Response of the Diatom Flora in Jiaozhou Bay, China to Environmental Changes During the Last Century ⁎ Dongyan Liu A,B, , Jun Sun C, Jing Zhang D, Guangshan Liu E

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Marine Micropaleontology 66 (2008) 279–290 www.elsevier.com/locate/marmicro

Response of the diatom flora in Jiaozhou Bay, China to environmental changes during the last century ⁎ Dongyan Liu a,b, , Jun Sun c, Jing Zhang d, Guangshan Liu e

a College of Marine Life Science, Ocean University of China, 5 Yushan Road, Qingdao, 266003, China b School of Earth and Environmental Sciences, University of Wollongong, NSW, 2522, Australia c Institute of Oceanology, The Chinese Academy of Science, Qingdao, 266071, China d State Key Lab of Estuarine and Coastal Research, East China Normal University, 3663 Zhongshan Road North, Shanghai, 200062, China e Oceanography Department, Xiamen University, 422 Siming Road South, Xiamen, 361005, China

Received 25 October 2007; accepted 31 October 2007

Abstract

The diatom flora in a 164 cm long sediment core obtained from Jiaozhou Bay (Yellow Sea, China) was analyzed in order to trace the response of diatoms to environmental changes over the past 100 years. The sediment core was dated by 210Pb and 137Cs and represented approximately 100 years (1899–2001 A.D.). The flora was mainly composed of centric diatoms (59–96%). The concentration of diatoms declined sharply above 30 cm (after ~1981 A.D.), while the dominant species changed from Thalassiosira anguste-lineatus, Thalassiosira eccentria, Coscinodiscus excentricus, Coscinodiscus concinnus and Diploneis gorjanovici to Cyclotella stylorum and Paralia sulcata. Species richness decreased slightly, and the cell abundance of warm-water species increased. We argue that these floral changes were probably caused by climate change in combination with eutrophication resulting from aquaculture and sewage discharge. © 2007 Elsevier B.V. All rights reserved.

Keywords: Jiaozhou Bay; Diatom; Diversity; Sediment; Climate change; Eutrophication

1. Introduction waste water discharge into Jiaozhou Bay increased from 146×106 t in 1988 to 185×106 tin1997(Liu et al., Jiaozhou Bay (JZB), a semi-enclosed basin in the 2005b). Rapid economic development since the 1980s western part of the Yellow Sea, China, is surrounded by has made it an economically important harbor in the the city of Qingdao which has a population of 7 million. northern China. The bay has been modified extensively The population around JZB increased from 4.6 million by human activity, including industrial and agriculture in the 1960s to 7.0 million in the 1990s, and the annual activities around the bay, increasing aquaculture and harbor construction. The production of scallops in JZB increased dramatically from 540 t/y in 1980 to 81000 t/y ⁎ Corresponding author. School of Earth and Environmental Sciences (Building 19), University of Wollongong, NSW, 2522, in 1995 (Lu et al., 2001). However, an epidemic disease Australia. Tel.: +61 2 42215792; fax: +61 2 42214665. of scallops occurred at the end of 1990s due to the high E-mail address: [email protected] (D. Liu). density culture and pollution, resulting in the extensive

0377-8398/$ - see front matter © 2007 Elsevier B.V. All rights reserved. doi:10.1016/j.marmicro.2007.10.007 280 D. Liu et al. / Marine Micropaleontology 66 (2008) 279–290 death of scallops. This forced farmers to give up scallop The historical nutrient data, mainly from the culture in JZB for a few years (Wang and Xiang, 1999; Ecological Environment Monitoring Station in JZB, Wang et al., 2002). indicated that nutrient concentrations have significantly Evidence of a climatic regime shift toward warming increased over the past four decades, especially between in the Northeast Pacific in 1979–1988 has been the 1960s and 1980s. The concentrations of PO4–P, presented by several authors (Ebbesmeyer et al., 1991; NO3–N and NH4–N increased by factors of 2.2, 7.3 and Hare and Mantua, 2000; Mantua, 2004). The regional 7.1, respectively (Shen, 2001; Liu et al., 2005b)(Fig. 2). information from North Pacific also provides evidence No data for silicate concentration was recorded before of temperature increases and associated impacts on the 1970s, since it was thought that dissolved silicate regional ecosystems (Zhang et al., 2000; Lin et al., levels were high in JZB. However, data from 1985 to 2005). A previous study in JZB has found that the 1997 show that the silicate concentration in JZB average air temperature has increased 0.56 °C in summer declined (Fig. 2). Thus, the ratios of DIN/Si in the bay and 2.62 °C in winter since 1900 (Jiao, 2001). Liu (2006) have significantly increased over the past two decades noted that the sea surface temperature in JZB displayed (Shen, 2001; Liu et al., 2005b). Decreasing water an abrupt increase in 1978–1981 (Fig. 1). quality of the bay is further evidenced by the occurrence

Fig. 1. Variations of seawater surface temperature (sst), air temperature (AT), rainfall (PRC), seawater surface salinity (SSS) and winds speed in Jiaozhou Bay from 1960–2001. D. Liu et al. / Marine Micropaleontology 66 (2008) 279–290 281

Fig. 2. Variations of phytoplankton abundance (×104 cells/L) and nutrient concentrations (μM) in Jiaozhou Bay from 1960–2001. of frequent red tides, and the collapse of fisheries, with large-scale aquaculture. However, in the absence of the loss of several fish species (Jiao, 2001; Liu et al., long-term monitoring and baseline condition records, 2005a). we can not prove a causal relation between these Data on phytoplankton, the most important primary factors and the phytoplankton changes. This lack of producers in aquatic ecosystems and the base of their solid information increases the difficulty of restoration food chains, have been widely used as proxies for management. environmental variables (e.g., temperature, nutrient and Paleoecological techniques provide a powerful tool salinity) (Fritz et al., 1991; Sweets et al., 1990). For for obtaining such base-line data. Ecological informa- JZB, data on the phytoplankton community in the water tion derived from sedimentary deposits can be used to column over the last forty years show that cell evaluate both short-term and long-term variations in abundance decreased and there was a change in phytoplankton assemblage and in their environment. dominant species (Jiao, 2001; Liu, 2004). The max- Diatom frustules are generally well preserved, and their imum cell abundance decreased from 108–109 cells/L in assemblages serve as proxies for environmental the 1980s to the 107–108 cells/L in the 1990s. In the changes, including eutrophication, temperature, salinity 1990s, small sized diatoms such as Skeletonema and pH (Hall and Smol, 1999; Smol et al., 1995). costatum and Chaetoceros curvisetus dominated du- Diatom paleoenvironmental analysis can be applied in ring most years, rather than the large diatoms, such as JZB, where the primary production is usually dominated Coscinodiscus eccentria and Rhizosolenia setigera, by diatoms, which account for 79–92% of the total which were dominant in the earlier surveys of 1978– phytoplankton biomass (Liu, 2004). In this study, 1980 (Liu, 2004). These changes in phytoplankton diatoms from a sediment core were analyzed in order assemblages were hypothesized to reflect the com- to date the historical changes in phytoplankton assem- bined influences of eutrophication, climate change and blages, and to relate these changes to anthropogenic and 282 D. Liu et al. / Marine Micropaleontology 66 (2008) 279–290 natural changes that have occurred during the last exchange with the Yellow Sea. There are more than ten century. We present the distribution of diatom taxa in the small tributaries flowing into the Bay, the principal one sediments, discuss the possible causes for the significant of which is the Dagu River with an annual mean changes observed, and evaluate the indicative role of discharge of about 7.2×108 m3, accounting for 84% of diatoms in the evaluation of environmental change. the total riverine input (Marine Environmental Monitor- ing Center, 1992). The exchange of Bay and ocean 2. Materials and methods waters is principally controlled by the tidal residual currents from the Yellow Sea, which run in a clockwise 2.1. Study area and sampling methods circulation, moving up along the west coast and returning down the east coasts. The average residence JZB (35° 55'~36° 18'N, 120° 04'~120° 23'E; Fig. 3) time is about 52 days, ranging from less than 20 days covers ~390 km2, has an average depth of 7 m and a near the bay channel to over 100 days in the northwest maximum depth over 50 m, and is connected to the of the bay (Liu et al., 2004). Thus, the spatial Yellow Sea. The Bay is in a typical temperate coastal distribution and transportation of nutrients are deter- area, with an average water temperature of about 5.6 °C mined mainly by the distance to the bay channel, the in winter and 27.8 °C in summer. The average annual only connection with the Yellow Sea. precipitation is about 775.6 mm, with 56% occurring in A 275 cm long sediment core was taken using a summer (June to August). The dramatic seasonal gravity corer with a 10.5 cm internal diameter in the changes are a result of the cold Siberian winds in central part of JZB at a water depth of 20.6 m, where winter, in contrast to the warm summer monsoons (Wu extensive aquaculture has recently occurred (36° 5' 23'' and Long, 1995). The average salinity in surface waters N, 120° 14' 36'' E) (Fig. 3).The sediment in this area ranges seasonally from 27 ppt in summer to 31.8 ppt in mainly consists of sand, gravel and clay (Dai et al., winter, and is affected by the freshwater input and 2006).

Fig. 3. A map showing the sediment sampling site in Jiaozhou Bay. D. Liu et al. / Marine Micropaleontology 66 (2008) 279–290 283

2.2. Dating and diatom analysis the species assemblage data. It is an indirect ordination analysis that arranges samples along axes based on The sediment core was dated at Xiamen University, species composition (ter Braak, 1995). Ordination China, using 210Pb and 137Cs radiometric-dating techni- analysis indicates which samples are similar in species ques. The measurements were performed using a HPGe γ composition based on the percent abundance of species. spectrometer (Appleby and Oldfield, 1992). Sub-samples Cluster analysis was performed on the same data sets were taken from the sediment core at 1 cm intervals with the constraint that only adjacent samples could be between 0 and 36 cm and at 2 cm intervals between 36 and merged. Phytoplankton diversity was calculated using 275 cm. 156 sub-samples (0–275 cm) were dated, and a biomass-related version of Shannon's H′ Index 100 sub-samples (0–164 cm) were analyzed for diatoms. (Shannon and Weaver, 1949), as follows: Standard methods were used in the diatom analysis Xs (Battarbee, 1986; Renberg, 1990). Sub-samples were H V¼ P log P dried at 105 °C and weighed, then treated with 10% i 2 i i¼1 H2O2 for 3 h to remove organic matter. On the following day, samples were treated with 10% HCl for 3 h to where Pi is relative species biomass (D[abs]) and i and s remove carbonates. After rinsing several times to are the numbers of species. remove chemical residues, zinc bromide (specific The data from diatom biomass and environmental gravity 2.4) was added. Samples were then centrifuged factors were conducted using the logic regression at 2700 r.p.m for 5 min to separate the diatoms. Aliquots analyses to demonstrate their variation. (typically 200–400 µL) were taken from a known volume of suspension and placed onto cover-slips. 3. Results Permanent slides were made by mounting the cover- slips in Naphrax™. Diatoms were identified and 3.1. Core chronologies counted under an Olympus BH-2 light microscope with differential interference contrast optics at ×1000 Based on the 210Pb activity curves, the sedimentation magnification. Taxonomy and nomenclature were rate for the core was estimated at 1.72 cm/yr using the assessed by reference to Fenner et al. (1976), Hasle CRS (constant rate of 210Pb supply) model. The peak (1976), Hasle and Syvertsen (1996) and Guo and Qian (2003). One hundred sub-samples were analyzed and not fewer than 300 diatom valves were counted from each sub-sample. The absolute abundance of diatom valves D[abs] was estimated according to:

D½abs ¼ ½na=fAcv

Where n is the total number of valves counted, a is the area of cover-slip (mm2), f is the number of fields of view counted, A is the area of one field of view (mm2), c is the concentration of slurry pipeted onto the cover-slip (g/ml), and v is the volume of slurry pipeted onto the cover-slip (ml). The relative availability of planktonic and benthic habitats can be regarded as an indicator of environmental change, with eutrophication resulting in much higher ratios of planktic to benthic diatoms, as commonly expressed in Centric:Pennate ratios (C:P ratios) (Cooper, 1995a, b).

2.3. Data analysis

A multivariate ordination technique, detrended correspondence analysis (DCA), was used to analyze Fig. 4. The profiles of 210Pb and 137Cs in the sediment core. 284 D. Liu et al. / Marine Micropaleontology 66 (2008) 279–290 position of 137Cs in core was determined at the depth of 3.3. Diatom flora 62 cm, from which the sedimentation rate was calculated as 1.62 cm/yr (Fig. 4). As a result, the Ninety-six diatom species were identified. 55 species sedimentation rate obtained by averaging the values of centric diatoms and 41 species of pennate diatoms. from both methods was 1.68 cm/yr. Given this Centric diatoms dominated although they fluctuated in sedimentation rate, this core of 164 cm covered relative abundance with depth within the core (Table 1). approximately 100 years of settlement, spanning the The characteristics of diatom flora represented distinct period from 1899 to 2001 A.D. differences in Zones I and II, respectively, as described The estimated sedimentation rate for JZB based on below. this core is high, but supported by other evidence. Previous studies have pointed out the increase in 3.3.1. Zone I (1899–1981 A.D.; 30–164 cm) sedimentation rate for JZB in recent years (Dai et al., There were 83 diatom species in Zone I (Table 1). 2006). It is likely that increasing human activities since The main species were centric diatoms with 48 species, the 1980s, such as intensification of land-use, large- mainly from two families, the Coscinodiscaceae and scale aquaculture and urbanization, have caused the Thalassiosiraceae. Thirty five species of pennate high sedimentation rate in this area rather than natural diatoms were dominated by those in the family perturbation, because no large flood events have been Naviculaceae. Total diatom concentrations ranged reported over the past hundred years. from 6.35×104 valves/g to 24.6×104 valves/g, with an average value of 13.6×104 valves/g (Fig. 6). The 3.2. Detrended correspondence analyses highest diatom concentrations were at 54 cm, 80 cm and 112 cm, the lowest diatom concentrations were at In the DCA diagram, samples with similar diatom 106 cm and 136 cm (Fig. 6). Centric diatom assemblages have similar scores along axis 1 and 2, and concentrations were higher than pennate diatom thus, similar samples plot closely together (Fig. 5). The concentrations, and ranged from 6.07×104 valves/g cluster analysis showed that the greatest change in to 22.8×104 valves/g, representing 73–95% of the diatom assemblages occurred at 30 cm in the core total diatom concentrations (Fig. 6). Pennate diatom (corresponding to 1981), with separate assemblages concentrations ranged from 0.47×104 valves/g to between 1–30 cm (Zone I) and 30–164 cm (Zone II). 3.47×104 valves/g, representing 5–27% of the total

Fig. 5. Detrended correspondence analysis ordination plot based on the diatom assemblages, the numbers on the figure indicate sample numbers. D. Liu et al. / Marine Micropaleontology 66 (2008) 279–290 285

Fig. 6. The changes of diatom concentrations (r2 =0.13), centric diatom concentrations (r2 =0.16), pennate diatom concentrations (r2 =0.01) and the ratio of planktonic to benthic (P:B; r2 =0.02) in the sediment core from Jiaozhou Bay. diatom concentrations (Fig. 6). Planktonic:benthic Diatoms decreased in abundance at 30 cm depth (P:B) ratios ranged from 3 to 29, averaging 7.9 where the total diatom concentrations declined by about (Fig. 6), indicating the deposited diatoms in sedi- 36.9% (on average) from Zone I to Zone II (r2 =0.13; ment core were mainly from the diatoms living in Fig. 6). P:B ratios decreased slightly towards the core the water column. top (r2 =0.02; Fig. 6), mainly because of the decrease in abundance of centric diatoms (r2 =0.16), not by changes 3.3.2. Zone II (1982–2001 A.D.; 1–30 cm) in abundance of pennate diatoms (r2 =0.01; Fig. 6). Of the 66 diatom species in Zone II, 44 were centric and 22 pennate diatoms (Table 1). Coscinodiscaceae, 3.4. Species richness, diversity and dominant species Thalassiosiraceae and Naviculaceae were the main families, as in as Zone I, but the pennate diatoms were The species richness in Zone II was less than that in less abundant in Zone II than in Zone I. Total dia- Zone I; it declined slightly above 30 cm (r2 = tom concentrations ranged from 3.8×104 valves/g 0.07) (Table 1; Fig. 7). For example, 5 species from to 1.33×105 valves/g, averaging 8.58×104 valves/g Coscinodiscus and 6 species from other genera present (Fig. 6), with higher concentrations in the upper 10 cm in Zone I were not found in Zone II; 21 species from the than in the interval between 10 and 30 cm (Fig. 6). Naviculaceae occurred in Zone I, only 12 species were Centric diatom concentrations ranged from 2.78×104 detected in Zone II (Table 1). The Shannon–Wiener valves/g to 10.3×104 valves/g, reaching 59–96% of index of diatom floral diversity fluctuated with depth, total diatom concentrations (Fig. 6). Pennate diatom with a slight, gradual increase above 30 cm (r2 =0.09) concentrations ranged from 0.55×104 valves/g to (Fig. 7). 4.62×104 valves/g, representing 4–35% of total diatom A remarkable shift is dominance occurred at concentrations (Fig. 6). P:B values ranged from 2 to 26, the transition from Zone II into Zone I. The spe- averaging 6.02, compared to 7.9 in Zone II (Fig. 6). cies Thalassiosira anguste-lineatus (21.6–61.6%), 286 D. Liu et al. / Marine Micropaleontology 66 (2008) 279–290

Fig. 7. The changes of species richness (r2 =0.07) and Shannon-Weiner index (r2 =0.09) in the sediment core from Jiaozhou Bay.

T. eccentricus (0–10%), Coscinodiscus excentricus (22– (Fig. 9). C. stylorum, a marine planktonic species 42%), C. concinnus (0.4–11%), Diploneis gorjanovici typical of warmer southern temperate regions, increased (0–12%) and Cyclotella stylorum (4–9%) dominated in markedly in abundance from Zone I and II. The more Zone I (Fig. 8). All of these species, except for temperate species T. anguste–lineatus, T. eccentria, C. stylorum, decreased sharply in abundance in Zone C. excentricus, C. concinnus and D. gorjanovici showed II. The species C. stylorum and Paralia sulcata increased an opposite trend (Fig. 8). in abundance to 15–51.8% and 13–25.6% respectively, It is difficult to classify the trophic type of diatom and dominated in Zone II (Fig. 8). species due to incomplete ecological information, although some researchers have correlated the presence 3.5. Diatom Habitat Preferences of some species with nutrient levels (Margalef, 1969; Chavez, 1989; Tamigneaux et al., 1999). Extensive data In order to examine the potential impact of changes on the species P. sulcata indicated that the species is in salinity, temperature and nutrients, diatom habitat most abundant in high nutrient environments, especially preferences were determined (Table 1) according to waters with high concentrations of dissolved nitrogen Fenner et al., 1976; Hasle, 1976; Hasle and Syvertsen, (Abrantes, 1988a,b, 1991; Margalef, 1978; McQuoid 1996; and Guo and Qian, 2003. In general, the species in and Nordberg, 2003). In JZB, there was an increase in our core are part of a typical marine, temperate diatom the abundance of P. sulcata since the 1980s, at the same assemblage, composed of ninety marine species and six time as the increasing nutrient concentrations in the brackish species. Temperate and warm species were water. Our data thus further confirm that this species is presented in proportions of four to one (Table 1). an indicator of high nutrient levels. Abundant marine species in the diatom flora within the core indicated that no obvious decrease in salinity 4. Discussion occurred over the past hundred years. In addition, warm- water species increased in abundance (r2 =0.36) from The pattern of diatom floral change shown in a Zone I to Zone II, while temperate species declined core taken in JZB indicates that the environment of D. Liu et al. / Marine Micropaleontology 66 (2008) 279–290 287

Fig. 8. The changes of dominant species concentrations in the sediment core of Jiaozhou Bay. deposition underwent a major disturbance at 30 cm 1900, which suggested an increase of average air depth, estimated to have been deposited approxi- temperature in summer of 0.56 °C and 2.62 °C in winter mately 20 years ago (early 1980s). Above this point, (Jiao, 2001). Liu (2006) found sea surface temperature diatom concentrations decreased, there was a change of JZB had an abrupt increase in 1978–1981 (Fig. 1). in dominant species and the abundance of warm- The related studies in Yellow sea during 1976–2000 water species increased. Factors that could have showed 1.7 °C increase of air temperature (Lin et al., caused the observed changes in diatom flora are dis- 2005). Overall, this evidence suggests that water cussed below. temperature increases have occurred in JZB over the past few decades. 4.1. Physical factors A decrease in precipitation and slight increase in salinity over the four decades were also observed in JZB In our results, diatom assemblages in the sediment (Fig.1). The increase in salinity was accompanied by core showed possible responses to temperature increase, reductions in freshwater discharge. For example, the which included the increased abundance of warm annual mean discharge of Dagu River, the major species after the 1980s (above 30 cm, in Zone II) tributary flowing to JZB, has decreased 42% over the (Fig. 9). This was especially true for C. stylorum,a four decades (Shen, 2002). Dominant diatoms in the species preferring warm temperate aquatic environ- sediment core were marine species, reflecting this ments (Fig. 8). Some researchers have indicated that a consistent marine environment within JZB. slight variation in temperature can cause a dramatic effect on the diatom flora because of their low 4.2. Chemical factors temperature compensation ability (Battarbee, 1986; Miller and Florin, 1989). An increasing air temperature P. sulcata, as an indicative species in waters with in JZB has been found based on the observed data since high dissolved nitrogen concentration, significantly 288 D. Liu et al. / Marine Micropaleontology 66 (2008) 279–290

Fig. 9. The changes of warm species (r2 =0.36) and temperate species (r2 =0.21) in the sediment core from Jiaozhou Bay. increased since the 1980s (above 30 cm) in JZB. Over that micro-phytoplankton accounted for 52.4–79.9% the last four decades, JZB has experienced increasing and 38.7–52.5% in winter and spring, respectively, levels of eutrophication. Historical data demonstrates a followed by nanophytoplankton at 17.3–38.2% and significant increase in nutrient concentrations, espe- 30.7–55.2% (Shen et al., 2006). Potential Si limitation cially for nitrogen (Fig. 2)(Shen, 2001; Liu et al., caused by the low freshwater discharge and the 2005b). For example, NO3–N and NH4–N increased 4.3 disproportion ratio of DIN:Si could be an important and 4.1 times respectively from the 1960s to the 1990s factor to control the cell size of diatom assemblage. The in JZB due to the land input (Shen, 2001). Moreover, the growth of larger diatoms with high Si demand is more surveys in water column of JZB in 2002–03 gave easily affected by Si limitation in contrast to smaller further confirmation. For example, red tide diatom diatoms with lower Si demand. Evidence from other species S. costatum and Chaetoceros curvetus preferring coastal areas has also suggested that the availability of to high DIN habitat, dominated in JZB and bloomed Si may control diatom production and assemblage several times in summer (Liu, 2004). These results composition (Dortch and Whitledge, 1992, 2001; suggested that phytoplankton assemblage could have Turner, 2002). been greatly influenced by the high DIN concentration in JZB. 4.3. Biological factors Changes in phytoplankton assemblages, such as an increase of biomass, the occurrence of blooms, changes Grazing by aquaculture species can also influ- in cell size, and shift of dominant species, etc., have ence the phytoplankton biomass and composition in been observed in many coastal waters, as consequences aquatic ecosystems, and has increased greatly in JZB of eutrophication (Yung et al., 1997; Jiao, 2001; in the past 30 years. The concentration of diatoms, Marshall et al., 2003; Liu, 2004). Diatom assemblages especially centric diatoms, roseandfellwiththerise in our sediment core show changes in dominance and in and collapse of scallop aquaculture. When aquacul- cell size rather than in the biomass. The large dominant ture increased in the early 1980s, the diatom con- diatom species T. anguste–lineatus (45–60 μm), centrations dropped precipitously, followed by a slow T. eccentria (35–110 μm), C. excentricus (36–72 μm), increase at 1–10 cm (1995–2001 A.D.) when the C. concinnus (390–464 μm) and D. gorjanovici (48– scallop culture collapsed. Limited phytoplankton 65 μm) in Zone I were replaced by the small species data for the water column also show a decline from C. stylorum (30–66 μm) and P. sulcata (15–36 μm) in 1980 to the 1990s (Fig. 2). Thus, high grazing pres- Zone II. The chlorophyll-a concentration in JZB showed sure caused by large-scale aquaculture of filter- D. Liu et al. / Marine Micropaleontology 66 (2008) 279–290 289 feeders could have been an important factor in the References decrease of diatom biomass in Zone II, in addition to the Si limitation discussed above. Moreover, the Abrantes, F., 1988a. 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