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Palaeoecological Analysis of Phytoplankton Regime Shifts in Response to Coastal Eutrophication

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Palaeoecological Analysis of Phytoplankton Regime Shifts in Response to Coastal Eutrophication Vol. 475: 1–14, 2013 MARINE ECOLOGY PROGRESS SERIES Published February 14 doi: 10.3354/meps10234 Mar Ecol Prog Ser OPENPEN ACCESSCCESS FEATURE ARTICLE Palaeoecological analysis of phytoplankton regime shifts in response to coastal eutrophication Dongyan Liu1,*, Xuhong Shen1,2, Baoping Di1, Yajun Shi1, John K. Keesing1,3, Yujue Wang1, Yueqi Wang1,2 1Key Laboratory of Coastal Zone Environmental Processes, Yantai Institute of Coastal Zone Research, Chinese Academy of Sciences; Shandong Provincial Key Laboratory of Coastal Zone Environmental Processes, 264003, Yantai, Shandong, PR China 2Graduate University of the Chinese Academy of Sciences, 100049, Beijing, PR China 3CSIRO Wealth from Oceans National Research Flagship, Marine and Atmospheric Research, Private Bag 5, Wembley, Western Australia 6913, Australia ABSTRACT: We used a multiple-proxy palaeoeco - logical method to reconstruct a 100 yr time series showing coastal eutrophic processes and phyto- plankton re sponses. Total organic carbon, total nitrogen, diatom frustules, dinoflagellate cysts, brassicasterol and dinosterol were extracted from chronologic sediment cores in Sishili Bay, a pol- luted area in China. The cores showed that eutrophication occurred during about 1975 to 1985, which corresponds to increased human activity associated with China’s economic develop- ment since 1978. During eutrophication, the bio- mass of diatoms and dinoflagellates increased, and dominant species shifted abruptly. The small, heavily silicified diatoms Cyclotella stylorum and Paleoecological methods make it possible to reconstruct Paralia sulcata gradually took the place of the anthropogenic effects such as coastal eutrophication over large dominant diatom Coscinodiscus radiatus, periods of a century. while dinoflagellates displayed a progressive in - Photos: Dongyan Liu & Zhijun Dong crease since 1975. Compared to changes in tem - perature and rainfall during 1950 to 2010, increased fertilizer use, marine aquaculture and sewage discharge showed a better match to the INTRODUCTION increasing trend in biomass, species shift and nutrient concentration. Altered nutrient supply Over recent decades, coastal waters have under- ratios caused by increased nitrogen inputs play gone significant deterioration, much of it due to an important role in the shifts in diatom and dino- anthropogenic eutrophication (de Jonge et al. 2002) flagellate assemblages. and climate change (Harley et al. 2006). Setting a KEY WORDS: Palaeoecology · Eutrophication · target for nutrient reduction requires not only infor- Diatom · Dinoflagellate · Biomarkers mation on nutrient sources, distribution and recy- cling, but also requires knowledge of the trends and Resale or republication not permitted without written consent of the publisher baselines of nutrient concentrations in coastal waters *Email: [email protected] © Inter-Research 2013 · www.int-res.com 2 Mar Ecol Prog Ser 475: 1–14, 2013 (e.g. de Jonge & Essink 1991, Cooper 1995a, Billen & and the 1940s, with major species shifts towards those Garnier 1997, Clarke et al. 2006, Parsons et al. 2006), more tolerant to nutrient enrichment. to determine the effects of anthropogenic activity. Among biological proxies (e.g. diatoms, dinoflagel- Similarly, variations in marine ecosystems responding late cysts, foraminifera, pigments, biomarkers) de - to eutrophication can be identified objectively against posited in the sediment, diatom frustules and dino - the background of long-term environmental changes. flagellate cysts display the best representation of For example, long-term marine observation data anthropogenic activity in coastal lagoons (Andersen (e.g. North Sea, Baltic Sea and Chesapeake Bay) et al. 2004), for several reasons: (1) they are the major have shown that nutrient enrichment can increase primary producers in most marine ecosystems and the incidence of phytoplankton blooms and induce are sensitive to various environmental changes (such a major species shift from diatoms to flagellates at as temperature, salinity and nutrients; e.g. Cooper decadal scales (Hickel et al. 1993, Wasmund 2002, 1995a, Parsons et al. 1999); and (2) their key taxo - Marshall et al. 2009). nomical features, viz. cell walls, are preserved in the In China, a high human population density of sediment distinctly enough to obtain both species >800 ind. km−2 living in coastal areas (Ge & Feng identification and enumeration, and thus to inter- 2009) and rapid economic development since the pret the responses of phytoplankton to environmen- 1978 economic reforms have produced remarkable tal change (e.g. Cooper 1995b, Parsons et al. 2002, anthropogenic impacts along the coastline. Chinese Feifel et al. 2012). However, factors which create coastal eutrophication is characterized by a dramatic uncertainty in the application of diatom frustules and nitrogen overload in the mouths of large rivers (e.g. dinoflagellate cysts have also been found: (1) small Yangtze and Pearl Rivers; Huang et al. 2003, Chai et colony-forming diatoms (<20 μm), which occupy al. 2006) and in coastal waters (e.g. Bohai Sea, Yellow many coastal waters in large proportions, are not Sea; B. Wang et al. 2003, X. Wang et al. 2009). Con- well preserved in the sediment, due to their fragile sequently, high-biomass algal blooms have increased frustules (e.g. Skeletonema costatum,Chaetoceros sp.); significantly in Chinese coastal waters since the thus, the accuracy of identification may be low and 1980s and particularly during the late 1990s (Zhou et enumeration may be underestimated (Battarbee et al. 2001). How ever, it is difficult to track the eutrophi - al. 2001, Sabetta et al. 2005); (2) only ~15% of dino- cation history and identify trends in phytoplankton flagellates (about 200 species) are known to produce shifts in response to eutrophication processes over resting cysts during their dormancy phase (Matsuoka recent decades, because long-term and continuous & Fukuyo 2000), and this can result in a significant observational data in Chinese coastal waters before underestimate of the dinoflagellate biomass in the the 1990s are very limited. upper water column; (3) some diatom frustules and The development of palaeoceanographical techno - cysts can be lost during sampling and isolating pro- logy provides an effective pathway for understand- cesses, de pending on sample sizes, chemical concen- ing past changes in marine environments and the trations, sieve materials and sizes, and sample treat- responses of associated organisms. A chronology of ment (Wood et al. 1996, Lignum et al. 2008). Thus, it environmental and ecological information can be is important to establish other parameters related established by extracting the geochemical and bio- to the abundance of diatoms and dinoflagellates to logical remains stored in sediments and using a verify the accuracy of biomass estimates. method of multi-proxy analysis (e.g. Cooper 1995a,b, Sterols are considered the best biomarkers for Cornwell et al. 1996, Clarke et al. 2006, Dale 2009). diatoms and dinoflagellates, due to their biosynthetic Cooper (1995a) used several geochemical indicators specificity and resistance to degradation in the sedi- (e.g. organic carbon and biogenic silica) and diatoms ment; in particular, dinosterol (4α, 23, 24-trimethyl- for reconstructing a 2000 yr history of sedimenta- 5α-cholest-22(E)-en-3β-ol) is produced almost exclu- tion, eutrophication, anoxia and diatom community sively by dinoflagellates (Withers 1987, Leblond & structure in Chesapeake Bay, USA, and the results Chapman 2000), and brassicasterol (24-methylchol- indicated that eutrophication began at the time of est-5, 22(E)-dien-3-ol) is a biomarker of diatoms European settlement of the watershed and increased (Barrett et al. 1995, Volkman et al. 1998). Although with increasing land use. Ellegaard et al. (2006) used various chemical and physical conditions (e.g. sedi- geochemical and biological proxies in a sediment mentation rate, temperature, dissolved oxygen, bac- core to track the eu trophication process in the Danish teria, and bioturbation; Canfield 1994, Sun & Wake- estuary Mariager Fjord and found that the main ham 1998) can affect the sterol concentration in the changes over the past 100 yr occurred between 1915 sediment, particularly in the surface sediment, these Liu et al.: Palaeoecology of phytoplankton regime shifts 3 compounds can be preserved for up to 3 million yr luated in the context of in creased nutrient loading, (Rousseau et al. 1995). Changes in the brassicasterol changes in phytoplankton assemblages in the upper concentration of marine sediments are related to water body, regional climate change and historic varia tions in diatoms and primary pro ductivity (Schu- knowl edge of Yantai City’s development through bert et al. 1998, Hinrichs et al. 1999, Schulte & Bard time. 2003). Leblond et al. (2010) reviewed approximately 100 dinoflagellates that can produce over 50 differ- ent sterols and found that about two-thirds of the MATERIALS AND METHODS dinoflagellates contained dino sterol. A positive expo- nential correlation between dinoflagellate cyst con- Study area and sampling centration and dinosterols was observed in sedi- ments of the Celtic and Irish Seas (Marret & Scourse Sishili Bay has an area of about 130 km2 (Fig. 1). It 2003); moreover Mouradian & Panetta (2007) found is characterized by a temperate climatic regime, with that the sum of all dinoflagellate-derived sterols a sea surface temperature of 23.3 to 27.4°C in sum- shows a better correlation with
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