Marine Pollution Bulletin xxx (2015) xxx–xxx Contents lists available at ScienceDirect Marine Pollution Bulletin journal homepage: www.elsevier.com/locate/marpolbul Responses of benthic foraminifera to the 2011 oil spill in the Bohai Sea, PR China ⇑ Yan Li Lei a, Tie Gang Li a, , Hongsheng Bi b, Wen Lin Cui c, Wen Peng Song c,JiYeLic, Cheng Chun Li a a Department of Marine Organism Taxonomy & Phylogeny, Key Laboratory of Marine Geology and Environment, Institute of Oceanology, Chinese Academy of Sciences, Qingdao 266071, PR China b Chesapeake Biological Laboratory, University of Maryland Center for Environmental Science, Solomon, MD 20688, USA c The Organization of North China Sea Monitoring Center, SOA, PR China article info abstract Article history: The 2011 oil spill in the Bohai Sea was the largest spill event in China. Nine sediment cores were taken Received 5 October 2014 near the spill site and environmental factors including Polycyclic Aromatic Hydrocarbon (PAHs), oils, sul- Revised 12 May 2015 fides, organic carbon were measured 6 months later. Benthic foraminifera were separated into >150 lm Accepted 12 May 2015 (large) and 63–150 lm (small) size fractions for 2-cm depth interval of each sediment core. Statistical Available online xxxx analyses suggested that the species composition of living foraminifera was impacted by oils, PAHs and sulfides. Large foraminifera were more sensitive to the oils than the small. Abnormal specimens were Keywords: positively correlated with oils or PAHs. Small forms, however, tended to have high reproduction and mor- Benthic foraminifera tality. Pollution-resistant and opportunistic taxa were identified to calculate a Foraminiferal Index of Biological response Ecological monitoring Environmental Impacts (FIEI). The FIEI increased from low to high oil-polluted station and from deep Indicator species layer to surface sediment reflects the impact of oil pollution in this area. The Yellow Sea Ó 2015 The Authors. Published by Elsevier Ltd. This is an open access article under the CC BY license (http:// creativecommons.org/licenses/by/4.0/). 1. Introduction oil and 2620 barrels (416 m3) of mineral oil-based drilling mud seeping into the Bohai Sea (http://www.soa.gov.cn/) and yet very Oil spills have a wide range of adverse impacts on the marine few studies have examined the potential environmental impact. environment at different temporal scales (Peterson, 2001). They The Bohai Sea is a half-closed sea and is only connected with the can have dire consequences on the survival of marine flora and Yellow Sea through the Bohai Strait. The residence water in the fauna including ecological and economically important fish and Bohai Sea has a mean age of >1.2–3.9 years (Liu et al., 2012). To mammals (Brody et al., 1996; Murphy et al., 1997; Wiens et al., examine and assess the potential impact of the ‘‘Penglai’’ oil spill 1996) and affect marine organisms by disrupting reproduction on the local marine environment, we investigated the potential (Andres, 1997; Lamont et al., 2012), development of using benthic foraminifera as biotic indicators. (Gonzalez-Doncel et al., 2008; Incardona et al., 2014), and feeding Benthic organisms are used extensively as biotic indicators of (Romero et al., 2012). Besides the direct impacts on marine organ- environment because they generally have limited mobility and isms and their habitats, the toxic substances can also affect human cannot avoid adverse environmental changes. Benthic foraminifera health through food webs (Aguilera et al., 2010; Gin et al., 2001; are particularly useful for environmental monitoring (Frontalini O’Rourke and Connolly, 2003). There is a large body of literature and Coccioni, 2011; Hallock et al., 2003; Foster et al., 2012). First, on large oil spills such as the 1978 ‘‘Amoco Cadiz’’ spill in France they are widely distributed and very diverse. Second, they can pre- (Dauvin, 1998; Mille et al., 1998), the 1989 ‘‘Exxon Valdez’’ spill serve historical information in their shells (>500 million years) in Alaska (Atlas and Hazen, 2011; Harwell et al., 2010; Payne which can be used to study the marine environments from ancient et al., 2008; Peterson, 2001) and the 2010 ‘‘Deepwater Horizon’’ (Cambrian) to present (Holocene). Therefore, their species compo- spill in the Gulf of Mexico (Kurtz, 2013; Lavrova and Kostianoy, sition and chemical elements reflect palaeoenvironment (Spero 2011). The 2011 ‘‘Penglai’’ oil spill in the Bohai Sea was the worst et al., 1997; Li et al., 2009; Nigam et al., 2009). Third, they are sen- oil spill in China. There were approximately 723 barrels (115 m3)of sitive to changes in marine environments such as water tempera- ture, salinity, pH, water mass, ocean current, marine geographical variables (Murray, 1991, 2006). Furthermore, their shells preserved ⇑ Corresponding author. at different depths in sediment can reflect environmental changes E-mail address: [email protected] (T.G. Li). including oil exploitation activities (Denoyelle et al., 2010; Sabean http://dx.doi.org/10.1016/j.marpolbul.2015.05.020 0025-326X/Ó 2015 The Authors. Published by Elsevier Ltd. This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/). Please cite this article in press as: Lei, Y.L., et al. Responses of benthic foraminifera to the 2011 oil spill in the Bohai Sea, PR China. Mar. Pollut. Bull. (2015), http://dx.doi.org/10.1016/j.marpolbul.2015.05.020 2 Y.L. Lei et al. / Marine Pollution Bulletin xxx (2015) xxx–xxx et al., 2009), which is particularly useful when no baseline data river runoff (Fig. 1). There are 16 rivers entering the Bohai Sea were available. including the Yellow River. The average residence time water in Previous studies showed that foraminifera could serve as biotic the Bohai Sea is 3 years (Liu et al., 2012). Current from the indicators to evaluate the impacts of oil spills (Casey et al., 1980; Yellow Sea entered the Bohai Sea from the bay mouth and flowed Armynot du Châtelet et al., 2004). Durrieu et al. (2006) and west towards inner Bay. The dominant circulation pattern is anti- Mojtahid et al. (2006) showed that benthic foraminifera could be clockwise (Chen, 2009). used to estimate the pollution from oil drill mud disposal. The Bohai Sea has significant hydrocarbon deposits and offshore However, Locklin and Maddocks (1982) found no negative effects oil exploration started in 1980s. The ‘‘Penglai’’ field is that biggest of petroleum operations on benthic foraminifera on the southwest oil field in this region, which is 51% owned by the China National Louisiana shelf. Offshore Oil Corporation (CNOOC), and 49% owned by the The general responses of benthic foraminifera to pollutants ConocoPhillips (COPC). The exploration of the ‘‘Penglai’’ Oilfield include decreased diversity and increased dominance of tolerant started in 1999 and the operation started on December 31, 2002. or opportunistic species, or alteration of species morphology and From June to July in 2011, at least two major leaks events occurred reproduction, but different species may show differential response. in the ‘‘Penglai’’ Oilfield, which became the largest oil spill accident For example, Morvan et al. (2004) conducted a laboratory culture in China. experiment and observed morphological abnormalities of benthic foraminifera (Ammonia tepida) and a reduction of reproduction rate 2.2. Sampling under oil pollution. But Ernst et al. (2006) found that the mortality of foraminiferal faunas increased in response to the presence of oils Nine sediment cores with a depth of 22–28 m to the surface in a laboratory microcosm experiment, but some species did were sampled on December 18–19, 2011 in the Bohai Sea (38°100 increase their density by increasing their reproduction. Although -39°000N, 119°300–120°10E). The locations of the oil spill and sam- the toxic hydrocarbon components appeared to be responsible pling sites were shown in Fig. 1. For detecting the impact of oil pol- for the observed changes in foraminiferal abundance and species lution, the sediments near the oil spill site were intensively composition (Armynot du Châtelet and Debenay, 2010; Mojtahid sampled. Station 14 was closest to the spill site, followed by et al., 2006), species-specific responses to environmental stress St22, St36, St31, St11, St19 and St6. Station 26 was furthest away induced by oil pollution were evident. Considering the from the spill site and was considered as a reference site. StA8 bio-geographical distribution of foraminifera and the different was considered as an intermediate station. Sediment samples were habitat may colonize different foraminiferal community domi- taken using a 0.1 m2 Gray–Ohara box corer. At each sampling sta- nated by different species, the foraminiferal responses to the oil tion, environmental variables (water depth, sediment type, sedi- pollution should vary among different foraminiferal communities ment color) and pollution factors including Polycyclic aromatic from different geographical regions. hydrocarbons (PAHs), oils, sulfides and organic carbon were mea- When compared to other regions, e.g., the temperate Atlantic sured from the surface sediment (Table 1). Sediment grain size regions (e.g. Brunner et al., 2013; Hallock et al., 2003), there is a analysis was based on Shepard (1954). The measurements for the lack of studies on monitoring and assessing environmental impact chemical contaminants of the sediments were based on the of oil spills using benthic foraminifera in the Western Pacific Chinese National Standards of GB/T 18668-2002 and GB/T region, Chinese continental shelf in particular (Li et al., 2009; Jian 17378.5-2007. et al., 2000). As offshore drilling increases, there is a growing need The sampled sediment cores were subsampled using a recently to identify suitable indicator species and develop local indices that developed Pushing-type Quantitative Layering Sampler with an could be used to assess environmental conditions. While there inner diameter of 6 cm, i.e., 28.26 cm2 sampling surface (Fig.