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The dynamics of cladoceran assemblages in response to eutrophication and planktivorous fish introduction in Lake Chenghai, a plateau saline lake
Quaternary International 355 (2015) 188e193
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The dynamics of cladoceran assemblages in response to eutrophication and planktivorous fish introduction in Lake Chenghai, a plateau saline lake Guimin Liu a, b, Zhengwen Liu c, *, Joseph M. Smoak d, Binhe Gu e a
School of Environmental and Municipal Engineering, Lanzhou Jiaotong University, Anning West Road 88, Lanzhou, China Engineering Research Center for Cold and Arid Regions Water Resource Comprehensive Utilization, Ministry of Education, China, 730070, China State Key Laboratory of Lake Science and Environment, Nanjing Institute of Geography and Limnology, Chinese Academy of Science, 73 East Beijing Road, Nanjing 210008, China d Department of Environmental Science, Policy, and Geography, University of South Florida, 140 7th Avenue South, Davis Hall 258, St. Petersburg, FL 33701, USA e Soil and Water Sciences Department, University of Florida, Gainesville, FL 32611, USA b c
a r t i c l e i n f o
a b s t r a c t
Article history: Available online 24 August 2014
Lake Chenghai, a brackish lake located in southwest China, has changed from oligotrophic to mesotrophic and finally eutrophic conditions since the 1990s. In the late 1990s, planktivorous icefish were introduced into the lake, which dramatically altered the fish population. A paleolimnological evaluation using the cladoceran remains was conducted in order to analyze the effects of increasing nutrient load and fish introduction on the cladoceran community of this lake. Our results showed that the dominant cladocerans were littoral species, with a low abundance of planktonic Bosmina in the sediment. Increasing eutrophication since the late 1990s greatly enhanced the abundance of cladoceran assemblages, especially for the species that prefer eutrophic conditions. Meanwhile, the species which prefer oligotrophic conditions were extirpated. The changes in Daphnia ephippium length suggested that the planktivorous icefish have varying effects on the body size of different species. © 2014 Elsevier Ltd and INQUA. All rights reserved.
Keywords: Lake Chenghai Cladoceran microfossils Eutrophication Planktivorous fish Sediment dating
1. Introduction Impact of human activities on the lake environments is of growing concern as ecosystems are increasingly degraded. As historical records of lake ecosystems are largely unavailable in most lakes, detailed information on long-term development and biological responses to environmental changes is limited. Fortunately, the palaeolimnological record can provide valuable information about how lake ecology has changed during the past. The study of zooplankton dynamics is crucially important in understanding the mechanisms of how human activities affect lake ecosystems (Jensen et al., 2010). As a key component of zooplankton, cladocerans occur in open water and the littoral zone (Duigan and Birks, 2000), and are known to respond to changes in a wide range of environmental variables such as pH, trophic state, predation pressure, macrophyte abundance, and salinity. Cladocerans are important in lake ecosystems, especially with regard to * Corresponding author. E-mail addresses: [email protected] (G. Liu), [email protected] (Z. Liu). http://dx.doi.org/10.1016/j.quaint.2014.07.029 1040-6182/© 2014 Elsevier Ltd and INQUA. All rights reserved.
nutrient turnover and food web dynamics, in which they link primary producers to higher consumers (Lampert, 1997). Lake Chenghai is one of nine major plateau lakes on the Yunnan Plateau, southwest China. Lake Chenghai is the only brackish lake. During past decades, most of the Yunnan Plateau lakes have been strongly affected by anthropogenic impacts including increased nutrient input and fish introduction (Wang et al., 2012; Zhang et al., 2013; Chen et al., 2014; Wang et al., 2014). Previous studies showed that the accelerated eutrophication and fish introduction have greatly changed the cladoceran structures in freshwater lakes in the plateau region (Liu et al., 2009, 2013). However, the cladoceran dynamics of Lake Chenghai are poorly elucidated. It has been demonstrated that salinity affects the composition of animal communities and thereby alters the trophic interactions in lakes (Jeppesen et al., 1994; Jensen et al., 2010). Moreover, brackish lakes react differently than do freshwater lakes to changes in nutrient loadings (Hansson et al., 1990). Therefore, it is important to study the cladoceran structure and dynamics in Lake Chenghai, as brackish lakes constitute a large proportion of the word's waters (Hammer, 1986).
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A historical cladoceran community can be analyzed by examining the microfossils in lake sediments (Jeppesen et al., 2001; Shumate et al., 2002; Sweetman and Finney, 2003). The purpose of this study is to examine the cladoceran dynamics of Lake Chenghai and to determine the driving factors influencing the pattern in remains recovered from a sediment core. 2. Lake description Lake Chenghai, situated in Yunnan Province (26 270 ~26 380 N, 100 380 ~100 410 E), southwest China, is a plateau lake (Fig. 1). The lake has a total area of about 77.22 km2. The average depth is 25.7 m and its maximum depth is 35.1 m, with an elevation of 1503 m. The water storage capacity is about 19.87 108 m3. Lake Chenghai is one of only three lakes in the world where Spirulina is found naturally. Lake Chenghai was formed during the Early Pleistocene. Before the 1690s, the lake was linked with the Jinsha River via the Haikou River. After the 1690s, the Haikou River stopped flowing naturally because the water level decreased progressively and the lake has become a closed basin. As a result, the lake gradually turned brackish. The total amount of ion concentration in the lake water is up to 1 g L1. This lake area belongs to a temperate zone with a mountainous monsoonal climate, influenced by the southwest monsoon. It is one of the typical Jinsha River hot-dry valley areas. There are no long term meteorological datasets for Lake Chenghai. Meteorological data from Lijiang city, which is about 50 km from Lake Chinghai, have been collected since 1951. Between 1951 and 2006, the mean annual air temperature (MAAT) was 12.7 C. The mean annual precipitation (MAP) was 967 mm, with 786 mm occurring in JuneeSeptember (data from Chinese national Meteorological Centre). The annual evaporating capacity is 2040.3 mm. Productivity in Lake Chenghai has increased since the 1690s when the lake became isolated, but the lake remained oligotrophic until the 1910s. The lake evolved to a mesotrophic state in 1999. The nutrient levels continued to increase and the lake became eutrophic in the 2000s (Wu and Wang, 2003). Marcophytes (mainly comprised of Potamogeton pectinatus, Myriophyllum spicatum) are found in the littoral zone of the lake, with coverage of about 1%
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(Dong et al., 2011). In a survey in 2009e2010, the total nitrogen, total phosphorus, and total Chlorophyll-a in the lake water were 0.773, 0.046 and 0.024 mg L1, respectively (Dong et al., 2012). From 1998 to 2008, the mean Secchi depth in the lake decreased 70%. Historically, the indigenous fish community of the lake was dominated by Distoechodon tumirostris, Erythroculter mongolicus elongatus, Topmouth culter and carps. In 1986, four Chinese carp species (Mylopharyngodon piceus, Ctenopharyngodon idellus, Hypophthalmictuthys molitrix, and Aristichthys mobilis) were deliberately introduced. In 1989, the icefish, Neosalanx taihuensis, was also introduced and increased markedly thereafter. The annual fish yield before 1990 was about 500 t. After 1990, the fish yield increased gradually from 500 to 1100 t in 1996. N. taihuensis became the dominant species and accounted for 70% of the total fish yield (Yang, 1996). According to local historical documentation, there was no evidence that the fish population in Lake Chenghai changed much in recent years. There are 29 fish species belonging to 9 taxa and 12 genera, with 16 native species. 3. Material and methods A sediment core was collected from a depth of 30 m from a site in Lake Chenghai (N26 30.9250 , E100 39.5620 ) using a Kajak gravity corer (Sweetman and Finney, 2003) with a 58 mm diameter in June 2007 (Fig. 1). The length of these cores was approximately 43 cm. All cores were sectioned at 0.5 cm intervals for dating, cladoceran microfossil and chemical analyses, respectively. Samples of dried sediment were analyzed for 210Pb, 226Ra and 137Cs by direct gamma spectrometry using Ortec HPGe GWL series, well-type, coaxial, low background, intrinsic germanium detectors (Appleby et al., 1986). 210 Pb activity was determined via its direct gamma emissions at 46.5 keV, and 226Ra via the 295.2 and 351.9 keV g-rays emitted by its daughter isotope 214Pb following 3 weeks storage in sealed containers to allow secular equilibration to be established. 137Cs was measured by its emissions at 662.7 keV. Supported 210Pb in each sample was assumed to be in equilibrium with in-situ 226Ra. Unsupported 210Pb activity at each depth was calculated by subtracting 226Ra activity from total 210Pb activity. Total organic carbon (TOC) was determined by potassium dichromate volumetry titration with ferrous sulfate after treating the sediment sample with potassium dichromate and sulfuric acid (Jin and Tu, 1990). Total nitrogen (TN) and total phosphorus (TP) were determined by persulphate digestion according to Qian et al. (1990). Cladoceran microfossils were extracted from sediment samples using a modified method reported by Frey (1986). A known amount of wet sediment was deflocculated in 10% KOH at 60 C for 1 h. After filtering through an 80 mm sieve, the remaining material was transferred carefully to a vial, and treated with one drop of formaldehyde solution to prevent fungal growth. Cladoceran microfossils were identified and counted under a light microscope. All ephippia were counted, and the ephippia lengths of Daphnia were measured from at least 20 resting eggs. Cladoceran microfossils were identified to species based on Jiang and Du (1979). Abundance of cladocerans was calculated both as absolute abundance of flux (Amsinck et al., 2005) and relative percentage (a percentage of the fossil sum). 4. Results 4.1. Sediment dating
Fig. 1. Location of Lake Chenghai and the sampling site.
Sediment chronology was established using stratigraphic decay profile of unsupported 210Pb activity and the constant rate of supply (CRS) model. The appearance and the peak of 137Cs activity at the
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22 cm depth represent the year of 1963, the year of peak deposition in the northern hemisphere, respectively. This result was consistent with the 210Pb deduced chronology (Fig. 2). 4.2. Sediment chemical analyses TOC and TN content showed a very gradual increase (Fig. 3) from the bottom to top of the core with acceleration in the upper 10 cm (corresponding to 1998). There was a sharp increase in TP content beginning at the depth of 4.5 cm (corresponding to 2003). The atomic ratios of TOC to TN ratios were steady with small fluctuations over time, with a mean value of 11.75 (Fig. 3). 4.3. Cladoceran microfossil analyses A total of 14 cladoceran taxa representing 9 genera were identified in the sediment of Lake Chenghai. The dominant cladoceran was littoral Chydorus sphaericus, after which they were superseded by Alona rectangula. The absolute abundance and relative percentage of most cladocerans are shown in Fig. 4. Disparalona rostrata, Graptoleberis testudinaria, and Camtocercus rectirostris were very rarely observed, and were omitted from the figure. Daphnia magna, Daphnia hyalina, and Ceriodaphnia spp. which were represented by ephippia, are presented separately (see Fig. 4). Absolute abundance and relative percentage of most cladocerans are shown in Fig. 4. The measured lengths of Daphnia spp. are shown in Fig. 4. Based on the changes in the cladoceran abundance, especially of the dominant Bosmina group, the historic changes of cladoceran exuviae were divided into three phases described as follows: Phase 1: before 1997 (43e13 cm), Cladoceran were at low abundances. The dominant group was Alona gutta before 1993 (corresponding to 13 cm). In this phase, Alona quadrangularis disappeared at 15.5 cm (corresponding to 1985). The ephippia of Ceriodaphnia and D. hyalina showed a slight increase. Phase 2: 1998e2003 (12.5e4.5 cm), the ephippia of D. magna were recorded firstly. The absolute abundance of Alona spp., C. sphaericus, and A. rectangula increased markedly. The average percentage of C. sphaericus increased from 19.5% in phase 1e51.8%, and A. rectangular increased from 3.3% to 15.5%. The A. gutta decreased from 35.2% to 10.2% and disappeared at the depth of 5 cm (corresponding to 2003). A. intermedia disappeared at 9 cm (corresponding to 1998).
Fig. 2. CRS modeled unsupported
210
Pb and
137
Phase 3: 2003e2006 (4.5 cm e sediment surface), the absolute abundance of the littoral species C. sphaericus, A. rectangula, Alona spp. and Leydigia spp. increased prominently. Meanwhile, the ephippia of planktonic species Ceriodaphnia spp., D. hyalina, and D. magna were at their maximum values. The relative percentage of the Cladocerans showed that the C. sphaericus, A. rectangula, accounted for 66.8% and 24.4% of the total cladocerans. The length of ephippium of D. hylina and D. magna is shown in Fig. 4. The length of D. hyalina was relatively low before 2000 (at the depth of 7.5 cm). The mean length of D. hyalina ephippia showed an increasing trend since 2000. The mean ephippia length of D. magna from 6.5 cm (corresponding to 2001) to 2 cm (corresponding to 2005) was not shown because the ephippia numbers at other depths were scarce. The mean length of D. magna showed a decreasing tendency.
5. Discussion Lake phytoplankton has a TOC/TN ratio between 5 and 10, whereas vascular plants have a TOC/TN ratio of 20 or greater (Meyers, 1994; Meyers and Teranes, 2001). Sediment TOC/TN ratio of Lake Chenghai was approximately 11.75 through the core, suggesting the source of organic matter in the sediments should be mainly from the endogenous phytoplankton. This was in agreement with the evidence from stable carbon isotope in Lake Chenghai (Zhu et al., 2011). The TOC, TN and TP concentrations (Smoak and Swarzenski, 2004) trend showed increasing nutrient accumulation since 1997, and indicates an acceleration in the eutrophication of Lake Chenghai beginning in 1997. It has been documented that at low salinity both planktonic/ free-swimming and benthic/plant-associated cladocerans occurred, while only benthic ones occurred at high salinity (Jensen et al., 2010). As a result of saline stress, the littoral species were the dominant cladocerans in Lake Chenghai. Despite the lake being eutrophic, the cladoceran remains are lower than those of freshwater lakes in the Yunnan Plateau (Liu et al., 2009, 2013, 2014) due to the salinity stress. Salinity is an important ecological determinant in brackish and saline lakes (Williams et al., 1990). Bosmina longirostris are detected only in water with low salinity (Kipriyanova et al., 2007). In this study, the very low abundance of B. longirostris suggests that the salinity of the lake was approaching
Cs profiles (A) and age versus depth (B) of the core from Lake Chenghai.
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Fig. 3. TOC, TN, TP concentration and atomic TOC/TN ratio versus depth in the core of Lake Chenghai.
the tolerance limit of this species, which normally has a broad ecological range in freshwater. In contrast to B. longirostris, which were influenced greatly by salinity, D. hyalina can appear in brackish lakes (Jakobsen et al., 2003), and D. magna is commonly found in brackish water (Arner and Koivisto, 1993). Ceriodaphnia quadrangula was distributed in different ranges of salinity, while C. sphaericus decreased along the salinity gradient (Kipriyanova et al., 2007). Our study showed that C. sphaericus appeared in relative high abundance in the sediments, and the ephippium of D. magna, D. hyalina and Ceriodaphnnia were observed in the sediments of Lake Chenghai. These species were all have been recorded in brackish water bodies, which showed that the salinity stress is an
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important ecological determinant of cladoceran composition in Lake Chenghai. In the sediment core, ephippia of D. hyalina were very low in abundance before 17 cm (corresponding to early 1982), and ephippia of D. magna and Ceriodaphnia were first observed from the depth of 9 cm (corresponding to 1998). Daphnia ephippia counts have been used to reconstruct the historical population density (Cousyn et al., 2001; Brendonck and De Meester, 2003). However, it has been reported that many factors can affect the number of ephippia in the sediment besides the historical population €nen et al., 2009). In the present study, the number of ephipia (Nyka for D. hyaline and D. Magna did not have similar trends in the sediments. This is a further reminder that ephippia numbers should be used carefully in reconstructing historical population densities for cladocerans. Therefore, it is difficult to draw a definite conclusion from the changing abundances of ephippia in the present study. It was well known that size-selective predation by planktivorous fish can favor small cladocerans over large ones (Blindow et al., 2000; Liu, 2001). The size of ephippia in sediments could potentially provide information on historic changes in Daphnia size, because the former relates linearly to the body size of the eggbearing female (Verschuren and Marnell, 1997; Jeppesen et al., 2002). The planktivorous fish, icefish, was introduced to Lake Chenghai in 1989 and soon became well established in the lake. Previous studies have demonstrated that invertebrate predation tends to limit numbers of smaller zooplankton, while fish predation impacts larger zooplankton (Gliwicz and Pijanowska, 1989). In the present study, the decrease of ephippia length of D. magna most likely reflects the predation pressure from planktivorous icefish in the lake. Similarly, one may expect that the ephippia length of D. hyalina would decrease along with the increase in icefish in Lake Chenghai. However, the ephippia length of D. hyalina showed an increasing trend since 2000. A possible explanation is that the densities of this D. hyalina are much lower than that of D. manga,
Fig. 4. Changes of the absolute abundance, relative percentage of cladoceran microfossils, and the epippium length of Daphnia hyalina and D. magna of Lake Chenghai.
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which means the predation pressure of D. hyalina from the planktivorous fish was lower than that of D. manga. Most Daphnia have low tolerance of salinity, with the exception of D. magna (Jeppesen et al., 1994). The increase of D. hyalina body size could be a result of increasing nutrient supply which leads to increased food availability. However, this assumption needs to be tested with the data from field investigations. Nutrient levels can affect cladocerans by changing their food availability and their habitat (Whiteside, 1970; Bos and Cumming, 2003). Lake Chenghai reached a mesotrophic state in 1999 and became eutrophic in 2000s (Wu and Wang, 2003). Cladoceran microfossil analyses in Lake Chenghai suggest that the trophic state of this lake had gradually changed since the 1990s. Shumate et al. (2002) demonstrated that C. sphaericus, L. leydigii, and A. rectangular all prefer eutrophic environments. Therefore, the low abundance of L. leydigii, A. rectangular and C. sphaericus in phase 1 probably reflects a stable oligotrophic state in Lake Chenghai, while the increase in their abundances in phase 2 and rapid increase in phase 3 clearly indicate the beginning and the acceleration of eutrophication, respectively. The gradual decrease and disappearance of A. intermedia, A. guttata, and A. quadrangularis, which prefer oligotrophic water (Whiteside, 1970; Hofmann, 1996; Alam and Khan, 1998; Brodersen et al., 1998; Amsinck et al., 2005) and the increasing abundance of eutrophic species from phase 1 to phase 3 confirm this transition in trophic state. Although A. quadrangularis and A. rectangula share similar ecological niches in nutrient levels, A. quadrangularis prefers acidic waters (Steinberg et al., 1988). Therefore, the earlier disappearance of A. quadrangularis possibly related to the changing alkaline conditions in the lake. In conclusion, the sediment evidence of cladoceran microfossils demonstrated that nutrient input has increased since late 1990s in Lake Chengahi. In this brackish lake, the littoral species are dominant in the sediment. Although the numbers of the planktonic species D. hyalina and D. magna were relative high, Bosmina spp., appeared in low abundance in comparison to the high abundance in typical freshwater lakes in the plateau. The salinity of the lake was most likely an important determinant of the low abundance of this species in the lake. Our results suggest that the accelerated eutrophication since the late 1990s significantly altered the cladoceran assemblages in Lake Chenghai, with the rapid increase of the species that prefer eutrophic condition and the disappearance of the species which prefer oligotrophic conditions. The results also suggested that the planktivorous icefish had different effects on the body size of different Daphnnia species. However, it is difficult to draw definitive conclusions for the dynamics of large-sized cladoceran Daphnia, which appeared in ephippia in the sediments. In addition, although it is very important to explore model and statistical analysis of cladoceran microfossils to study the lake ecosystem evolution, it is very difficult to apply existing models to address the historical changes in this brackish lake, as studies performed in brackish lakes are rare (Bos and Cumming, 2003). Further studies are needed to clarify these issues which may link to nutrient inputs and fish introduction in this brackish lake.
Acknowledgements This work was supported by the National Basic Research Program of China (2012CB956104) and the National Natural Science Foundation of China (U1033602, 40901268, 41261002). The authors thank Weilan Xia for sediment dating. The authors gratefully acknowledge the anonymous reviewers as well as the editor, Professor Norm Catto, for their kind work and comments.
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Sweetman, J.N., Finney, B.P., 2003. Differential responses of zooplankton populations (Bosmina longirostris) to fish predation and nutrient-loading in an introduced and a natural sockeye salmon nursery lake on Kodiak Island, Alaska, USA. Journal of Paleolimnology 30, 183e193. Verschuren, D., Marnell, L.F., 1997. Fossil zooplankton and the historical status of Westslope Cutthroat Trout in a headwater lake of Glacier National Park, Montana. Transactions of the American Fisheries Society 126, 21e34. Wang, Q., Yang, X., Anderson, N.J., Zhang, E., Li, Y., 2014. Diatom response to climate forcing of a deep, alpine lake (Lugu Hu, Yunnan, SW China) during the Last Glacial Maximum and its implications for understanding regional monsoon variability. Quaternary Science Reviews 86, 1e12. Wang, R., Dearing, J.A., Langdon, P.G., Zhang, E., Yang, X., Dakos, V., Scheffer, M., 2012. Flickering gives early warning signals of a critical transition to a eutrophic lake state. Nature 492, 419e422. Whiteside, M.C., 1970. Danish chydorid cladocera: modern ecology and core studies. Ecological Monographs 40, 79e118. Williams, W.D., Boulton, A.J., Taaffe, R.G., 1990. Salinity as a determinant of salt lake fauna: a question of scale. Hydrobiologia 197, 256e266. Wu, J.L., Wang, S.M., 2003. Stable isotopic tracing of historical progressive eutrophication from Lake Chenghai, Yunnan in China. Quaternary Sciences 23, 557e564 (in Chinese with English abstract). Yang, J.X., 1996. The exotic and native fish in Yunan: effects, extent and related problems. In: Wang, S., Xie, B.D. (Eds.), Biodiversity Conservation in China (II). China Environmental Press, Beijing, China, pp. 129e138. Zhang, E., Tang, H., Cao, Y., Langdon, P., Wang, R., Yang, X., Shen, J., 2013. The effects of soil erosion on chironomid assemblages in Lugu Lake over the past 120 years. International Review of Hydrobiology 98, 165e172. Zhu, Z.J., Chen, J.A., Zeng, Y., Li, H., Yan, H., Ren, S.C., 2011. Research on the carbon isotopic composition of organic matter from Lake Chenghai and Caohai Lake sediments. Chinese Journal of Geochemistry 30, 107e113.
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Quaternary International journal homepage: www.elsevier.com/locate/quaint
The dynamics of cladoceran assemblages in response to eutrophication and planktivorous fish introduction in Lake Chenghai, a plateau saline lake Guimin Liu a, b, Zhengwen Liu c, *, Joseph M. Smoak d, Binhe Gu e a
School of Environmental and Municipal Engineering, Lanzhou Jiaotong University, Anning West Road 88, Lanzhou, China Engineering Research Center for Cold and Arid Regions Water Resource Comprehensive Utilization, Ministry of Education, China, 730070, China State Key Laboratory of Lake Science and Environment, Nanjing Institute of Geography and Limnology, Chinese Academy of Science, 73 East Beijing Road, Nanjing 210008, China d Department of Environmental Science, Policy, and Geography, University of South Florida, 140 7th Avenue South, Davis Hall 258, St. Petersburg, FL 33701, USA e Soil and Water Sciences Department, University of Florida, Gainesville, FL 32611, USA b c
a r t i c l e i n f o
a b s t r a c t
Article history: Available online 24 August 2014
Lake Chenghai, a brackish lake located in southwest China, has changed from oligotrophic to mesotrophic and finally eutrophic conditions since the 1990s. In the late 1990s, planktivorous icefish were introduced into the lake, which dramatically altered the fish population. A paleolimnological evaluation using the cladoceran remains was conducted in order to analyze the effects of increasing nutrient load and fish introduction on the cladoceran community of this lake. Our results showed that the dominant cladocerans were littoral species, with a low abundance of planktonic Bosmina in the sediment. Increasing eutrophication since the late 1990s greatly enhanced the abundance of cladoceran assemblages, especially for the species that prefer eutrophic conditions. Meanwhile, the species which prefer oligotrophic conditions were extirpated. The changes in Daphnia ephippium length suggested that the planktivorous icefish have varying effects on the body size of different species. © 2014 Elsevier Ltd and INQUA. All rights reserved.
Keywords: Lake Chenghai Cladoceran microfossils Eutrophication Planktivorous fish Sediment dating
1. Introduction Impact of human activities on the lake environments is of growing concern as ecosystems are increasingly degraded. As historical records of lake ecosystems are largely unavailable in most lakes, detailed information on long-term development and biological responses to environmental changes is limited. Fortunately, the palaeolimnological record can provide valuable information about how lake ecology has changed during the past. The study of zooplankton dynamics is crucially important in understanding the mechanisms of how human activities affect lake ecosystems (Jensen et al., 2010). As a key component of zooplankton, cladocerans occur in open water and the littoral zone (Duigan and Birks, 2000), and are known to respond to changes in a wide range of environmental variables such as pH, trophic state, predation pressure, macrophyte abundance, and salinity. Cladocerans are important in lake ecosystems, especially with regard to * Corresponding author. E-mail addresses: [email protected] (G. Liu), [email protected] (Z. Liu). http://dx.doi.org/10.1016/j.quaint.2014.07.029 1040-6182/© 2014 Elsevier Ltd and INQUA. All rights reserved.
nutrient turnover and food web dynamics, in which they link primary producers to higher consumers (Lampert, 1997). Lake Chenghai is one of nine major plateau lakes on the Yunnan Plateau, southwest China. Lake Chenghai is the only brackish lake. During past decades, most of the Yunnan Plateau lakes have been strongly affected by anthropogenic impacts including increased nutrient input and fish introduction (Wang et al., 2012; Zhang et al., 2013; Chen et al., 2014; Wang et al., 2014). Previous studies showed that the accelerated eutrophication and fish introduction have greatly changed the cladoceran structures in freshwater lakes in the plateau region (Liu et al., 2009, 2013). However, the cladoceran dynamics of Lake Chenghai are poorly elucidated. It has been demonstrated that salinity affects the composition of animal communities and thereby alters the trophic interactions in lakes (Jeppesen et al., 1994; Jensen et al., 2010). Moreover, brackish lakes react differently than do freshwater lakes to changes in nutrient loadings (Hansson et al., 1990). Therefore, it is important to study the cladoceran structure and dynamics in Lake Chenghai, as brackish lakes constitute a large proportion of the word's waters (Hammer, 1986).
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A historical cladoceran community can be analyzed by examining the microfossils in lake sediments (Jeppesen et al., 2001; Shumate et al., 2002; Sweetman and Finney, 2003). The purpose of this study is to examine the cladoceran dynamics of Lake Chenghai and to determine the driving factors influencing the pattern in remains recovered from a sediment core. 2. Lake description Lake Chenghai, situated in Yunnan Province (26 270 ~26 380 N, 100 380 ~100 410 E), southwest China, is a plateau lake (Fig. 1). The lake has a total area of about 77.22 km2. The average depth is 25.7 m and its maximum depth is 35.1 m, with an elevation of 1503 m. The water storage capacity is about 19.87 108 m3. Lake Chenghai is one of only three lakes in the world where Spirulina is found naturally. Lake Chenghai was formed during the Early Pleistocene. Before the 1690s, the lake was linked with the Jinsha River via the Haikou River. After the 1690s, the Haikou River stopped flowing naturally because the water level decreased progressively and the lake has become a closed basin. As a result, the lake gradually turned brackish. The total amount of ion concentration in the lake water is up to 1 g L1. This lake area belongs to a temperate zone with a mountainous monsoonal climate, influenced by the southwest monsoon. It is one of the typical Jinsha River hot-dry valley areas. There are no long term meteorological datasets for Lake Chenghai. Meteorological data from Lijiang city, which is about 50 km from Lake Chinghai, have been collected since 1951. Between 1951 and 2006, the mean annual air temperature (MAAT) was 12.7 C. The mean annual precipitation (MAP) was 967 mm, with 786 mm occurring in JuneeSeptember (data from Chinese national Meteorological Centre). The annual evaporating capacity is 2040.3 mm. Productivity in Lake Chenghai has increased since the 1690s when the lake became isolated, but the lake remained oligotrophic until the 1910s. The lake evolved to a mesotrophic state in 1999. The nutrient levels continued to increase and the lake became eutrophic in the 2000s (Wu and Wang, 2003). Marcophytes (mainly comprised of Potamogeton pectinatus, Myriophyllum spicatum) are found in the littoral zone of the lake, with coverage of about 1%
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(Dong et al., 2011). In a survey in 2009e2010, the total nitrogen, total phosphorus, and total Chlorophyll-a in the lake water were 0.773, 0.046 and 0.024 mg L1, respectively (Dong et al., 2012). From 1998 to 2008, the mean Secchi depth in the lake decreased 70%. Historically, the indigenous fish community of the lake was dominated by Distoechodon tumirostris, Erythroculter mongolicus elongatus, Topmouth culter and carps. In 1986, four Chinese carp species (Mylopharyngodon piceus, Ctenopharyngodon idellus, Hypophthalmictuthys molitrix, and Aristichthys mobilis) were deliberately introduced. In 1989, the icefish, Neosalanx taihuensis, was also introduced and increased markedly thereafter. The annual fish yield before 1990 was about 500 t. After 1990, the fish yield increased gradually from 500 to 1100 t in 1996. N. taihuensis became the dominant species and accounted for 70% of the total fish yield (Yang, 1996). According to local historical documentation, there was no evidence that the fish population in Lake Chenghai changed much in recent years. There are 29 fish species belonging to 9 taxa and 12 genera, with 16 native species. 3. Material and methods A sediment core was collected from a depth of 30 m from a site in Lake Chenghai (N26 30.9250 , E100 39.5620 ) using a Kajak gravity corer (Sweetman and Finney, 2003) with a 58 mm diameter in June 2007 (Fig. 1). The length of these cores was approximately 43 cm. All cores were sectioned at 0.5 cm intervals for dating, cladoceran microfossil and chemical analyses, respectively. Samples of dried sediment were analyzed for 210Pb, 226Ra and 137Cs by direct gamma spectrometry using Ortec HPGe GWL series, well-type, coaxial, low background, intrinsic germanium detectors (Appleby et al., 1986). 210 Pb activity was determined via its direct gamma emissions at 46.5 keV, and 226Ra via the 295.2 and 351.9 keV g-rays emitted by its daughter isotope 214Pb following 3 weeks storage in sealed containers to allow secular equilibration to be established. 137Cs was measured by its emissions at 662.7 keV. Supported 210Pb in each sample was assumed to be in equilibrium with in-situ 226Ra. Unsupported 210Pb activity at each depth was calculated by subtracting 226Ra activity from total 210Pb activity. Total organic carbon (TOC) was determined by potassium dichromate volumetry titration with ferrous sulfate after treating the sediment sample with potassium dichromate and sulfuric acid (Jin and Tu, 1990). Total nitrogen (TN) and total phosphorus (TP) were determined by persulphate digestion according to Qian et al. (1990). Cladoceran microfossils were extracted from sediment samples using a modified method reported by Frey (1986). A known amount of wet sediment was deflocculated in 10% KOH at 60 C for 1 h. After filtering through an 80 mm sieve, the remaining material was transferred carefully to a vial, and treated with one drop of formaldehyde solution to prevent fungal growth. Cladoceran microfossils were identified and counted under a light microscope. All ephippia were counted, and the ephippia lengths of Daphnia were measured from at least 20 resting eggs. Cladoceran microfossils were identified to species based on Jiang and Du (1979). Abundance of cladocerans was calculated both as absolute abundance of flux (Amsinck et al., 2005) and relative percentage (a percentage of the fossil sum). 4. Results 4.1. Sediment dating
Fig. 1. Location of Lake Chenghai and the sampling site.
Sediment chronology was established using stratigraphic decay profile of unsupported 210Pb activity and the constant rate of supply (CRS) model. The appearance and the peak of 137Cs activity at the
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22 cm depth represent the year of 1963, the year of peak deposition in the northern hemisphere, respectively. This result was consistent with the 210Pb deduced chronology (Fig. 2). 4.2. Sediment chemical analyses TOC and TN content showed a very gradual increase (Fig. 3) from the bottom to top of the core with acceleration in the upper 10 cm (corresponding to 1998). There was a sharp increase in TP content beginning at the depth of 4.5 cm (corresponding to 2003). The atomic ratios of TOC to TN ratios were steady with small fluctuations over time, with a mean value of 11.75 (Fig. 3). 4.3. Cladoceran microfossil analyses A total of 14 cladoceran taxa representing 9 genera were identified in the sediment of Lake Chenghai. The dominant cladoceran was littoral Chydorus sphaericus, after which they were superseded by Alona rectangula. The absolute abundance and relative percentage of most cladocerans are shown in Fig. 4. Disparalona rostrata, Graptoleberis testudinaria, and Camtocercus rectirostris were very rarely observed, and were omitted from the figure. Daphnia magna, Daphnia hyalina, and Ceriodaphnia spp. which were represented by ephippia, are presented separately (see Fig. 4). Absolute abundance and relative percentage of most cladocerans are shown in Fig. 4. The measured lengths of Daphnia spp. are shown in Fig. 4. Based on the changes in the cladoceran abundance, especially of the dominant Bosmina group, the historic changes of cladoceran exuviae were divided into three phases described as follows: Phase 1: before 1997 (43e13 cm), Cladoceran were at low abundances. The dominant group was Alona gutta before 1993 (corresponding to 13 cm). In this phase, Alona quadrangularis disappeared at 15.5 cm (corresponding to 1985). The ephippia of Ceriodaphnia and D. hyalina showed a slight increase. Phase 2: 1998e2003 (12.5e4.5 cm), the ephippia of D. magna were recorded firstly. The absolute abundance of Alona spp., C. sphaericus, and A. rectangula increased markedly. The average percentage of C. sphaericus increased from 19.5% in phase 1e51.8%, and A. rectangular increased from 3.3% to 15.5%. The A. gutta decreased from 35.2% to 10.2% and disappeared at the depth of 5 cm (corresponding to 2003). A. intermedia disappeared at 9 cm (corresponding to 1998).
Fig. 2. CRS modeled unsupported
210
Pb and
137
Phase 3: 2003e2006 (4.5 cm e sediment surface), the absolute abundance of the littoral species C. sphaericus, A. rectangula, Alona spp. and Leydigia spp. increased prominently. Meanwhile, the ephippia of planktonic species Ceriodaphnia spp., D. hyalina, and D. magna were at their maximum values. The relative percentage of the Cladocerans showed that the C. sphaericus, A. rectangula, accounted for 66.8% and 24.4% of the total cladocerans. The length of ephippium of D. hylina and D. magna is shown in Fig. 4. The length of D. hyalina was relatively low before 2000 (at the depth of 7.5 cm). The mean length of D. hyalina ephippia showed an increasing trend since 2000. The mean ephippia length of D. magna from 6.5 cm (corresponding to 2001) to 2 cm (corresponding to 2005) was not shown because the ephippia numbers at other depths were scarce. The mean length of D. magna showed a decreasing tendency.
5. Discussion Lake phytoplankton has a TOC/TN ratio between 5 and 10, whereas vascular plants have a TOC/TN ratio of 20 or greater (Meyers, 1994; Meyers and Teranes, 2001). Sediment TOC/TN ratio of Lake Chenghai was approximately 11.75 through the core, suggesting the source of organic matter in the sediments should be mainly from the endogenous phytoplankton. This was in agreement with the evidence from stable carbon isotope in Lake Chenghai (Zhu et al., 2011). The TOC, TN and TP concentrations (Smoak and Swarzenski, 2004) trend showed increasing nutrient accumulation since 1997, and indicates an acceleration in the eutrophication of Lake Chenghai beginning in 1997. It has been documented that at low salinity both planktonic/ free-swimming and benthic/plant-associated cladocerans occurred, while only benthic ones occurred at high salinity (Jensen et al., 2010). As a result of saline stress, the littoral species were the dominant cladocerans in Lake Chenghai. Despite the lake being eutrophic, the cladoceran remains are lower than those of freshwater lakes in the Yunnan Plateau (Liu et al., 2009, 2013, 2014) due to the salinity stress. Salinity is an important ecological determinant in brackish and saline lakes (Williams et al., 1990). Bosmina longirostris are detected only in water with low salinity (Kipriyanova et al., 2007). In this study, the very low abundance of B. longirostris suggests that the salinity of the lake was approaching
Cs profiles (A) and age versus depth (B) of the core from Lake Chenghai.
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Fig. 3. TOC, TN, TP concentration and atomic TOC/TN ratio versus depth in the core of Lake Chenghai.
the tolerance limit of this species, which normally has a broad ecological range in freshwater. In contrast to B. longirostris, which were influenced greatly by salinity, D. hyalina can appear in brackish lakes (Jakobsen et al., 2003), and D. magna is commonly found in brackish water (Arner and Koivisto, 1993). Ceriodaphnia quadrangula was distributed in different ranges of salinity, while C. sphaericus decreased along the salinity gradient (Kipriyanova et al., 2007). Our study showed that C. sphaericus appeared in relative high abundance in the sediments, and the ephippium of D. magna, D. hyalina and Ceriodaphnnia were observed in the sediments of Lake Chenghai. These species were all have been recorded in brackish water bodies, which showed that the salinity stress is an
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important ecological determinant of cladoceran composition in Lake Chenghai. In the sediment core, ephippia of D. hyalina were very low in abundance before 17 cm (corresponding to early 1982), and ephippia of D. magna and Ceriodaphnia were first observed from the depth of 9 cm (corresponding to 1998). Daphnia ephippia counts have been used to reconstruct the historical population density (Cousyn et al., 2001; Brendonck and De Meester, 2003). However, it has been reported that many factors can affect the number of ephippia in the sediment besides the historical population €nen et al., 2009). In the present study, the number of ephipia (Nyka for D. hyaline and D. Magna did not have similar trends in the sediments. This is a further reminder that ephippia numbers should be used carefully in reconstructing historical population densities for cladocerans. Therefore, it is difficult to draw a definite conclusion from the changing abundances of ephippia in the present study. It was well known that size-selective predation by planktivorous fish can favor small cladocerans over large ones (Blindow et al., 2000; Liu, 2001). The size of ephippia in sediments could potentially provide information on historic changes in Daphnia size, because the former relates linearly to the body size of the eggbearing female (Verschuren and Marnell, 1997; Jeppesen et al., 2002). The planktivorous fish, icefish, was introduced to Lake Chenghai in 1989 and soon became well established in the lake. Previous studies have demonstrated that invertebrate predation tends to limit numbers of smaller zooplankton, while fish predation impacts larger zooplankton (Gliwicz and Pijanowska, 1989). In the present study, the decrease of ephippia length of D. magna most likely reflects the predation pressure from planktivorous icefish in the lake. Similarly, one may expect that the ephippia length of D. hyalina would decrease along with the increase in icefish in Lake Chenghai. However, the ephippia length of D. hyalina showed an increasing trend since 2000. A possible explanation is that the densities of this D. hyalina are much lower than that of D. manga,
Fig. 4. Changes of the absolute abundance, relative percentage of cladoceran microfossils, and the epippium length of Daphnia hyalina and D. magna of Lake Chenghai.
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which means the predation pressure of D. hyalina from the planktivorous fish was lower than that of D. manga. Most Daphnia have low tolerance of salinity, with the exception of D. magna (Jeppesen et al., 1994). The increase of D. hyalina body size could be a result of increasing nutrient supply which leads to increased food availability. However, this assumption needs to be tested with the data from field investigations. Nutrient levels can affect cladocerans by changing their food availability and their habitat (Whiteside, 1970; Bos and Cumming, 2003). Lake Chenghai reached a mesotrophic state in 1999 and became eutrophic in 2000s (Wu and Wang, 2003). Cladoceran microfossil analyses in Lake Chenghai suggest that the trophic state of this lake had gradually changed since the 1990s. Shumate et al. (2002) demonstrated that C. sphaericus, L. leydigii, and A. rectangular all prefer eutrophic environments. Therefore, the low abundance of L. leydigii, A. rectangular and C. sphaericus in phase 1 probably reflects a stable oligotrophic state in Lake Chenghai, while the increase in their abundances in phase 2 and rapid increase in phase 3 clearly indicate the beginning and the acceleration of eutrophication, respectively. The gradual decrease and disappearance of A. intermedia, A. guttata, and A. quadrangularis, which prefer oligotrophic water (Whiteside, 1970; Hofmann, 1996; Alam and Khan, 1998; Brodersen et al., 1998; Amsinck et al., 2005) and the increasing abundance of eutrophic species from phase 1 to phase 3 confirm this transition in trophic state. Although A. quadrangularis and A. rectangula share similar ecological niches in nutrient levels, A. quadrangularis prefers acidic waters (Steinberg et al., 1988). Therefore, the earlier disappearance of A. quadrangularis possibly related to the changing alkaline conditions in the lake. In conclusion, the sediment evidence of cladoceran microfossils demonstrated that nutrient input has increased since late 1990s in Lake Chengahi. In this brackish lake, the littoral species are dominant in the sediment. Although the numbers of the planktonic species D. hyalina and D. magna were relative high, Bosmina spp., appeared in low abundance in comparison to the high abundance in typical freshwater lakes in the plateau. The salinity of the lake was most likely an important determinant of the low abundance of this species in the lake. Our results suggest that the accelerated eutrophication since the late 1990s significantly altered the cladoceran assemblages in Lake Chenghai, with the rapid increase of the species that prefer eutrophic condition and the disappearance of the species which prefer oligotrophic conditions. The results also suggested that the planktivorous icefish had different effects on the body size of different Daphnnia species. However, it is difficult to draw definitive conclusions for the dynamics of large-sized cladoceran Daphnia, which appeared in ephippia in the sediments. In addition, although it is very important to explore model and statistical analysis of cladoceran microfossils to study the lake ecosystem evolution, it is very difficult to apply existing models to address the historical changes in this brackish lake, as studies performed in brackish lakes are rare (Bos and Cumming, 2003). Further studies are needed to clarify these issues which may link to nutrient inputs and fish introduction in this brackish lake.
Acknowledgements This work was supported by the National Basic Research Program of China (2012CB956104) and the National Natural Science Foundation of China (U1033602, 40901268, 41261002). The authors thank Weilan Xia for sediment dating. The authors gratefully acknowledge the anonymous reviewers as well as the editor, Professor Norm Catto, for their kind work and comments.
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