Marine Micropaleontology Diatoms from the Pearl River estuary, China and their suitability as water salinity indicators for coastal environments Yongqiang Zong a,*, Fengling Yu b, Jeremy M. Lloyd b, Guangqing Huang c, Wyss W.-S. Yim a a Department of Earth Sciences, The University of Hong Kong, Hong Kong, SAR China b Department of Geography, University of Durham, Durham, U.K. c Guangzhou Institute of Geography, Guangzhou, China Abstract We collected modern diatom samples from 77 sites across the Pearl River estuary to analyze the relationship between diatom assemblages and the environmental parameters including water salinity, water depth and particle size of surface sediments. Results show that marine diatoms appear mostly in the high salinity environment around Hong Kong and the outer part of the estuary. Brackish water diatoms are found in high abundance in the central part of the estuary. Both marine and brackish water diatoms are predominantly planktonic taxa. Freshwater diatoms are recorded in low salinity environment, with planktonic taxa in the deep tidal channel and benthic species in the shallow deltaic distributaries. Statistical tests indicate a strong correlation between the diatom assemblages and the water salinity, and thus a diatom-based salinity transfer function was developed. The relationship between observed and diatompredicted water salinity suggested accurate and precise reconstruction of palaeo-salinity are possible. Keywords: diatoms, salinity, transfer function, estuary, Pearl River * Corresponding author: Tel.: +852 22194815; Fax: +852 25176912. E-mail address: yqzong@hkucc.hku.hk (Y Zong) 1. Introduction Variability in freshwater discharge from a river into an estuary is an important factor that causes changes in the sedimentary regime, salinity and bio-productivity within an estuarine environment (Chen et al., 2007; Zhang et al., 2008; Zong et al., 2009). Since freshwater discharge is closely related to precipitation patterns of a given river catchment, the changing freshwater flux can be used to reflect changes in climate conditions. In the case of Asian Monsoon, long-term changes in summer precipitation result in fluctuations in freshwater flux entering an estuary (Cliff and Plumb, 2008). The stronger the summer monsoon was, the greater amount of freshwater was discharged into an estuary, and vice versa (Zong et al., 2006). Accurate knowledge of monsoon climate change and more importantly the associated variability in freshwater flux in the recent past is critical for improving our understanding of what may happen in the near future to the coastal environment of East Asia and beyond. Furthermore, water supply is becoming an important issue for human society in the 21st century (Zhang et al., 2008). Most of recent studies regarding Holocene Asian monsoon variability are based on loess sequences for summer monsoon strength (e.g. An et al., 2004), marine deposits for SST (e.g. Tambuini et al., 2003; Wang et al., 2005), lake sequences for local productivity and vegetation history (e.g. Mingram et al., 2004; Shen et al., 2006), and stalagmites (e.g. Wang et al., 2008). However, few attempts have been made to reconstruct the history of monsoonal driven freshwater flux. A pilot study (Zong et al., 2006) has explored the possibility of using microfossils (diatom) as an indicator of freshwater flux, and examined the qualitative relationship between diatom assemblages and water salinity. In order to improve this method, in this paper we document the distributional patterns of modern diatoms across the Pearl River estuary based on an enriched data set and analyze the statistical relationship between diatom assemblages and a number of environmental variables including water salinity. We develop and test the applicability of the first diatom-based salinity transfer functions to aid reconstruction of freshwater flux history from estuarine sediments of the Pearl River estuary and beyond. 2. Study area The Pearl River drains its latitude-orientated drainage catchment which lies between 26º N and 22º N (Figure 1a), a transitional region between tropic and temperate zones under the influence of humid summer monsoon from the south and dry winter monsoon from the north. Three main rivers (the East River, the North River and the West River) drain into the drowned coastal basin and create two deltaic complexes which are separated by the estuary of about 1740 km2 in area (Figure 1). The estuary is protected from storm waves by a cluster of offshore rocky islands. Wave energy within the estuary is low, except during the passage of a typhoon. The main tidal channel runs directly south between Hong Kong and Macau into the South China Sea. A secondary tidal channel runs southeast, through Hong Kong, and turns south into the sea. At present the annual average precipitation in the catchment area is between 1600 and 2000 mm/yr, but over 80% of rainfall occurs during spring and summer, indicative of a warm humid summer and a dry cool winter. Such seasonal differences in precipitation result in freshwater discharges as low as 2000 m3/s in a dry winter and as high as 46,300 m3/s in a 100year flood event (Huang et al., 2004). On average, the Pearl River discharges 302,000 x 10 6 m3 of water and 83.4 x 106 tons of suspended sediment a year (Zong et al., 2009). However, recent construction of reservoirs in the catchment area has reduced the sediment load to only 54.0 x 10 6 tons a year since the mid-1990s (Zhang et al., 2008). Spring tidal range within the estuary ranges from 0.86 m at the mouth area to 1.57 m at the head of the estuary, but increase to 2.29 m and 3.36 m respectively during highest astronomical tides (Huang et al., 2004). Despite the small tidal range, the average volume of flood tides is as high as 73,500 m3/s, which is nearly 13 times the average freshwater discharge. Due to the easterly offshore currents, the freshwater runoff tends to concentrate on the western side of the estuary and flows southwestwards when it reaches offshore Macau. Thus, on the eastern side of the estuary, water salinity is higher than that on the western side. A clear salinity gradient is observed, with the highest salinity in the waters east of Hong Kong, decreasing through waters west of Hong Kong, eastern side and then to western side of the estuary. The lowest salinity is recorded from sites within the deltaic distributaries. 3. Methods 3.1.Modern sediment samples and environmental variables Surface sediment samples were collected from 77 locations across the estuary (Figure 1b) for the analysis of particle size distribution and diatom assemblages. At each sampling location, a grab sampler was used to capture the top 10 cm surface sediment. Water depth and salinity were measured when sediment samples were taken. The water salinity measurements were compared with the average values produced by the Guangzhou Institute of Geography (for the estuarine and deltaic parts) and the Environmental Protection Department of the Hong Kong government for the Hong Kong waters, who have repeatedly measured water salinity across the estuary (Figure 1c, d). The samples for diatom analysis are prepared following standard procedures, by mixing each sediment sample to average the seasonal variability (e.g. Horton et al., 2007; Zong, 1997; Zong and Horton, 1999; Zong et al., 2003). Diatom valves and frustules were identified under a microscope with 1000 magnification to species level according to key references (e.g. van der Werff and Huls, 1958-1966). The diatom counts were displayed using the TILIA package (Grimm, 2004), and expressed as percentage of total diatom valves. It is noted that at each sampling site, the diatom assemblages is likely to be a mixture of locally produced taxa and transported taxa (e.g. Horton et al., 2007; Zong, 1997; Zong and Horton, 1998). Such a mixture of allochthonous and autochthonous diatom valves would also occur in sediments that deposited in the past (Zong, 1998; Sawai, 2001). Thus, we did not attempt to separate the allochthonous component from the diatom assemblages. 3.2.Statistical analyses To display the spatial distribution of diatoms across the estuary, we used the kriging function in ArcGIS to perform spatial interpolation based on the diatom data. The outputs show relative abundance of key diatom taxa. To detect, describe and classify the distribution of diatoms across the estuary, we used unconstrained cluster analysis based on unweighted Euclidean distance (CONISS) within the TILIA package (Grimm, 2004) and detrended correspondence analysis (DCA) (Hill and Gauch, 1980). These two methods are complementary (Birks, 1992) and help group similar sediment samples together and set apart dissimilar samples. The cluster analysis help identify more or less homogeneous groups of sediment samples that have similar diatom assemblages, but DCA provides further information about the pattern of variation within and between groups (ter Braak and Smilauer, 1997-2003). To test the relative strength of relationships between diatoms and environmental variables (salinity, water depth and sand content), we applied canonical correspondence analysis (CCA) with Monte Carol test of 199 random permutations (ter Braak and Smilauer, 1997-2003). To develop a diatom-based water-salinity transfer function, we used unimodal-based regressions (Birks, 1995; Gasse et al., 1997; Juggins, 1992) known as weighted averaging with partial least squares (WA-PLS) (ter Braak and Juggins, 1993) using the calibration program C2 (Juggins, 2004). This analysis used only species with an abundance of over 2%. The diatom data set was not transformed or standardized (Horton et al., 2007). 4. Spatial distribution of modern diatoms From the surface sediment samples (Figure 1), we have found 73 diatom taxa in total, with 57 species having an abundance over 2% and with 17 taxa in abundance of 10% or higher. The frequencies of these 17 diatom species are presented in Figure 2, and the 77 sediment samples are divided into 9 groups based on the cluster analysis (CONISS). Among these dominant taxa, there are two groups of freshwater diatoms that appear abundant in the sediment samples. Freshwater benthic diatoms, including Cymbella affinis, Fallacia subhamulata, Gomphonema parvulum and Synedra ulna, dominate group B of sediment samples (Figure 2a) which are from the two distributaries of the delta plain (also see Figure 3a). Freshwater planktonic diatoms, such as Cyclotella meneghiniana, Cyc. radiosa and Aulacoseira granulata, however, features strongly in groups A and C (Figure 2a) or the inner part of the estuary and the main tidal channel reaching Guangzhou (Figure 3b). It is noted that Aulacoseira granulate is also abundant in the central part of the estuary (group E samples). This species seems to be able to follow the outflow of freshwater further into the brackish water area. Thus, the spatial distribution patterns of the freshwater diatoms suggest that they are strongly associated with water salinity. However, to some extent, water depth is also determining factor in the distributional patterns of benthic and planktonic taxa. This illustrated by the average water depth for each zone (Table 1). The most abundant brackish water diatoms are Coscinodiscus blandus, Cos. divisus, Cyclotella striata and Cyc. stylorum. These taxa are all planktonic types, and they concentrate in groups D, E, F and G (Figure 2a), or the central and outer parts of the estuary (Figure 3c, d). The dominant marine species are also planktonic types, with Chaetoceros radians, Paralia sulcata, Skeletonema costatum and Thalassionema nitzschioides concentrating in groups F, G, H and I (Figure 2a). In particular, Chaetoceros radians and Skeletonema costatum appear most abundant in the area of southern Hong Kong (Figure 3e). Thalassionema nitzschioides is most abundant in the four sediment samples southeast of Hong Kong, and its abundance decreases towards the inner estuary (Figure 3f). The DCA results show clear divisions of modern diatom assemblages. In the DCA bi-plot (Figure 2b), sediment samples from groups A, B and C with dominant freshwater diatoms are plotted on the left hand side, with the two brackish water groups (D and E) plotted in the central part, followed by the two brackish-marine groups (F and G) on the right hand side, and finally the two marine groups (H and I) on the far right of the diagram. Overall, the spatial distributions of the diatom samples show a strong correlation with water salinity from the freshwater end to the marine end of the study area, as shown by axis 1 which is 3.60 in standard unit length and represents 29.7% of total variance in the diatom data. Axis 2 represents 11.2% of total variance of the diatom data and distinguishes groups B and D from groups A, C and E, emphasizing the influence of water depth (Figure 2b). Furthermore, the DCA results confirm the validity of the divisions of diatom samples which are based on the cluster analysis (CONISS). Figure 4 shows the range of annual average water salinity for samples of each zone, which again suggest the diatom zones are strongly related to water salinity. 5. Relationships between modern diatoms and environmental variables The CCA results are listed in Table 2. The three canonical axes account for 32.4% of the explained variance in the diatom data. Partial CCAs show that the total explained variance is composed of 51.9% for salinity, 20.1% for water depth, 13.2% for sand content and 14.8% for inter-correlation of the three environmental variables. The associated Monte Carol permutation tests indicate that water salinity gradient accounts for a significant portion of the total variance in the diatom data (p < 0.005 with 199 random permutations), whilst both water depth and sand content gradients are not significant (p > 0.030 with 199 permutations for both cases). Therefore, statistically significant transfer functions quantifying the relationship between modern diatom assemblages and water salinity can be developed. The CCA results are also graphically illustrated in species-environment and sampleenvironment bi-plots (Figure 5). On the bi-plots, the position of species or sediment samples projected on to the environmental arrows approximate their weighted average optima along each environmental variable. In the bi-plots, salinity aligns closely with CCA axis 1, which has an eigenvalue of 0.522 that represents 89.1% of the total canonical eigenvalues, whereas the environmental variables of axis 2 are unclear. All the marine and brackish diatom taxa are plotted to the left of axis 1, and the freshwater species, on the opposite side (Figure 5a). Similarly, sediment samples collected from the high salinity environment appear on the left hand side, whilst sediment samples from distributaries are found on the opposite side (Figure 5b). These features in the sample-environment and species-environment relationships suggest salinity is the most important environmental variable. Both water depth and sand content have much lower contribution to the variance in the diatom data. Furthermore, the contribution from the intercorrelation between environmental variables is also low. However, there is still about two-third of the variance (67.6%) unexplained. It is unclear what other factors are involved. It is noted that there is a certain degree of variation along the DCA axis 2 among the sediment samples which contain dominantly freshwater diatoms (Figure 2b). Thus part of the unexplained variance in the diatom data may possibly involve nutrient of agricultural and industrial effluence. Nevertheless, the unexplained percentage is considerably lower than reported biological data (Gasse et al., 1995; Jones and Juggins, 1995; Zong and Horton, 1999). 6. The diatom-based salinity transfer function In order to decide on whether or not a unimodal-based technique such as WA-PLS should be used, detrended canonical correspondence analysis (DCCA) was performed. The DCCA result indicates that axis 1 is highly correlated with salinity (weighted correlation, r = 0.97) and represents 85.7% of total variance in the species-environment relationship. The length of gradient is long (3.14 standard deviations). Based on such a strong relationship between diatoms and salinity recorded in the Pearl River estuary, a transfer function is developed. Results from WA-PLS with cross validation indicate that both apparent r2 and prediction r2 are all high in the five components produced (between 0.94 and 0.98, Table 3). On the one hand, such high correlation between the recorded diatom assemblages and the observed salinity without outliers (Figure 6a) suggests a strong predictive power for the transfer function developed. The prediction r2 reported here is similar to, or a little higher than many comparable studies, e.g. diatom-based transfer functions for estuarine salinity (e.g. Juggins, 1992), nutrient level (e.g. Anderson and Vos, 1992), lake water salinity (e.g. Fritz et al., 1991), acidity (e.g. Battarbee et al., 2005), and sea level (e.g. Zong and Horton, 1999; Zong et al., 2003; Horton et al., 2007). On the other, cautions must be taken here, because the sediment samples for this study are collected from sites close to each other across an environmental gradient. This sampling scheme is likely to produce samples resembling one another more than randomly selected sites, resulting in positive spatial autocorrelation in the diatom data (e.g. Telford and Birks, 2005). Such autocorrelation is somewhat unavoidable due to the nature and the purpose of the study. Thus positive spatial autocorrelation is likely present in our data, and its effects should not be ignored. Particularly, the predicted r2 (Table 3) may be artificially a little too high. In terms of the potential errors in prediction, the RMSEP varies between 2.81 and 1.84 ‰, suggesting that the transfer function is capable of producing predictions for palaeo-salinity reconstruction with reasonable precisions (Figure 6b). The predicted error range is comparable with many diatom-based transfer functions (e.g. Battarbee et al., 2005, 2008; Horton et al., 2007; Zong and Horton, 1999; Zong et al., 2003) in terms of the error range proportional to the range of the environmental gradient studied. Estuaries are dynamical environments where fluvial and marine waters are mixing and exchanging. As Figures 3 and 4 show, freshwater diatoms appear abundantly in the freshwater environments. However, they are also found in low numbers in brackish water and even marine environments, possibly being brought to these environments by floodwater. Likewise, low numbers of marine and brackish water diatoms are recorded in the freshwater environments, possibly being transported by incoming tidal currents. Due to the nature of the estuarine environment, an average error of c. 2 ‰ is considered as a very good result. However, as mentioned above, the cross-validation RMSEP estimates may be a little over optimistic because of the presence of possible autocorrelation in the modern diatom data (Telford et al., 2004). Nevertheless, the strength of the correlation between the diatom assemblages and the observed salinity recorded in the Pearl River estuary suggests accurate and precise reconstructions of palaeo-salinity history are possible using the diatom-based salinity transfer function developed. Conclusion We have examined the modern diatom assemblages from 77 sites across the Pearl River estuary. Among these sediment samples, we have identified 73 diatom taxa, with 17 species of over 10% abundance. The majority of marine and brackish water diatoms are planktonic taxa. Marine diatoms appear mostly in the Hong Kong waters and the outer part of the estuary, whilst brackish water diatoms concentrate in the central part of the estuary. Both planktonic and benthic freshwater diatoms appear prominently in samples collected from the low salinity environments. Freshwater planktonic diatoms are recorded from the deep channel, whilst freshwater benthic diatoms are found from two deltaic distributaries. Statistical analyses confirm the strong correlation between diatom assemblages and salinity. The relationship between observed and diatom-predicted water salinity suggested accurate and precise reconstruction of palaeo-salinity are possible. Acknowledgements This research is supported by a research grant from the National Science Foundation of China (No. 40771218) to Huang and Zong, two research grants from the Research Grants Council of the Hong Kong SAR, China (No. HKU7058/06P and HKU7052/08P) to Yim and a NERC/EPSRC 05-08 (UK) PhD studentship from the Dorothy Hodgkin Postgraduate Award to Yu. The authors thank the director of the Environmental Protection Department, Hong Kong SAR for the collection of surface sediment samples and water salinity in the Hong Kong area. References An, C., Feng, Z., Tang L. 2004. Environmental change and cultural response between 8000 and 4000 cal. yr BP in the western Loess Plateau, northwest China. Journal of Quaternary Science 19, 529-535. Anderson, N.J., Vos, P., 1992. Learning from the past: diatoms as palaeoecological indicators of changes in marine environments. Netherlands Journal of Aquatic Ecology 26, 19-30. 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Percentages of the diatom species and the associated environmental variables can be sought from the lead author. Figure 3. Maps show the spatial distribution patterns of dominant diatom taxa across the Pearl River estuary, based on the results of spatial analysis (kriging) of the modern diatom data. Figure 4. Ranges of observed water salinity for each group of sediment samples are shown. Figure 5. Results of the Canonical Correspondence Analysis are shown as bi-plots of species against environmental variables (a) and samples against environmental variables (b). Figure 6. Results of the diatom-based salinity transfer function (component 5): (a) The diatompredicted salinity against the observed salinity and (b) the residuals of the regression using weighted averaging partial least squares (WA-PLS). Table 1. Summary of the environmental variables recorded for each sampling sites Group A (5 samples) B (9 samples) C (10 samples) D (13 samples) E (7 samples) F (15 samples) G (7 samples) H (7 samples) I (4 samples) Water salinity (‰) 3.7 ± 2.0 3.7 ± 3.7 8.0 ± 4.8 17.3 ± 4.1 21.7 ± 3.1 25.6 ± 4.3 30.6 ± 0.9 31.8 ± 1.1 33.4 ± 0.2 Water depth (m) 7.2 ± 2.6 2.6 ± 0.7 3.6 ± 1.2 6.4 ± 3.1 10.3 ± 6.1 10.1 ± 4.2 14.2 ± 11.3 13.7 ± 4.0 27.0 ± 3.2 Sand content (%) 34.0 ± 6.8 32.6 ± 21.5 23.5 ± 11.1 20.3 ± 15.6 20.3 ± 10.6 16.4 ± 2.9 21.3 ±14.6 15.0 ± 6.5 13.7 ± 7.2 Table 2. Summary of CCA results from modern diatom assemblages Axis Eigenvalues Species-environment correlations Cumulative percentage variance of species data of species-environment relationship Sum of all unconstrained eigenvalues Sum of all canonical eigenvalues 1 0.522 0.974 2 0.046 0.570 3 0.017 0.496 4 0.300 0.000 28.9 89.2 31.4 97 32.4 100.0 49.0 0.0 Total inertia 1.807 1.807 0.586 Table 3. Apparent and jack-knifed errors of estimation and prediction for the diatom-based water salinity transfer function Component RMSE (‰) 1 2 3 4 5 2.52 1.70 1.43 1.29 1.16 RMSEP (jack ‰) 2.66 1.96 1.80 1.68 1.63 Apparent (r2) 0.946 0.975 0.983 0.986 0.989 Prediction (jack r2) 0.940 0.967 0.973 0.976 0.977 Jack_Ave_ Bias -0.046 0.039 -0.135 0.043 -0.035 Jack_Max_ Bias 3.281 1.841 1.600 1.611 1.202