James K. H. Fang

Bioerosion: the other ocean acidification problem

&NA; Bioerosion of calcium carbonate is the natural counterpart of biogenic calcification. Both are affected by ocean acidification (OA). We summarize definitions and concepts in bioerosion research and knowledge in the context of OA, providing case examples and meta‐analyses. Chemically mediated bioerosion relies on energy demanding, biologically controlled undersaturation or acid regulation and increases with simulated OA, as does passive dissolution. Through substrate weakening both processes can indirectly enhance mechanical bioerosion, which is not directly affected by OA. The low attention and expert knowledge on bioerosion produced some ambiguous views and approaches, and limitations to experimental studies restricted opportunities to generalize. Comparability of various bioerosion and calcification rates remains difficult. Physiological responses of bioeroders or interactions of environmental factors are insufficiently studied. We stress the importance to foster and advance high quality bioerosion research as global trends suggest the following: (i) growing environmental change (eutrophication, coral mortality, OA) is expected to elevate bioerosion in the near future; (ii) changes harmful to calcifiers may not be as severe for bioeroders (e.g. warming); and (iii) factors facilitating bioerosion often reduce calcification rates (e.g. OA). The combined result means that the natural process bioerosion has itself become a “stress factor” for reef health and resilience.

The use of muscle burden in rabbitfish Siganus oramin for monitoring polycyclic aromatic hydrocarbons and polychlorinated biphenyls in Victoria Harbour, Hong Kong and potential human health risk

Muscle concentrations of polycyclic aromatic hydrocarbons (PAHs) and polychlorinated biphenyls (PCBs) were determined in rabbitfish Siganus oramin collected from Victoria Harbour and its vicinity, Hong Kong from 2004 to 2007. Spatially, relatively higher levels of [summation operator]PAH (1.05-4.26 microg g(-1)) and [summation operator]PCB (45.1-76.9 ng g(-1)) were determined in the central and western sites inside the harbour. Temporally, upward trend of [summation operator]PAH, accompanied with a proportion shift from high molecular weight to low molecular weight PAHs, was detected during the three-year study period, suggesting a heavier marine traffic in Victoria Harbour and its western region. However, human health risk assessment based on five individual PAHs indicated that PAHs in fish muscles posed minimal health risk through consumption. In contrast, a downward trend of [summation operator]PCB was registered as the open use of PCBs has been banned. Despite this, the level of [summation operator]PCB in fish muscles still posed a health risk on the local people who have a high fish consumption rate. While seasonal influences on [summation operator]PAH/[summation operator]PCB accumulation in S. oramin seemed to be negligible, our findings in S. oramin were in line with the established PAH and PCB levels in sediments and/or mussels from the harbour, suggesting S. oramin can be used as a model fish species for monitoring PAHs and PCBs in the region.

Seasonality of bioaccumulation of trace organics and lysosomal integrity in green-lipped mussel Perna viridis.

Lysosomal integrity in mussels is widely used as a biomarker in coastal environments to demonstrate exposure to trace organic pollutants. However, few studies have determined the long-term influences of seasonal variations on the bioaccumulation of trace organics and subsequently altered response of lysosomal integrity in mussels. This study aimed to test three null hypotheses that (1) bioaccumulations of total polycyclic aromatic hydrocarbon (SigmaPAH) and (2) total polychlorinated biphenyl (SigmaPCB), and (3) lysosomal integrity as indicated by Neutral Red retention time (NRRT) in haemocytes, in the green-lipped mussel Perna viridis were not seasonally dependent. The tissue concentrations of SigmaPAH and SigmaPCB and haemocytic NRRT were determined in P. viridis in a metropolitan harbour, subtropical Hong Kong during the wet and dry seasons from 2004 to 2007. Additional information on temperature, salinity, dissolved oxygen and total ammonia nitrogen in seawater, and sediment levels of SigmaPAH and SigmaPCB, were extracted from published data and re-analyzed. Our results accepted all null hypotheses, based on the minimal seasonal influences of seawater temperature and salinity on all studied parameters, in which no significant differences between the wet and dry seasons were detected. The seasonal effect was likely outweighed by the greatly improved water quality and pollution abatement noted inside the harbour, with a gradual shift in mussel PAHs from a pyrolytic origin to a petrogenic origin. Spatially, the site east of the harbour was relatively unpolluted. The single use of NRRT in P. viridis explained 25% of the total variation of the integrated pollution patterns in seawater, sediments and mussels. The present study suggested that the dynamic change of trace organics could be reflected by the response on lysosomal integrity in P. viridis, which was recommended as a routine screening biomarker in monitoring of harbour water quality across seasons.

Influences of ammonia-nitrogen and dissolved oxygen on lysosomal integrity in green-lipped mussel Perna viridis: Laboratory evaluation and field validation in Victoria Harbour, Hong Kong

Lysosomal integrity in mussels has been applied as a biomarker to detect the pollution of trace organics and metals in the natural environments. However, few studies have examined the effects of water quality on the response of lysosomal integrity, in particular total ammonia-nitrogen (TAN) and dissolved oxygen (DO). This study demonstrated that high level of TAN (2.0mg/l) and low DO (2.5mg O(2)/l) could significantly reduce the lysosomal integrity in green-lipped mussel Perna viridis, respectively by 33% and 38%, whereas the mussel lysosomal integrity decreased by 70% in the combined treatment of TAN and low DO under laboratory conditions after one week. The mussel lysosomal integrity of all treatment groups could return to the control level after a three week recovery period. In the field validation in Victoria Harbour, Hong Kong during an one-year study period, lysosomal integrity in P. viridis identified the cleanest site east to the harbour, where the lowest TAN and highest DO concentrations were found. While lysosomal integrity in mussels seemed not affected by seasonal changes, approximately 40% of the variation of this biomarker could be attributable to the changes in TAN and DO in seawater. In conclusion, the response of the mussel lysosomal integrity can be confounded by both TAN and DO prevailing in the natural environments and thus caution must be exercised in relating the observed changes in lysosomal integrity to any specific pollutant in coastal water quality monitoring studies.

Induction, adaptation and recovery of lysosomal integrity in green-lipped mussel Perna viridis

Biomarkers are generally applied to detect pollution in environmental monitoring. Such biological responses should accurately reflect the stress over time in a quantitative manner. As such, the initial and maximum responses induced by stress, as well as adaptation and recovery of these biomarkers, need to be fully understood or else erroneous false-negative or false-positive may be arrived. However, most of the biomarker studies only provided information on initially induced responses under different concentrations of toxicants, while biological adaptation and recovery were poorly known. In this study, the time required for induction, adaptation and recovery of lysosomal integrity in green-lipped mussel Perna viridis upon exposure to benzo[a]pyrene was investigated over a period of 62 days. Maximum induction occurred on day 6 when lysosomal integrity was significantly reduced by 51%, and no further change or adaptation was detected thereafter. When mussels were depurated in clean seawater after 18 days of exposure to benzo[a]pyrene, a gradual recovery was observed, with lysosomal integrity returning to its background level and showing a complete recovery after 20 days of depuration. Lysosomal integrity was significantly correlated with the body burden concentrations of benzo[a]pyrene and condition index of the mussels. The relatively fast induction (6 days) and recovery (20 days) without apparent adaptation suggested that lysosomal integrity in P. viridis can serve as a good biomarker in biomonitoring, as its response is not likely to generate both false-negative and false-positive results.

Power analysis for biomarkers in mussels for use in coastal pollution monitoring

Data from literature on neutral red retention time (NRRT) in lysosomes, micronucleus (MN) frequency and condition index (CI) in mussel Mytilus, especially Mytilus edulis and Mytilus galloprovincialis, were re-analyzed to ascertain their statistical power in detecting a minimum 20% spatial/temporal change in field studies. Results showed that CI largely displayed higher statistical power (>90%) than lysosomal NRRT and MN frequency (<50%), suggesting that data from the latter two biomarkers may lead to erroneous conclusions if sample size is inadequate. Samples of green-lipped mussel Perna viridis were also analyzed in Hong Kong. To achieve statistically valid power, the optimal sample sizes for monitoring lysosomal NRRT, MN frequency, CI and gonosomatic index (GSI) were determined as >or=34, >or=90, >or=16 and >or=29, respectively. Natural variability of lysosomal NRRT and MN frequency was significantly greater than CI and/or GSI in mussels, rejecting the general belief in the greater variability of higher-tiered hierarchical biomarkers.

Sponge bioerosion on changing reefs: ocean warming poses physiological constraints to the success of a photosymbiotic excavating sponge

Excavating sponges are prominent bioeroders on coral reefs that in comparison to other benthic organisms may suffer less or may even benefit from warmer, more acidic and more eutrophic waters. Here, the photosymbiotic excavating sponge Cliona orientalis from the Great Barrier Reef was subjected to a prolonged simulation of both global and local environmental change: future seawater temperature, partial pressure of carbon dioxide (as for 2100 summer conditions under “business-as-usual” emissions), and diet supplementation with particulate organics. The individual and combined effects of the three factors on the bioerosion rates, metabolic oxygen and carbon flux, biomass change and survival of the sponge were monitored over the height of summer. Diet supplementation accelerated bioerosion rates. Acidification alone did not have a strong effect on total bioerosion or survival rates, yet it co-occurred with reduced heterotrophy. Warming above 30 °C (+2.7 °C above the local maximum monthly mean) caused extensive bleaching, lower bioerosion, and prevailing mortality, overriding the other factors and suggesting a strong metabolic dependence of the sponge on its resident symbionts. The growth, bioerosion capacity and likelihood of survival of C. orientalis and similar photosymbiotic excavating sponges could be substantially reduced rather than increased on end-of-the-century reefs under “business-as-usual” emission profiles.

Ethoxyresorufin-O-deethylase enzyme activities and accumulation of secondary/tertiary lysosomes in rabbitfish Siganus oramin as biomarkers for xenobiotic exposures

The sensitivities of using hepatic and intestinal ethoxyresorufin-O-deethylase (EROD) activities and hepatic accumulation of secondary/tertiary (2 degrees/3 degrees) lysosomes to detect xenobiotic exposures were assessed in the rabbitfish Siganus oramin in a metropolitan harbour, subtropical Hong Kong, over a complete seasonal cycle of one year. Additional information on the body-burden pollutants and physiological indices in S. oramin, and seasonal variables in seawater quality, were extracted from published data and re-analyzed. Under the influences of pollutant cocktail and seasonal factors, neither the hepatic nor intestinal EROD activity was indicative of total polycyclic aromatic hydrocarbons (Sigma PAH), total polychlorinated biphenyls, condition factor and hepatosomatic index (HSI) in S. oramin. However, the relative ratio of hepatic to intestinal EROD activities provided an indication to differentiate the xenobiotic intake route in the fish through diffusion via gills/skin or consumption of contaminated food. In addition, the elevated hepatic accumulation of 2 degrees/3 degrees lysosomes was closely associated with the dominant temporal trends of zinc and Sigma PAH, as well as reduced HSI, in S. oramin. Being minimally influenced by any investigated seasonal factors, the hepatic 2 degrees/3 degrees lysosomes in S. oramin was recommended as an effective biomarker of xenobiotic exposures and toxic effects for use in coastal pollution monitoring programmes.

The response of a boreal deep-sea sponge holobiont to acute thermal stress

Effects of elevated seawater temperatures on deep-water benthos has been poorly studied, despite reports of increased seawater temperature (up to 4 °C over 24 hrs) coinciding with mass mortality events of the sponge Geodia barretti at Tisler Reef, Norway. While the mechanisms driving these mortality events are unclear, manipulative laboratory experiments were conducted to quantify the effects of elevated temperature (up to 5 °C, above ambient levels) on the ecophysiology (respiration rate, nutrient uptake, cellular integrity and sponge microbiome) of G. barretti. No visible signs of stress (tissue necrosis or discolouration) were evident across experimental treatments; however, significant interactive effects of time and treatment on respiration, nutrient production and cellular stress were detected. Respiration rates and nitrogen effluxes doubled in responses to elevated temperatures (11 °C & 12 °C) compared to control temperatures (7 °C). Cellular stress, as measured through lysosomal destabilisation, was 2–5 times higher at elevated temperatures than for control temperatures. However, the microbiome of G. barretti remained stable throughout the experiment, irrespective of temperature treatment. Mortality was not evident and respiration rates returned to pre-experimental levels during recovery. These results suggest other environmental processes, either alone or in combination with elevated temperature, contributed to the mortality of G. barretti at Tisler reef.

Bleaching and mortality of a photosymbiotic bioeroding sponge under future carbon dioxide emission scenarios

The bioeroding sponge Cliona orientalis is photosymbiotic with dinoflagellates of the genus Symbiodinium and is pervasive on the Great Barrier Reef. We investigated how C. orientalis responded to past and future ocean conditions in a simulated community setting. The experiment lasted over an Austral summer under four carbon dioxide emission scenarios: a pre-industrial scenario (PI), a present-day scenario (PD; control), and two future scenarios of combined ocean acidification and ocean warming, i.e., B1 (intermediate) and A1FI (extreme). The four scenarios also simulated natural variability of carbon dioxide partial pressure and temperature in seawater. Responses of C. orientalis generally remained similar between the PI and PD treatments. C. orientalis under B1 displayed a dramatic increase in lateral tissue extension, but bleached and displayed reduced rates of respiration and photosynthesis. Some B1 sponge replicates died by the end of the experiment. Under A1FI, strong bleaching and subsequent mortality of all C. orientalis replicates occurred at an early stage of the experiment. Mortality arrested bioerosion by C. orientalis under B1 and A1FI. Overall, the absolute amount of calcium carbonate eroded by C. orientalis under B1 or A1FI was similar to that under PI or PD at the end of the experiment. Although bioerosion rates were raised by short-term experimental acidification in previous studies, our findings from the photosymbiotic C. orientalis imply that the effects of bioerosion on reef carbonate budgets may only be temporary if the bioeroders cannot survive long-term in the future oceans.