprecedented rate of ocean warming as well as the simultaneous pressure of local stressors such as poor water quality. Only 1°C above mean summer sea surface temperatures (SSTs) on the Great Barrier Reef (GBR) can trigger the loss of Symbiodiniaceae from the host, and very low concentrations of the most common herbicide, diuron, can disrupt the photosynthetic activity of microalgae. In an era of rapid environmental change, investigation into the assisted evolution of the coral holobiont is underway in an effort to enhance the resilience of corals. Apicomplexan-like microalgae were discovered in 2008 and the Phylum Chromerida (chromerids) was created. Chromerids have been isolated from corals and contain a functional photosynthetic plastid. Their discovery therefore opens a new avenue of research into the use of alternative/additional photosymbionts of corals. However, only two studies to-date have investigated the symbiotic nature of Chromera velia with corals and thus little is known about the coral-chromerid relationship. Furthermore, the response of chromerids to environmental stressors has not been examined. Here we tested the performance of four chromerid strains and the common dinofiagellate symbiont Cladocopium goreaui (formerly Symbiodinium goreaui, ITS2 type C1) in response to elevated temperature, diuron and their combined exposure. Three of the four chromerid strains exhibited high thermal tolerances and two strains showed exceptional herbicide tolerances, greater than observed for any photosynthetic microalgae, including C. goreaui. We also investigated the onset of symbiosis between the chromerids and larvae of two common GBR coral species under ambient and stress conditions. Levels of colonization of coral larvae with the chromerid strains were low compared to colonization with C. goreaui. We did not observe any overall negative or positive larval fitness effects of the inoculation with chromerid algae vs. C. goreaui. However, we cannot exclude the possibility that chromerid algae may have more important roles in later coral life stages and recommend this be the focus of future studies

The effects of ultraviolet radiation and climate on oil toxicity to coral reef organisms – a review

Oil pollution remains a significant local threat to shallow tropical coral reef environments, but the environmental conditions typical of coral reefs are rarely considered in oil toxicity testing and risk assessments. Here we review the effects of three environmental co-factors on petroleum oil toxicity towards coral reef organisms, and show that the impacts of oil pollution on coral reef taxa can be exacerbated by environmental conditions commonly encountered in tropical reef environments. Shallow reefs are routinely exposed to high levels of ultraviolet radiation (UVR), which can substantially increase the toxicity of some oil components through phototoxicity. Exposure to UVR represents the most likely and harmful environmental co-factor reviewed here, leading to an average toxicity increase of 7.2-fold across all tests reviewed. The clear relevance of UVR co-exposure and its strong influence on tropical reef oil toxicity highlights the need to account for UVR as a standard practice in future oil toxicity studies. Indeed, quantifying the influence of UVR on toxic thresholds of oil to coral reef species is essential to develop credible oil spill risk models required for oil extraction developments, shipping management and spill responses in the tropics. The few studies available indicate that co-exposure to elevated temperature and low pH, both within the range of current daily and seasonal fluctuations and/or projected under continued climate change, can increase oil toxicity on average by 3.0- and 1.3-fold, respectively. While all three of the reviewed environmental co-factors have the potential to substantially increase the impacts of oil pollution in shallow reef environments, their simultaneous effects have not been investigated. Assessments of the combined effects of oil pollution, UVR, temperature and low pH will become increasingly important to identify realistic hazard thresholds suitable for future risk assessments over the coming century

Simulated coal spill causes mortality and growth inhibition in tropical marine organisms

Coal is a principal fossil fuel driving economic and social development, and increases in global coal shipments have paralleled expansion of the industry. To identify the potential harm associated with chronic marine coal contamination, three taxa abundant in tropical marine ecosystems (the coral Acropora tenuis, the reef fish Acanthochromis polyacanthus and the seagrass Halodule uninervis) were exposed to five concentrations (0–275 mg coal l−1) of suspended coal dust (<63 μm) over 28 d. Results demonstrate that chronic coal exposure can cause considerable lethal effects on corals, and reductions in seagrass and fish growth rates. Coral survivorship and seagrass growth rates were inversely related to increasing coal concentrations (≥38 mg coal l−1) and effects increased between 14 and 28 d, whereas fish growth rates were similarly depressed at all coal concentrations tested. This investigation provides novel insights into direct coal impacts on key tropical taxa for application in the assessment of risks posed by increasing coal shipments in globally threatened marine ecosystems

Settlement of larvae from four families of corals in response to a crustose coralline alga and its biochemical morphogens

Healthy benthic substrates that induce coral larvae to settle are necessary for coral recovery. Yet, the biochemical cues required to induce coral settlement have not been identified for many taxa. Here we tested the ability of the crustose coralline alga (CCA) Porolithon onkodes to induce attachment and metamorphosis, collectively termed settlement, of larvae from 15 ecologically important coral species from the families Acroporidae, Merulinidae, Poritidae, and Diploastreidae. Live CCA fragments, ethanol extracts, and hot aqueous extracts of P. onkodes induced settlement (>10%) for 11, 7, and 6 coral species, respectively. Live CCA fragments were the most effective inducer, achieving over 50% settlement for nine species. The strongest settlement responses were observed in Acropora spp.; the only non-acroporid species that settled over 50% were Diploastrea heliopora, Goniastrea retiformis, and Dipsastraea pallida. Larval settlement was reduced in treatments with chemical extracts compared with live CCA, although high settlement (>50%) was reported for six acroporid species in response to ethanol extracts of CCA. All experimental treatments failed (< 10%) to induce settlement in Montipora aequituberculata, Mycedium elephantotus, and Porites cylindrica. Individual species responded heterogeneously to all treatments, suggesting that none of the cues represent a universal settlement inducer. These results challenge the commonly-held notion that CCA ubiquitously induces coral settlement, and emphasize the critical need to assess additional cues to identify natural settlement inducers for a broad range of coral taxa

Climate change doubles sedimentation-induced coral recruit mortality

Coral reef replenishment is threatened by global climate change and local water-quality degradation, including smothering of coral recruits by sediments generated by anthropogenic activities. Here we show that the ability of Acropora millepora recruits to remove sediments diminishes under future climate conditions, leading to increased mortality. Recruits raised under future climate scenarios for fourteen weeks (highest treatment: +1.2 °C, pCO2: 950 ppm) showed twofold higher mortality following repeated sediment deposition (50% lethal sediment concentration LC50: 14–24 mg cm−2) compared to recruits raised under current climate conditions (LC50: 37–51 mg cm−2), depending on recruit age at the time of sedimentation. Older and larger recruits were more resistant to sedimentation and only ten-week-old recruits grown under current climate conditions survived sediment loads possible during dredging operations. This demonstrates that water-quality guidelines for managing sediment concentrations will need to be climate-adjusted to protect future coral recruitment

Effects of climate change and light limitation on coral recruits

Climate change impacts and light attenuation from suspended sediments due to runoff, natural resuspension or dredging, can both impede the replenishment of coral populations. Here we tested the independent and combined impacts of climate change (current temperature and dissolved CO2, and two future climate scenarios) and a one-month-long light attenuation period at 5 different light levels (0.1 to 4 mol photons m−2 d−1) on early Acropora millepora recruits. Additionally, we evaluated whether the effects were age dependent by comparing responses of recruits that were one-month-old (‘early attenuation’) vs two months old (‘late attenuation’). Recruit survival, size and Symbiodiniaceae densities increased slightly under moderate future climate conditions (current temperature +0.44°C, 692 ppm pCO2), but decreased under a more severe climate scenario (+0.94°C, 985 ppm pCO2). Light attenuation significantly decreased recruit survival, size and Symbiodiniaceae densities only for recruits exposed to the late attenuation, suggesting an increasing reliance on photosynthesis as recruits age. Under the more severe climate scenario tested, recruit survival was diminished by both climate change (≤ 18 ± 4 [SE]% in the early attenuation) and light limitation (≤ 32 ± 6% in the late attenuation) compared with controls. However, there was no interaction between future climate scenarios and light attenuation indicating these effects were additive. This study demonstrates the potential effects of light limitation and future climate conditions on coral recruitment success and highlights the need to manage the timing of sediment-generating activities near reefs to optimise light availability for several months post-settlement

Comparative sensitivity of the early life stages of a coral to heavy fuel oil and UV radiation

During an oil spill, shallow, tropical coral reefs are likely to be simultaneously exposed to high intensities of ultraviolet radiation (UVR), which can exacerbate the toxicity of petroleum oils. While successful recruitment of corals is critical for reef recovery following disturbances, the sensitivity of several early life stages of coral to petroleum hydrocarbons has not been investigated, particularly for UVR co-exposure. Here we present the first dataset on the relative sensitivity of three early life stages (gametes, embryos and planula larvae) in a model broadcast spawning coral species, Acropora millepora, to the dissolved fraction of a heavy fuel oil (HFO), both in the absence and presence of UVR. All early life stages were negatively impacted by HFO exposure but exhibited distinct sensitivities. Larval metamorphosis was the most sensitive endpoint assessed with a 10% effect concentration of 34 μg L−1 total aromatic hydrocarbons (TAH) in the absence of UVR. The impact on fertilisation success was highly dependent on sperm density, while the fragmentation of embryos masked embryo mortality. Larval metamorphosis was conclusively the most reliable endpoint for use in risk assessments of the endpoints investigated. Putative critical target lipid body burdens (CTLBBs) were calculated for each life stages, enabling a comparison of their sensitivities against species in the Target Lipid Model (TLM) database. A. millepora had a putative CTLBB of 4.4 μmol g−1 octanol for larval metamorphosis, indicating it is more sensitive than any species currently included in the TLM database. Coexposure to UVR reduced toxicity thresholds by 1.3-fold on average across the investigated life stages and endpoints. This increase in sensitivity in the presence of UVR highlights the need to incorporate UVR co-exposure (where ecologically relevant) when assessing oil toxicity thresholds, otherwise the risks posed by oil spills to shallow coral reefs are likely to be underestimated

Cumulative effects of suspended sediments, organic nutrients and temperature stress on early life history stages of the coral Acropora tenuis

Coral reproduction is vulnerable to both declining water quality and warming temperatures, with simultaneous exposures likely compounding the negative impact of each stressor. We investigated how early life processes of the coral Acropora tenuis respond to increasing levels of suspended sediments in combination with temperature or organic nutrients. Fertilization success and embryo development were more sensitive to suspended sediments than to high temperatures or nutrient enrichment, while larval development (after acquisition of cilia) and settlement success were predominantly affected by thermal stress. Fertilization success was reduced 80% by suspended sediments, and up to 24% by temperature, while the addition of nutrients to suspended sediments had no further impact. Larval survivorship was unaffected by any of these treatments. However, settlement success of larvae developing from treatment-exposed embryos was negatively affected by all three stressors (e.g. up to 55% by suspended sediments), while exposure only during later larval stages predominantly responded to temperature stress. Environmentally relevant levels of suspended sediments and temperature had the greatest impacts, affecting more processes than the combined impacts of sediments and nutrients. These results suggest that management strategies to maintain suspended sediments at low concentrations during coral spawning events will benefit coral recruitment, especially with warming climate

Phototoxic effects of PAH and UVA exposure on molecular responses and developmental success in coral larvae

Exposure to polycyclic aromatic carbons (PAHs) poses a growing risk to coral reefs due to increasing shipping and petroleum extraction in tropical waters. Damaging effects of specific PAHs can be further enhanced by the presence of ultraviolet radiation, known as phototoxicity. We tested phototoxic effects of the PAHs anthracene and phenanthrene on larvae of the scleractinian coral Acropora tenuis in the presence and absence of UVA (320–400 nm). Activity of superoxide dismutase (SOD) enzyme was reduced by anthracene while phenanthrene and UVA exposure did not have any effect. Gene expression of MnSod remained constant across all treatments. The genes Catalase, Hsp70 and Hsp90 showed increased expression levels in larvae exposed to anthracene, but not phenanthrene. Gene expression of p53 was upregulated in the presence of UVA, but downregulated when exposed to PAHs. The influence on stress-related biochemical pathways and gene expresson in A. tenuis larvae was considerably greater for anthracene than phenanthrene, and UVA-induced phototoxicity was only evident for anthracene. The combined effects of UVA and PAH exposure on larval survival and metamorphosis paralleled the sub-lethal stress responses, clearly highlighting the interaction of UVA on anthracene toxicity and ultimately the coral's development