Spatiotemporal variations of inorganic nutrients along the Jiangsu coast, China, and the occurrence of macroalgal blooms (green tides) in the southern Yellow Sea

Abstract

Large macroalgal blooms (i.e. green tides of Ulva prolifera) occurred in the southern Yellow Sea, China, yearly from 2007 to 2016. They were among the largest of such outbreaks around the world, and these blooms likely originated along the coast of the Jiangsu Province, China. Understanding the roles of nutrients in the onset of these macroalgal blooms is needed to identify their origin. This study analyzes the spatiotemporal variations in dissolved inorganic nitrogen and phosphorus (DIN and PO₄–P) and the N/P ratio along the Jiangsu coast from 1996 to 2014 during late-March to April, the months which corresponds to the pre-bloom period of green tides since 2007. A zone of high DIN and PO₄–P concentrations has developed along the Jiangsu coast, between the cities of Sheyang and Nantong, since 1996. There was an 18-year trend of increasing DIN concentrations during the pre-bloom period as well as a positive correlation between the U. prolifera biomass and DIN concentrations. Nutrient inputs from rivers and mariculture in the Jiangsu Province may have provided nitrogen that contributed the magnitude of macroalgal blooms that subsequently spread into the southern Yellow Sea.

Introduction

Blooms of green macroalgae are occurring worldwide, and can have large negative ecological and economic impacts (Choi et al., 2006, Guidone and Thornber, 2013, Smetacek and Zingone, 2013, Hu et al., 2014, Perrot et al., 2014). These blooms are commonly associated with coastal eutrophication caused by inputs of nutrients (Valiela et al., 1997, Morand and Merceron, 2004, Ye et al., 2011, Jiang et al., 2014, Li et al., 2014a), such as nitrogen (N) and phosphorus (P) resulting from rapid human population growth, excessive agricultural fertilization, intensive mariculture, and other anthropogenic perturbations (Glibert et al., 2006, Heisler et al., 2008, Zhou et al., 2008), but not inputs of silicon. Based on nutrient enrichment experiments conducted in Maui (Hawaii, USA), Dailer et al. (2012) found a correlation between macroalgal blooms and increased nutrient concentrations. Nelson et al. (2003) also indicated the strong positive correlation between ulvoid algal biomass and additional anthropogenic N concentrations in the coastal waters of Washington State (USA), and showed that high nutrient supply had a crucial role in macroalgal growth. Perrot et al. (2014) reported that massive green-tide events that have recurred annually in Brittany (France) since the 1970s were related to increasing anthropogenic N input. Similar events occurred in the Ios Island, Greece (Tsagkamilis et al., 2010), Biscayne Bay, USA (Collado-Vides et al., 2013), Knysna Estuary, South Africa (Allanson et al., 2016), Narragansett Bay, USA (Conover et al., 2016), and coastal seas of both Korea (Choi et al., 2006) and Japan (Ogawa et al., 2015), where nutrient inputs from adjacent land use and green macroalgal blooms have increased over the past 14 years (i.e. 2003 to present).

Macroalgal blooms in China threatened the 2008 Olympic sailing competition in Qingdao (Jiang et al., 2008) and since 2007 they have occurred annually in the southern Yellow Sea (Fig. 1B,C), with no overall decreasing trend in bloom extent or duration (Liu et al., 2013a, Li et al., 2015, Liu et al., 2016). These macroalgal blooms usually originate in the Jiangsu coastal area during late-April or early May (Wang et al., 2015, Zhou et al., 2015) and start as small patches of floating algae (Liu et al., 2009, Hu et al., 2010), which expand when growth is favorable to large area of the southern Yellow Sea (Fig. 1A). Along the Jiangsu coast, Porphyra mariculture has expanded over a large region between the cities of Yancheng and Nantong since 2006, and covers an area of >20,000 ha where 126,000 t of fresh Porphyra are harvested annually (Liu et al., 2010, Xing et al., 2015). Mariculture activities have rapidly expanded in the Jiangsu province over the last decade (Pang et al., 2010, Wang et al., 2011). In Lianyungang, Yancheng and Nantong, which are three coastal cities of Jiangsu province, there are large coastal areas of mariculture ponds where fish, shrimp and shellfish, are farmed in ponds. The discharge of nutrient-rich wastewater from the intensive mariculture ponds may contribute to eutrophication along the Jiangsu coast (Liu et al., 2013a, Li et al., 2015). Moreover, the main rivers that flow through Jiangsu province, i.e. the Guanhe and Sheyang Rivers, discharge large quantities of inorganic and organic nutrients into coastal areas in the western Yellow Sea (Liu et al., 2013a). This region is characterized by a sand plateau approximately 200 km long and 100 km wide (Keesing et al., 2011), forming an extended intertidal mudflat region along the Jiangsu coast. The combination of this physical environment and the inputs of nutrients and macroalgal propagules creates near-optimal conditions for the development of macroalgal blooms (Wang et al., 2015).

The importance of nutrients for green-tide blooms in the southern Yellow Sea have been previously studied (Li et al., 2015, Shi et al., 2015, Zhou et al., 2015). Li et al. (2015) reported that increased concentrations of dissolved inorganic nitrogen (DIN) may be one of the most important factors contributing to the large extent and long duration of green tides. Nevertheless, the role of nutrients in initiating the green-tide bloom along the Jiangsu coast has not been investigated previously.

The present study addresses the hypothesis that changes in nutrient concentrations of waters along the Jiangsu coast since 2007 are correlated with the initial development of blooms of green tides in the southern Yellow Sea. A combination of published data, for years 1996, 1998, 2001, 2005, 2007, 2010, 2011, 2012 and field-collected information, for years 1997, 2003, 2006, 2008, 2014 were used to examine the relationship between nutrient concentrations and bloom onset for 1996–2014.