Estuarine, Coastal and Shelf Science 207 (2018) 338–344

Contents lists available at ScienceDirect

Estuarine, Coastal and Shelf Science

journal homepage: www.elsevier.com/locate/ecss

Oil spill recorded by skeletal δ13CofPorites corals in Weizhou Island, Beibu T Gulf, Northern South Sea

∗ Shendong Xua,b,c, Kefu Yua,b,c, , Yinghui Wanga,b,c, Tao Liua,b,c, Wei Jianga,b,c, Shaopeng Wanga,b,c, Minghang Chud a Coral Reef Research Centre of China, University, 530004, PR China b Guangxi Laboratory on the Study of Coral Reefs in the , , Nanning 530004, PR China c School of Marine Sciences, Guangxi University, Nanning 530004, PR China d College of Life Science and Technology, Guangxi University, Nanning 530004, PR China

ARTICLE INFO ABSTRACT

Keywords: Oil, is one kind of natural product of biological origin which is depleted in 13C. Coral skeletal δ13C is an im- Oil spill portant archive of environmental and climatic change. However, few studies have been conducted on the effect 13 Coral δ C of oil spill on the coral skeletal δ13C at present. This kind of research is useful for us to obtain environmental and DIC climatic information from coral skeletal δ13C. In this study, two continuously growing Porites corals (W1 and Weizhou island W3), aged 22 and 31 years (1994–2015 and 1985–2015), respectively, were collected from the fringing reef of Northern south China sea Weizhou Island in October 2015, coral skeletal δ13C and δ18O were analyzed. Besides, seawater was collected Since 2008 13 13 during an oil spill in 28 January 2018, and was used for δ CDIC (δ C values of DIC) analysis. The purpose is to 13 13 13 explore the potential impact of oil spills on δ CDIC and coral δ C. δ CDIC value during oil spill was significantly lower than that of normal seawater (Δδ13C≈-2.38‰). Coral δ13C of both two coral colonies showed lower values since 2008 (average value of δ13C before and after 2008 change from −2.04 ± 0.48‰ to −3.33 ± 0.55‰‰ and −1.77 ± 0.49‰ to −2.88 ± 0.54‰ of W1 and W3 respectively), especially, several abrupt negative shifts in 2008, 2009, 2011, 2012 and 2014 when oil spills occurred (extent of δ13C variation were W1：−3.08‰, −1.82‰, −1.82‰, −1.53‰, −1.37‰;W3：−3.27‰, −1.8‰, −1.91‰, −1.21‰, −1.13‰ respectively). Our results clearly show that degradation of oil by microorganisms when oil spill occurs should render a decrease in the 13C/12C ratio of the seawater dissolved inorganic carbon (DIC) which is the ultimate carbon source of coral calcification.

1. Introduction environmental variables, such as light availability, water depth, thermal bleaching, suess effect, river runoff have all been suggested as Coral δ13C of reef coral is widely used as archive of environmental influences on coral skeletal δ13C(Allison et al., 1996; Heikoop et al., and climatic change (Grottoli, 2002; Moyer and Grottoli, 2011; Allison 2000; Grottoli, 2002; Rosenfeld et al., 2003; Dassié et al., 2013; Deng and Finch, 2012; Yu et al., 2012), coral bleaching (Levy, 2006), and can et al., 2013). However, the effect of oil spill on the δ13C of coral ske- also be used as a proxy for land-ocean carbon flux in tropical regions letons has received less detailed attention. Ignorance of the effect of oil (Moyer et al., 2012). But there are some arguments, because control spill may leads to an erroneous interpretation of the environmental and factors of coral skeletal δ13C are varied (McConnaughey, 1989; Swart climatic information contained in coral skeletal δ13C. et al., 1996; McConnaughey et al., 1997; Omata et al., 2008). At the Crude oil is a natural product of biological origin that is strongly cellular scale, DIC in extracellular calcifying fluid (ECF) provide a depleted in 13C, hence its δ13C is characterized by a strongly negative carbon source for carbon precipitated in coral skeletons (Gattuso et al., signature (Aggarwal et al., 1997). Bacteria and microbial biodegrada- 1999). Any biological or environmental factor that might influence δ13C tion present in the oil-polluted seawater are readily able to transform in the sources of inorganic carbon input to the ECF may affect δ13C components of the crude oil into inorganic carbon (Javier et al., 2005). variations recorded in the coral skeleton. Numerous studies have at- Both δ13C and δ18O values of seawater are characterized by a narrow tempted to address the causes of δ13C variations in coral. These pre- range that close to 0‰ (Kroopnick et al., 1972). Therefore, biode- vious studies were focus mainly on the influence of climatic and gradation of crude oil with depleted δ13C by seawater microorganisms

∗ Corresponding author. Coral Reef Research Centre of China, Guangxi University, Nanning 530004, PR China. E-mail address: [email protected] (K. Yu). https://doi.org/10.1016/j.ecss.2018.04.031 Received 14 December 2017; Received in revised form 8 April 2018; Accepted 25 April 2018 Available online 30 April 2018 0272-7714/ © 2018 Elsevier Ltd. All rights reserved. S. Xu et al. Estuarine, Coastal and Shelf Science 207 (2018) 338–344

13 should render a local seawater relatively C-poor CO2 and, as a con- sampling time, and counting backwards in time (Knutson et al., 1972). sequence, a decrease in the 13C/12C ratio of the ambient water DIC. The chronologies were cross-verified by δ18O under the assumption that However, biodegradation of oil components has no effect on δ18Oof each δ18O cycle represents 1 year (Sun et al., 2008). seawater (Javier et al., 2005). In the past few years, this combined Approximately 0.5–1 mg of powdered calcium carbonate was col- characteristics of δ13C and δ18O have been used to assess biodegrada- lected using a surgical blade along the maximum growth axis guided by tion of oil components in natural samples (Jason et al., 2000; Bugna, the annual bands identified in the X-rays. Before collecting the samples, 2004; Javier et al., 2005). Samples for these studies were showing a preliminary milling along the designated sample track was undertaken δ18O (water) rather close to 0‰ but a δ13C (DIC) relatively negative, to remove the upper 1 mm. The powdered samples fell onto a weighing which evidenced typical biodegradation of a very δ13C-negative source, paper placed beneath the coral slab that was then wrapped, with a fixed such as the oil in a marine environment. microsampling interval. Then, these powdered samples were used in Coral skeletal δ13C is susceptible affected by isotopic values of sea instrumental analysis of δ13C and δ18O. water DIC due to external seawater could contribute to the carbon in the ECF used for coral calcification. We thus hypothesized that oil- 2.3. Coral stable isotope analyses polluted seawater with depleted δ13C may affect δ13C variations re- corded in the coral skeleton. However, to date, there has been few re- Coral δ13C and δ18O were measured at the Coral Reef Research 13 13 searches on the possible effect of oil spills on the seawater δ CDIC and Center of China (School of Marine Sciences, Guangxi University). δ C coral δ13C in Weizhou Island, or even the entire northern South China and δ18O analysis were conducted using a Finnigan MAT-253 stable Sea, under the context of increasing oil pollution. isotope mass spectrometer attached to a Fairbanks carbonate prepara-

Weizhou Island in the NSCS is ideally suited for deciphering the tion device. Powdered samples were reacted with 100% H3PO4 at 75 °C 13 influence of oil spills on the coral δ C. Firstly, Weizhou Island is a in an automated carbonate device to extract CO2. Isotopic ratios were volcano that is suitable for coral growth. Coral reefs are distributed reported in the per mil (‰) convention and normalized to the Vienna around the island, there was a great deal of reef-building Porites co- Pee Dee Belemnite (V-PDB) using the GBW04405 standard lonies with continuous growth. As one kind of massive reef-building (δ13C = 0.57‰, δ18O=−8.49‰). Multiple measurements (n = 15) of corals, Porites colonies can provide continuous δ13C and δ18O data with this standard yielded a standard deviation of 0.03% for δ13C, and 0.08% high-resolution over timescales ranging from seasonal to decades for δ18O. In addition, replicate measurements were taken for approxi- (Gagan et al., 2000). The temporal variation of the seawater δ13C mately 20% of all the samples to guarantee the differences between the concentration is continuously recorded in Porites skeletons, through the two measurements were within the range of analytical error. calcification reactions. So high resolution attributes make it can record 13 changes in seawater isotopic values timely and accurately. Secondly, 2.4. Analysis of δ CDIC Weizhou Island has been confronted with increasingly frequent oil spill events and petroleum contamination accompanied by development of Isotope analysis of DIC was performed with 1 ml water sample by tourism and increase in the number of offshore oil platforms since 2008. releasing CO2 via acidification of the sample with H3PO4 (Assayag In the present study, we collected two Porites corals (31 and 22 years in et al., 2006). The process was on a fully automated preparation system age, respectively) from the fringing reef of Weizhou Island, northern with online headspace sampling (Gas Bench) followed by isotopic SCS. The coral skeletal δ13C, δ18O were analyzed. We investigated the analysis using an IRMS (Delta V Advantage). The analytical precision 13 13 change trend of δ C. Our intention is to examine whether the oil spills for δ CDIC analysis was ± 0.2‰. since 2008 perturbed the original carbon isotopic values of the seawater DIC and is reflected in the coral δ13C and then elaborate on the ability 2.5. Climate and environmental parameters of coral δ13C to record oil spill incidents. 13 Data for δ Catm were taken from the Carbon Dioxide Information 2. Materials and methods Analysis Center (http://cdiac.ornl.gov/trends/co2/iso-sio/iso-sio.htm). Solar insolation, rainfall and salinity datas of Weizhou Island was 2.1. Study site downloaded from the National Oceanic and Atmospheric Administration, Physical Sciences Division, Climate and Weather Data Two samples of Porites coral W1 and W3 were collected from (NOAA, PSD, Climate and Weather Data, www.esrl.noaa.gov/psd/data/ Weizhou Island, Beibu Gulf, northern SCS, namely, WI (N21°0′27″, ). PSD archives gridded climate datasets extending hundreds of years at E109°5′4″) and W3 (N21°4′7″, E109°5′24″), at sampling depths of 6 m a single location. These data have been widely used in coral reef eco- and 4 m, respectively. The coral reefs are located close to the northern system monitoring and reef management. The year 2008, 2009, 2011, latitudinal limit of the hermatypic coral distribution of the mainland 2012 and 2014 in which oil spill occurred was inquired from coast of southern China. The sampling locations are shown in Fig. 1. Environmental Bulletin of the Oceanic Administration of Guangxi. Weizhou Island is a volcano with area of 26 km2 and highest elevation of 79 m. It is located in the subtropical monsoon climate zone, and the 3. Results mean annual SST is 24.5 °C, ranging seasonally from < 15 °C in winter to > 30 °C in summer. Over the last 30 years, annual solar insolation The chronologies of the two colonies, W1 and W3, were 22 and 31 intensity ranged between 2390 and 2775 W/m2, with an average of years (1994–2015 and 1985–2015), respectively. 2 13 2541 W/m . As shown in Fig. 6, δ CDIC value during oil spill in January 2018 is 13 −2.34‰ ± 0.44 that is obviously lower than normal sea water δ CDIC 2.2. Age model and coral sampling value (0.04‰ approximately) in the study. As shown in Fig. 3, δ13C of both W1 and W3 showed a negative bias Two colonies of massive Porites were collected at depths of 6 m (W1) before 2002 and then transitioned into a relatively high value stage and 4 m (W3) below mean tide in October 2015. Each coral colony until 2008, at which point a significant negative shift occurred. Since appeared healthy, without any obvious bleaching or disease. In the 2008, δ13C of both W1 and W3 has remained at a more negative level, laboratory, each colony was cut into slabs 8–10 cm wide and 1 cm thick average value of δ13C before and after 2008 change from along the major growth axis by a rock saw, and then they were dried −2.04 ± 0.48‰ to −3.33 ± 0.55‰ and −1.77 ± 0.49‰ to and X-rayed, as shown in Fig. 2. The chronologies of two colonies were −2.88 ± 0.54‰ of W1 and W3 respectively. established by identifying the most surface band deposited at the There have been several abrupt negative shifts of varying degrees

339 S. Xu et al. Estuarine, Coastal and Shelf Science 207 (2018) 338–344

Fig. 1. Location of the coral samples collected (Yellow stars): Weizhou Island, Beibu Gulf, northern South China Sea. (For interpretation of the references to colour in this figure legend, the reader is referred to the Web version of this article.)

decrease. As shown in Fig. 3, coral δ18O of both W1 and W3 showed no sig- nificant variation and sail on through normally in the past 30 years.

4. Discussion

4.1. Potential natural factors that may affect variation of coral skeletal δ13C

Coral obtain carbon for skeletogenesis both directly from the DIC in seawater, and indirectly derived from metabolic respiration inside the coral polyps, although the relative contributions from these two sources remain unknown (Grottoli and Wellington, 1999; Furla et al., 2000; Fig. 2. Photographs and X-radiographs of two coral slabs. The X-radiographs Grottoli, 2002). Any factors such as riverine and rainfall influence, were made on the slabs to identify growth bands. Red lines mark the coral suess effect, SST, solar insolation may change carbon source of sea- maximum growth axis. Sub-samples for geochemical analysis were manually water, metabolic effects of coral symbiosis, and ultimately influence collected from coral slabs with a surgical blade along the maximum growth coral skeletal δ13C. Understand the possible influence of these factors is axis. (For interpretation of the references to colour in this figure legend, the important for us to deciphering the effect of oil spill on coral skeletal reader is referred to the Web version of this article.) δ13C during this period (i.e., in 2009, 2011, 2012, and 2014). As shown in 4.1.1. Salinity variations δ13 13 Fig. 4, the extent of coral C negative shifts of W1 in 2008, 2009, δ CDIC maybe partly attributable to the salinity variations which 2011, 2012 and 2014 were −3.08‰, −1.82‰, −1.82‰, −1.53‰, caused by riverine influence. Deng et al. (2013) pointed out that periods 13 and −1.37‰, respectively; the extent of the coral δ C negative shifts of high rainfall deliver increased amounts of terrestrial 13C-depleted of W3 in 2008, 2009, 2011, 2012 and 2014 were −3.27‰, −1.8‰, DIC to coastal seawater, resulting in an enhanced negative δ13C in the −1.91‰, −1.21‰, and −1.13‰, respectively. corals. This situation usually occurs in the coastal areas with relatively δ13 Catm has shown a downward trend over the past 30 years, de- larger terrestrial river runoff. However, in the study area Weizhou Is- creasing from −7.68‰ in 1985 to −8.51‰ in 2015. Annual rainfall land is relatively far away from the shore, also there is no big river and SST showed no significant variation in the past 30 years. Solar input around it. Besides, the rainfall has remained relatively stable, and insolation increased during 2002–2008, and then began to gradually there is no big fluctuation. So the influence of the river on the salinity

Fig. 3. δ13C and δ18O curves (black and red lines, respec- tively) of two coral cores. The results show that δ13C of both W1 and W3 can be divided into three stages: a steady de- creasing stage before 2002, a relatively high value stage until 2008, and a significant negative bias stage after 2008. Coral δ18O of both W1 and W3 showed no significant var- iation in the past 30 years. The chronologies of the two colonies were established by identifying the most surface band deposited at the sampling time, and counting back- wards in time, and then they were cross-verified by δ18O under the assumption that each δ18O cycle represents 1 year.

340 S. Xu et al. Estuarine, Coastal and Shelf Science 207 (2018) 338–344

Fig. 4. Left: five negative shifts in 2008, 2009, 2011, 2012 and 2014 of W1 and W3. Right: amplitude of negatively shifts.

13 and δ CDIC of the seawater is not great in the study area. As shown in the northern SCS did exhibit this trend (Sun et al., 2008). In this study, Fig. 5, both rainfall and salinity data show no relevance to the theo- coral δ13C has shown a negative bias over the past 30 years, declining 13 retical δ CDIC, especially have nothing to do with several abrupt ne- from −7.68‰ in 1985 to −8.51‰ in 2015. However, the change 13 13 13 gative shifts of coral δ C in 2008, 2009, 2011, 2012 and 2014. trajectories of coral δ C and surface water theoretical δ CDIC (which are assumed to be in isotopic equilibrium with atmospheric CO2 δ13 δ13 4.1.2. The suess effect Catm) are not synchronized. As shown in Fig. 5, theoretical CDIC Since the beginning of the industrial revolution, the δ13C of atmo- exhibits a relatively stable change, however, the change process of coral δ13 spheric CO (δ13C ) has decreased by ∼2‰ due to emissions of 13C- C can be divided into three stages. From 1985 to 2002, the ranges of 2 atm δ13 δ13 depleted CO from human activities, such as fossil fuel burning and land annual average coral C and theoretical CDIC were relatively equal, 2 ff clearing (Druffel and Benavides, 1986). The so-called “13C Suess effect” suggesting that the Suess e ect mainly controlled the change of coral δ13 (Keeling, 1979) also occurs in the surface ocean through air-sea ex- C through changing the carbon isotopic values of seawater during change (Broecker and Maier-Reimer, 1992; Quay et al., 1992; Lynch this period. et al., 1995; Bacastow et al., 1996), which has induced a long-term decrease in coral δ13C(Swart et al., 2010). For example, δ13C records 4.1.3. Solar insolation obtained from three modern corals spanning the past 15–35 years from In most shallow water corals, skeletal δ13C is largely influenced by

Fig. 5. Comparison between coral δ13C and climatic factors curves for the study area over the past 30 years. Green line: surface seawater theoretical 13 δ CDIC, which is assumed to be in isotopic equili- 13 13 brium with atmospheric CO2 δ Catm. δ CDIC was 13 13 calculated as follows: δ CDIC = δ Catm + Ɛ; therein Ɛ = −0.105*T+10.51 where Ɛ is the isotopic frac-

tionation between DIC and gaseous CO2, and T is the annual average SST in the study area (Zhang et al., 1995). Red line: solar insolation. Black line: coral skeletal δ13C (higher than monthly resolution, fluc- tuations represent seasonal variations of δ13C due to metabolic fractionation). Blue line: seawater salinity, and purple line: rainfall. (For interpretation of the references to colour in this figure legend, the reader is referred to the Web version of this article.)

341 S. Xu et al. Estuarine, Coastal and Shelf Science 207 (2018) 338–344

4.2. Oil spill led to abrupt negative shifts of coral skeletal δ13C since 2008

4.2.1. Occurrence of the actual oil spills An oil spill is a common marine pollution incident that may occur during the process of exploitation, storage, transportation, production or consumption of oil. In recent years, Weizhou Island was confronted with increasingly frequent oil spill events and petroleum contamination accompanied by the increase in the number of offshore oil/gas plat- forms. In 16, 23, 27 August 2008, the China National Offshore Oil Corp Weizhou oil field experienced three serious oil spill accidents of crude oil due to the overflow of a waste pipeline. In September, the influence range of the oil spill events extending to the whole coast of Guangxi Province. Black, bulk crude oil were found on the beach in , and . Since then, there have been sev- 13 13 13 Fig. 6. Actual seawater δ CDIC. Gray: δ CDIC without oil spill. Black: δ CDIC eral oil spill accidents with varying degrees of severity in July 2009, 13 during oil spill in January 2018, obviously, they were lower relative to δ CDIC August 2011, September 2012 and May 2014 in Weizhou Island, values of normal seawater. Northern Beibu Gulf, China. In 27 July 2009, an oil zone with a length of five hundred meters and width of ten meters was found offshore west fi metabolic fractionation effects due to changes in photosynthesis (Swart, Weizhou Island. Through identi cation, this oil zone was drift with the fi 1983; Grottoli, 2002; Hartmann et al., 2010). Therein, solar insolation waves from the oil elds in the southwest of Weizhou Island. In 5 fi fl can significantly affect the photosynthesis of coral endosymbiotic August 2011, About six square kilometers of unidenti ed oil oatation zooxanthellae in the shallow water (McConnaughey, 1989). In general, zone was found in the West coast of Weizhou Island. In 16 September fi fi DIC in the ECF plays an important role in the coral–algal symbiotic 2012, No. 88008 shing boat sank due to the re that lead to ten tons of ff community. First, it is fixed by zooxanthellae and then translocated to diesel leakage. Oil spill a ects an area of about 1 square kilometers. In the coral host for the coral's metabolic requirements (Muscatine and 16 May 2014, a cargo ship-Jieanda tilted rollover in western wharf of Weis, 1992). Second, it serves as the carbon source for coral skeleto- Weizhou Island that resulted in dozens of tons of engine cabin fuel genesis. During photosynthesis, zooxanthellae preferentially utilize leakage. Strip oil pollution was found in the western coast of Weizhou forms of DIC that contain the light carbon isotope 12C over the heavier Island. carbon isotope 13C, resulting in 13C enrichment of the DIC in the ECF. fi δ13 This carbon absorption model of zooxanthellae is called metabolic 4.2.2. Signi cant reduction of C of DIC fi fi fractionation (Swart, 1983; McConnaughey, 1989; Muscatine and Weis, In 28 January 2018, a shing boat was red and sunk that lead to 1992; de Carvalho et al., 2015). Therefore, moderate increases in solar tons of diesel leakage in Qiaogang port Beihai city (40 km from ff insolation enhance the duration of photosynthesis, thereby resulting in Weizhou Island). It provides us an opportunity to study the e ect of oil δ13 higher δ13C levels in the coral skeleton, whereas decreases in light re- spill on the C values of DIC directly. In 31 January, we collected δ13 sult in reduced δ13C values in the coral skeleton (Weber et al., 1976; seawater samples in the polluted waters and analyzed C values of δ13 δ13 Weil et al., 1981; Grottoli and Wellington, 1999). As shown in Fig. 5, DIC. These CDIC values are compared with CDIC values of seawater δ13 annual solar insolation began to increase gradually in 2002 and reached that was not contaminated by oil. Datas show that seawater CDIC ‰ a maximum in 2008, corresponding to a period in which coral δ13C was value during oil spill was approximately 2.38 lower than the normal more positive. It is possible that the positive bias in the δ13C preserved seawater, as shown in Fig.6. Arguably, oil spill event have led to the δ13 in the corals between 2002 and 2008 was driven by increase in solar reduction of C values of DIC which may eventually be absorbed by insolation. the coral. However, since 2008 coral δ13C values of both W1 and W3 showed a δ13 higher fractionation and maintained at a more negative level. They 4.2.3. The mechanism of coral C reduction during oil spills δ13 δ18 were significantly more deviating from the theoretical δ13C values Both C and O values of seawater are characterized by a DIC ‰ which was calculated according to atmospheric CO . This high degree narrow range that close to 0 (Kroopnick et al., 1972). Oil spills could 2 δ13 of coral δ13C fractionation can't be caused by the change in intensity of reduce C of seawater. However, biodegradation of oil components ff δ18 light. We speculate that there are two possible reasons for it. has no e ect on O of seawater (Javier et al., 2005). Therefore, coral δ13 δ18 Firstly, the natural illumination intensity are not the light that ac- C showed an obvious negative bias since 2008, while O were not tually impacting the corals. It is closely related to the turbidity of the changed and sail on through normally. δ13 seawater. Indeed, effects of light on coral δ13C is closely related to the Oil spills could lead to a negative bias in coral skeletal C by re- turbidity of the seawater. Increase of turbidity and reduction of visi- ducing the carbon isotopic values of seawater DIC directly. Crude oil is 13 bility is possible to reduce the light that actually impacting the pho- a natural product of biological origin that is depleted in C, hence its δ13 − ‰ tosynthesis intensity of symbiotic zooxanthellaea, ultimately reduce the C is characterized by a strongly negative signature, 28 ap- fi δ13C values of corals (Grottoli and Wellington, 1999). We can't ignore proximately (Aggarwal et al., 1997). Both eld studies and laboratory ffi the increase of turbidity and reduction of visibility caused by a series of simulations indicate that microbial biodegradation is an e cient pro- prolonged incidents of muddy water, or even resuspension. Especially, cess in the decontamination of oil-polluted seawater, and bacteria in the context of the strengthening of human activities in Weizhou Is- present in the contaminated water are readily able to transform com- land that lead to drop in water quality. ponents of the crude oil into inorganic carbon (Javier et al., 2005). In Secondly, we can't ignore that “theoretical DIC δ13C” was not the the process of degradation, carbon isotope discrimination during re- δ13 δ13 actual values that affect coral δ13C ultimately since 2008. Maybe, spiration is small and C values of respired CO2 is closed to the C 13 values of source substance (de Carvalho et al., 2011). For example, in δ CDIC has became more negative due to other factors, such as oil spills. We'll discuss this in next section. the laboratory experiments, labelled aromatic substrates were added and isotopic fractionation was followed in the remaining substrates after degradation and the fractionation levels obtained were generally below 3‰ (Dempster et al., 1997; Meckenstock et al., 1999; Ahad et al., 2000; Javier et al., 2005). The fractionation of 3‰ means that the

342 S. Xu et al. Estuarine, Coastal and Shelf Science 207 (2018) 338–344 original value in the oil (around −28‰) was largely maintained in Foundation of Guangxi (2016GXNSFBA380132), China Postdoctoral 13 respired CO2. Therefore, biodegradation of oil with depleted δ Cby Science Foundation (2016M602613) and the Guangxi Postdoctoral 13 seawater microorganisms should render a local relatively C-poor CO2 special funding. The responsible Editor and two anonymous reviewers and, as a consequence, a decrease in the δ13C values of the ambient are thanked for their valuable comments, which helped us improve water DIC (Velde et al., 1995; Aggarwal et al., 1997; Bolliger et al., significantly our paper. The authors thank Dr. Wei Guo from Jiangxi 13 1999; de Carvalho et al., 2011). Just as our datas showed above, δ CDIC Province Key Laboratory of the Causes and Control of Atmospheric was significantly reduced (Δδ13C≈-2.38‰, as shown in Fig.6) during Pollution, East China University of Technology. Dr. Wei Guo provides 13 oil spill in January 2018. Seawater DIC is the ultimate source of coral δ CDIC datas. The authors also thank Dr. Yuanfu Yue, and Tao Han 13 skeletal carbon, significant changes in seawater δ CDIC can be reflected from the South China Sea Institute of Oceanology, Chinese Academy of in the coral δ13C. Therefore, skeletal δ13CofPorites corals with con- Sciences, for their helpful advices. The data used in this paper can be tinuous growth can record the biodegradation of the crude oil when oil downloaded on the website or requested by emailing Kefu Yu at spills occurred. [email protected]. Oil spill could lead to a negative bias in coral skeletal δ13C, not only by reducing the carbon isotopic values of DIC directly but also by re- References ducing the photosynthetic intensity of symbiotic zooxanthellae. Large amounts of chemical dispersants are used when oil spill occurred in Aggarwal, P.K., Fuller, M.E., Gurgas, M.M., Manning, J.F., Dillon, M.A., 1997. Use of 2008 in order to control the diffusion of crude oil (Environmental stable oxygen and carbon isotope analyses for monitoring the pathways and rates of intrinsic and enhanced in situ biodegradation. Environ. Sci. Technol. 31, 590–596. Bulletin of the Oceanic Administration of Guangxi, 2008). The com- Ahad, J.M.E., Lollar, B.S., Edwards, E.A., Slater, G.F., Sleep, B., 2000. Carbon isotope bined effect of the crude oil plus the dispersant could significantly re- fractionation during anaerobic degradation of toluene: implications for intrinsic duce the intensity of photosynthesis of zooxanthellae through inhibiting bioremediation. Environ. Sci. Technol. 34, 892–896. Allison, N., Finch, A.A., 2012. A high resolution δ13C record in a modern Porites lobata incorporation of photosynthetic products into lipids (Cook et al., 1983). coral: insights into controls on skeletal δ13C. Geochem. Cosmochim. Acta 84, Reef-building corals (e.g., Porites corals) are “fatty” organisms that store 534–542. large amounts of wax esters and triglycerides (Benson et al., 1974, Allison, N., Tudhope, A.W., Fallick, A.E., 1996. Factors influencing the stable carbon and 1978). Most of the carbon fixed in photosynthesis of zooxanthellae is oxygen isotopic composition of Porites lutea coral skeletons from Phuket, South Thailand. Coral Reefs 15 (1), 43–57. incorporated into lipids. Symbiotic zooxanthellae provide a substantial Assayag, N., Rive, K., Ader, M., Jezequel, D., Agrinier, P., 2006. Improved method for- amount of this lipid to corals, either by providing small molecular isotopic and quantitative analysis of dissolved inorganic carbon in natural water- – weight photosynthetic products for coral lipid synthesis or by releasing samples. Rapid Commun. Mass Spectrom. 20, 2243 2251. Bacastow, R.B., Keeling, C.D., Lueker, T.J., Wahlen, M., Mook, W.G., 1996. The 13C Suess whole lipids (Patton et al., 1977; Patton et al., 1983). However, the effect in the world surface oceans and its implications for oceanic uptake of CO2: pathways of photosynthetic products into lipids are significantly af- analysis of observations at Bermuda. Global Biogeochem. Cycles 10, 335–346. fected by exposure to oil and chemical dispersants. Because dispersants Benson, A.A., Muscatine, L., 1974. Wax in coral mucus: energy transfer from corals to reef fishes. Limnol. Oceanogr. 19, 810–814. contain a large number of toxic hydrocarbons, the use of dispersants in Benson, A.A., Patton, J.S., Abraham, S., 1978. Energy exchange in coral reef ecosystems. oil polluted waters could cause increased uptake of toxic hydrocarbons Atoll Res. Bull. 220, 33–54. into coral cells and zooxanthellae, thereby reducing the intensity of Bolliger, C., Hohener, P., Hunkeler, D., Haberli, K., Zeyer, J., 1999. Intrinsic bior- emediation of a petroleum hydrocarbon-contaminated aquifer and assessment of photosynthesis (Cook et al., 1983). Reduced photosynthesis means less mineralization based on stable carbon isotopes. Biodegradation 10, 201–217. 12 12 C in the ECF was utilized by the zooxanthellae, and thus more C was Broecker, W.S., Maier-Reimer, E., 1992. The influence of air and sea exchange on the used for coral skeletogenesis, eventually resulting in a depleted δ13C carbon isotope distribution in the sea. Global Biogeochem. Cycles 6, 315–320. fi Bugna, G.C., Chanton, J.P., Kelley, C.A., Stauffer, T.B., MacIntyre, W.G., Libelo, E.L., signal in the coral skeleton. Thus, the signi cant negative bias of coral 2004. A field test of 13C as a tracer of aerobic hydrocarbon degradation. Org. 13 δ C could be attributed to the use of chemical dispersant when the oil Geochem. 35, 123–135. spill occurred in the summer of 2008, although the relative contribution Cook, C.B., Knap, A.H., 1983. Effects of crude oil and chemical dispersant on photo- – remains unknown. synthesis in the brain coral Diploria strigosa. Mar. Biol. 78, 21 27. Dassié, E.P., Lemley, G.M., Linsley, B.K., 2013. The Suess effect in Fiji coral δ13C and its potential as a tracer of anthropogenic CO2 uptake, Paleogeogr. Paleoclimatol. 5. Conclusions Paleoecol. 370 (0), 30–40. de Carvalho, M.C., Eyre, B.D., 2011. Carbon stable isotope discrimination during re- spiration in three seaweed species. Mar. Ecol. Prog. Ser. 437, 41–49. This study indicate that oil spills could led to abrupt negative shifts de Carvalho, M.C., Santos, I.R., Maher, D.T., Cyronak, T., Mcmahon, A., Schulz, K.G., 13 13 in coral δ C through reducing δ CDIC values and/or by reducing the Eyre, B.D., 2015. Drivers of carbon isotopic fractionation in a coral reef lagoon: – photosynthetic intensity of symbiotic zooxanthellae, although the re- predominance of demand over supply. Geochem. Cosmochim. Acta 153, 105 115. Dempster, H., Lollar, B.S., Feenstra, S., 1997. Tracing organic contaminants in ground- lative contribution of each pathway remains unknown. The skeletal water: a new methodology using compound specific isotopic analysis. Environ. Sci. 13 δ CofPorites coral with continuous growth has the ability to record oil Technol. 31, 3193–3197. spill incidents. The observed shift in δ13C after oil spills in our coral Deng, W.F., Wei, G.J., Xie, L.H., Yu, K.F., 2013. Environmental controls on coral skeletal δ – ff δ13 13C in the northern South China Sea. J. Geophys. Res-Biogeo 118 (4), 1359 1368. samples indicate that e ects of oil spill on coral skeletal C can not be Druffel, E.R.M., Benavides, L.M., 1986. Input of excess CO2 to the surface ocean based on ignored when it was used as index of climatic change, coral bleaching 13C/12C ratios in a banded Jamaican sclerosponge. Nature 321, 58–61. or proxy for land-ocean carbon flux. Although the relative contribution Furla, P., Allemand, D., Orsenigo, M.N., 2000. Involvement of H+- ATPase and carbonic fi anhydrase in inorganic carbon uptake for endosymbiont photosynthesis. Am. J. of oil degradation products to the carbon source of coral calci cation Physiol. Regul. Integr. Comp. Physiol. 278 (4), 870–881. 14 remains unknown. In previous studies, C was used as a tracer for Gagan, M.K., Ayliffe, L.K., Beck, J.W., Cole, J.E., Druffel, E.R.M., Dunbar, R.B., Schrag, petro-carbon contributions to foodwebs. Maybe, two endmember iso- D.P., 2000. New views of tropical paleoclimates from corals. Quat. Sci. Rev. 19 (1–5), – tope mass balance calculations based on the stable carbon isotope δ13C 45 64. Gattuso, J.P., Allemand, D., Frankignoulle, M., 1999. Photosynthesis and calcification at 14 combining radiocarbon (Δ C) could provided quantitative analysis to cellular, organismal and community levels in coral reefs: a review on interactions and evaluate the contributions of oil carbon. control by carbonate chemistry. Am. Zool. 39 (1), 160–183. Grottoli, A.G., 2002. Effect of light and brine shrimp on skeletal δ13C in the Hawaiian coral Porites compressa: a tank experiment. Geochem. Cosmochim. Acta 66 (11), Acknowledgments 1955–1967. Grottoli, A.G., Wellington, G.M., 1999. Effect of light and zooplankton on skeletal δ13C fi This work was financially supported by the National Natural values in the eastern Paci c corals Pavona clavus and Pavona gigantea. Coral Reefs 18 (1), 29–41. Sciences Foundation of China (Grant No. 91428203, 41663001, Hartmann, A.C., Carilli, J.E., Norris, R.D., Charles, C.D., Deheyn, D.D., 2010. Stable 41603091) and National Basic Research Program of China (Grant No. isotopic records of bleaching and endolithic algae blooms in the skeleton of the 2013CB956102). Yu thanks the BaGui Scholars Program Foundation boulder forming coral Montastraea faveolata. Coral Reefs 29, 1079–1089. Heikoop, J.M., Dunn, J.J., Risk, M.J., Schwarcz, H.P., McConnaughey, T.A., Sandeman, (Grant No. 2014BGXZGX03), Xu thanks the support of Natural Sciences

343 S. Xu et al. Estuarine, Coastal and Shelf Science 207 (2018) 338–344

I.M., 2000. Separation of kinetic and metabolic isotope effects in carbon-13 records isotope composition in the coral skeleton: long-term culture of Porites spp. J. preserved in reef coral skeletons. Geochem. Cosmochim. Acta 64 (6), 975–987. Geophys. Res. 113. Jason, M.E.A., Barbaba, S.L., Elizabeth, A.E., Greg, F.S., Brent, E.S., 2000. Carbon isotope Patton, J.S., Abraham, S., Benson, A.A., 1977. Lipogenesis in the intact coral Pocillopora fractionation during anaerobic biodegradation of toluene: implications for intrinsic capitata and its isolated zooxanthellae: evidence for a light-driven carbon cycle be- bioremediation. Environ. Sci. Technol. 34, 892–896. tween host and symbiont. Mar. Biol. 44, 235–247. Javier, I., Medina, B., Patricia, M., Antonio, D., Alicia, R.S., Emilio, R., Juan, L.R., Silvia, Patton, J.S., Battey, J.F., Rigler, M.W., Porter, J.W., Black, C.C., Burris, J.E., 1983. A M., 2005. Evidence for in situ crude oil biodegradation after the Prestige oil spill. comparison of the metabolism of bicarbonate 14C and acetate 14C and the variability Environ. Microbiol. 7 (6), 773–779. of species lipid composition in reef corals. Mar. Biol. 75, 121–130. Keeling, C.D., 1979. The Suess effect: 13Carbon-14Carbon interrelations. Environ. Int. 2, Quay, P., Tilbrook, B., Wong, C.S., 1992. Oceanic uptake of fossil fuel CO2: carbon-13 229–300. evidence. Science 256, 74–79. Knutson, D.W., Buddemeier, R.W., Smith, S.V., 1972. Coral chronometers:Seasonal Rosenfeld, M., Yam, R., Shemesh, A., Loya, Y., 2003. Implication of water depth on stable growth bands in reef corals. Science 177 (4045), 270–272. isotope composition and skeletal density banding patterns in a Porites lutea colony: Kroopnick, P., Weiss, R.F., Craig, H., 1972. Total CO2, δ13C, and dissolved oxygen-δ18O results from a long-term translocation experiment. Coral Reefs 22 (4), 337–345. at GEOSECS II in the north atlantic. Earth Planet Sci. Lett. 16, 103–110. Sun, D., Su, R., McConnaughey, T.A., Bloemendal, J., 2008. Variability of skeletal growth Levy, O., Rosenfeld, M., Yam, R., Shemesh, A., 2006. Heterogeneity of coral skeletons and δ13C in massive corals from the South China Sea: effects of photosynthesis, re- isotopic compositions during the 1998 bleaching event. Limnol. Oceanogr. 51 (2), spiration and human activities. Chem. Geol. 255 (3–4), 414–425. 1142–1148. Swart, P.K., 1983. Carbon and oxygen isotope fractionation in scleractinian corals: a re- Lynch, J., Stocker, T.F., Broecker, W.S., Fairbanks, R.G., 1995. The influence of air-sea view. Earth Sci. Rev. 19 (1), 51–80. exchange on the isotopic composition of oceanic carbon: observations and modeling. Swart, P.K., Leder, J.J., Szmant, A.M., Dodge, R.E., 1996. The origin of variations in the Glob. Biogeochem. Cycles 9, 653–655. isotopic record of scleractinian corals: II. Carbon. Geochem. Cosmochim. Acta 60 McConnaughey, T.A., 1989. 13C and 18O isotopic disequilibrium in biological carbo- (15), 2871–2885. nates: I. Patterns. Geochem. Cosmochim. Acta 53, 151–162. Swart, P.K., Greer, L., Rosenheim, B.E., Moses, C.S., Waite, A.J., Winter, A., Dodge, R.E., McConnaughey, T.A., Burdett, J., Whelan, J.F., Paull, C.H., 1997. Carbon isotopes in Helmle, K., 2010. The 13C Suess effect in scleractinian corals mirror changes in the biological carbonates: respiration and photosynthesis. Geochem. Cosmochim. Acta 61 anthropogenic CO2 inventory of the surface oceans. Geophys. Res. Lett. 37, L05604. (3), 611–622. Velde, K.D., Marley, M.C., Studer, J., Wagner, D.M., 1995. Stable carbon isotope analysis Meckenstock, R.U., Morasch, B., Warthmann, R., Schink, B., Annweiler, E., Michaelis, W., to verify bioremediation and bioattenuation. In: Hinchee, R.E., Douglas, G.S., Ong, Richnow, H.H., 1999. 13C/12C isotope fractionation of aromatic hydrocarbons S.K. (Eds.), Monitoring and Verification of Bioremediation. Batelle Press, Columbus, during microbial degradation. Environ. Microbiol. 1, 409–414. OH, USA, pp. 241–257. Moyer, R.P., Grottoli, A.G., 2011. Coral skeletal carbon isotopes (δ13C and Δ14C) record Weber, J.N., Deines, P., Weber, P.H., Baker, P.A., 1976. Depth related changes in the 13C/ the delivery of terrestrial carbon to the coastal waters of Puerto Rico. Coral Reefs 30 12C ratio of skeletal carbonate deposited by the Caribbean reef-frame building coral (3), 791–802. Montastrea annularis: further implications of a model for stable isotope fractionation Moyer, R.P., Grottoli, A.G., Olesik, J.W., 2012. A multiproxy record of terrestrial inputs to by scleractinian corals. Geochem. Cosmochim. Acta 40, 31–39. the coastal ocean using minor and trace elements (Ba/Ca, Mn/Ca, Y/Ca) and carbon Weil, S.M., Buddemeier, R.W., Smith, S.V., Kroopnick, P.M., 1981. The stable isotopic isotopes (δ13C/Δ14C) in a nearshore coral from Puerto Rico. Paleoceanography 27. composition of coral skeletons: control by environmental variables. Geochem. Muscatine, L., Weis, V., 1992. Productivity of zooxanthellae and biogeochemical cycles. Cosmochim. Acta 45 (7), 1147–1153. In: Falkowski, P.G., Woodhead, A.D., Vivirito, K. (Eds.), Environmental Science Yu, K.F., 2012. Coral reefs in the South China Sea: their response to and records on past Research; Primary Productivity and Biogeochemical Cycles in the Sea. Springer environmental changes. Sci. China Earth Sci. 55, 1217–1229. Verlag, New York, pp. 257–271. Zhang, J., Quay, P.D., Wilbur, D.O., 1995. Carbon isotope fractionation during gaswater Omata, T., Suzuki, A., Sato, T., Minoshima, K., Nomaru, E., Murakami, A., Murayama, S., exchange and dissolution of CO2. Geochem. Cosmochim. Acta 59 (1), 107–114. Kawahata, H., Maruyama, T., 2008. Effect of photosynthetic light dosage on carbon

344