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Cladoceran communities in soda lakes of the Badain Jaran desert, NW China
Journal of Arid Environments 177 (2020) 104133
Contents lists available at ScienceDirect
Journal of Arid Environments journal homepage: www.elsevier.com/locate/jaridenv
Cladoceran communities in soda lakes of the Badain Jaran desert, NW China a
a
b
Yuan Li , Hui Zhao , Ling Hu , Jaakko Johannes Leppänen
T
c,∗
a
Key Laboratory of Desert and Desertification, Northwest Institute of Eco-Environment and Resources, Chinese Academy of Sciences, Lanzhou, 730000, China MOE Key Laboratory of Western China's Environmental Systems, College of Earth and Environmental Sciences, Lanzhou University, Lanzhou, 730000, China Environmental Change Research Unit (ECRU), Ecosystems and Environment Research Programme, Faculty of Biological and Environmental Sciences, University of Helsinki, P.O. Box 65, 00014, Finland
b c
A R T I C LE I N FO
A B S T R A C T
Keywords: Zooplankton Alkaline lakes Paleolimnology
Desert lakes are among the world's most threatened ecosystems, but they are clearly less studied when compared to lakes in more moist regions. The Badain Jaran desert is an exceptional desert due to the presence of numerous megadunes and over hundred small lakes which exhibit large variation in pH and salinity. These lakes have received surprisingly small attention in terms of aquatic ecology and only few biota groups have been studied so far. Here, we present results on the cladoceran communities based on the study of 40 lakes in the Badain Jaran desert. Surface sediment samples were analysed in order to obtain species inventories as complete as possible. Unsurprisingly, we found the most saline lakes devoid of cladocerans, but the subsaline lakes harbor few salt tolerant species. The most interesting finding is the ability of these species to thrive in highly alkaline conditions. The Badain Jaran desert lakes should be studied in more detail (e.g. complete zooplankton and phytoplankton inventories) in order to understand these interesting ecosystems.
1. Introduction Desert lakes, which provide habitats for aquatic biota in arid regions, are among the world's most threatened biomes but remain less well studied when compared to those in wetter regions (Murphy et al., 2015). In desert environments the evaporation exceeds the precipitation, thus there is higher influence of climatic variation on lakes when compared to regions that are more humid. In many cases, they lack permanent surface inflow and are recharged via groundwater input or precipitation. Due to excessive evaporation, desert lakes are commonly high in electrolytes resulting in elevated salinity and pH values (Cole, 1968). High fluctuation in climatic conditions (and subsequent changes in water chemistry), high pH and salinity, and nearly constant input of fine sand in many desert lakes results in low biodiversity (i.e. few dominating taxa) when compared to e.g. boreal or temperate lakes (Cole, 1968). In ecosystems that are dominated by only a few species while other taxa are extremely rare, a complete sampling is sometimes difficult to achieve as rare (due to seasonality or overall low abundance) species are easily missed. Luckily, paleolimnological methods can be used to study biological communities in such environments. This is because sediment samples typically contain material accumulated during a number of years efficiently removing the sampling problems related to seasonal occurrence or overall rarity of species. In many ∗
cases, multiple biological groups are preserved allowing the reconstruction of the species communities. Cladocera are a group of microscopic crustacean zooplankton, which are usually highly abundant in lakes. Cladocerans leave identifiable and well preserving subfossil remains into the sediment upon death or molting allowing the analysis of historical populations (Korhola and Rautio, 2001). The surface sediment represents samples that are integrated in time and space. The cladocerans are of utmost importance in the ecology of the lakes, because they sit in the middle of food webs, transporting energy from primary producers (e.g. phytoplankton) to higher trophic levels (e.g. invertebrate predators, fish, and waterfowl). In addition, cladocerans exhibit species-level preferences towards environmental variables (Korhola and Rautio, 2001), allowing the reconstruction of the lake histories and future predictions. Hence, the group represents extremely useful indicator in environmental studies. Whereas the sediment cores retrieved from mid-lake locations are usually dominated by few planktonic taxa, the littoral samples may provide better representation of chydorid taxa and thus more complete species inventories in terms of species richness. Some cladoceran species are noted as being able to survive highly acidic conditions and the species composition along the acidity gradient has been studied (minimum in situ pH; Belyaeva and Deneke, 2007). However, alkaline conditions have received less attention. The cladoceran diversity has been assessed only from a handful of naturally
Corresponding author. E-mail address: jaakko.leppanen@helsinki.fi (J.J. Leppänen).
https://doi.org/10.1016/j.jaridenv.2020.104133 Received 19 October 2019; Received in revised form 13 February 2020; Accepted 14 February 2020 0140-1963/ © 2020 Published by Elsevier Ltd.
Journal of Arid Environments 177 (2020) 104133
Y. Li, et al.
Fig. 1. Study site data. (a) Sampled sites in the Badain Jaran desert. Inset: Location of the Badain Jaran desert. (b) Close-up view of the lake BDJL-40. (c) Instrumental data of monthly mean precipitation and mean temperature near lake BDJL-24 based on 2014–2017 data (Wang et al., 2019).
low intensity Badain Jaran Desert, consisting of grazing by the animals of Mongolian herdsmen.
alkaline (e.g. pH > 9) lakes, e.g. soda lakes in East Africa (Mengistou, 2016) and saline and hypersaline lakes in China (He et al., 1989). The Badain Jaran desert is located in the western part of the Alxa Plateau in northern China. It covers an area of about 49000 km2 (Zhu et al., 1980), and is considered to be the third largest desert in China (Fig. 1a). The desert contains the highest sand dunes on the earth, the highest of which can exceed 400 m. The inter-dune depressions contain a large number of seepage lakes (Fig. 1b). Many of the lakes are saline while others are subsaline or freshwater lakes. The water chemistry in these lakes is also characterized by high alkalinity across the salinity gradient (Hofmann, 1996). In the Badain Jaran desert, the research in recent decades has concentrated on megadune evolution and lake hydrology (e.g. Chen et al., 2004). Surprisingly few studies have considered biological diversity in these lakes (diatom algae; Rioual et al., 2013, bacterial and archaeal communities; Li et al., 2015, microbial communities; Arp et al., 1998; Banda et al., 2020). The aim of this study is to assess the cladoceran community structure in Badain Jaran Desert lakes using paleolimnological methods by sampling lakes with varying water chemistry characteristics. Our research contributes to the understudied arid lakes food web research, namely in alkaline systems, which are prone to climate change –induced ecological changes.
3. Materials and methods In July 2018, the pH, dissolved oxygen (DO) concentration, conductivity (EC) and total dissolved solids (TDS) of lake water were measured using a portable water quality analyzer (Aquaread AP-1000). Surface-sediment samples (the uppermost 1 cm) were collected from the littoral zones (~0.2 m depth) of each lake. Cladoceran subfossils in these samples were analysed according to standard methods (Korhola and Rautio, 2001). In brief, the sediment samples were heated (90 °C) in a 10% KOH bath for 1 h. The KOH treatment was followed by sieving the sediment sample with tap water (50 μm mesh). The residue was stained with safranin, and gelatin glycerol was applied to produce permanent slides. Cladoceran species were identified using a light microscope at 100–300× magnification. Nomenclature and identification are based on Sarmaja-Korjonen and Szeroczyñska (2007). The number of cladoceran individuals was based on most numerous component (e.g. headshields, shell valves, postabdomens) for each species. We used diatom data (species richness) digitized from Rioual et al. (2013) in order to assess any connections between cladoceran and diatom communities in Badain Jaran lakes. We used principal component analysis (PCA) to assess the general environmental variation between the lakes. The data (lake chemistry data and altitude) was log-transformed prior to PCA analysis. The PCA was conducted using PAST statistics 3.06 (Hammer et al., 2001).
2. Study site The 40 lakes included in this study represent two types of Badain Jaran lakes (i.e. saline and subsaline/fresh). These lakes are relatively small and shallow, and have no surface runoff. Only low salinity lakes freeze during winter whereas the saline lakes stay mostly ice-free (Hofmann, 1996). Charophytes and Potamogeton spp. are commonly observed in Badain Jaran lakes and dense reed beds (Phragmites communis) are present. According to Hofmann (1996) the subsaline/nearly freshwater lakes in the Badain Jaran desert have an established fish fauna (carps, Cyprinidae), whereas regarding the zooplankton, brine shrimp (Artemia sp.) is noted to occur in high salinity Badain Jaran lakes. The meteorological data for the hinterland of the Badain Jaran desert suggest that the mean annual temperature is ~13.5 °C and the mean annual precipitation was ~93 mm (Fig. 1c). Most of the precipitation falls in June and July (Fig. 1c). The annual potential evaporation is around 2600 mm (Hofmann, 1996). Human activity is of
4. Results The sediment samples are mainly composed of sand-rich debris. The cladoceran remains in the sediments were fragmented and rare. Out of the total number (40) of samples (i.e. studied lakes), only 10 contained cladoceran remains (Table 1) and the total number of species was 8. The highest species number was detected in BDJL-31 (6 species; Fig. 2a). The most common species was Alona guttata Sars, 1862/Coronatella rectangula Sars, 1862 pair (10 lakes), followed by Chydorus sphaericus O.F. Muller, 1776) (8 lakes), Alona costata Sars, 1862 (3 lakes) and Oxyurella tenuicaudis Sars, 1862 (2 lakes). Other species (Alona intermedia Sars, 1862; Graptoleberis testidunaria Fischer, 1848; 2
Journal of Arid Environments 177 (2020) 104133
Y. Li, et al.
Table 1 Study lake characteristics. DO is dissolved oxygen, EC is electrical conductivity, TDS is total dissolved solids. The lakes are sorted from lowest TDS to highest TDS. The lakes from where cladocerans were found are marked in italics. Lake name
Longitude
Latitude
Altitude (m.a.s.l)
pH
DO (%)
EC (mS/cm)
TDS (g/L)
BDJL-35 BDJL-36 BDJL-37 BDJL-31 BDJL-40 BDJL-34 BDJL-33 BDJL-32 BDJL-07 BDJL-38 BDJL-28 BDJL-06 BDJL-11 BDJL-27 BDJL-08 BDJL-12 BDJL-25 BDJL-24 BDJL-26 BDJL-39 BDJL-01 BDJL-14 BDJL-30 BDJL-03 BDJL-09 BDJL-04 BDJL-10 BDJL-02 BDJL-19 BDJL-23 BDJL-22 BDJL-29 BDJL-20 BDJL-16 BDJL-05 BDJL-21 BDJL-15 BDJL-18 BDJL-13 BDJL-17
102.48 102.44 102.39 102.52 102.37 102.48 102.49 102.49 102.15 102.39 102.49 102.15 102.21 102.47 102.19 102.27 102.43 102.46 102.43 102.37 101.99 102.26 102.52 102.02 102.22 102.02 102.22 101.99 102.35 102.44 102.42 102.49 102.37 102.27 102.10 102.38 102.23 102.33 102.30 102.30
39.60 39.59 39.59 39.62 39.55 39.60 39.61 39.61 40.00 39.59 39.77 40.00 39.90 39.78 40.03 39.91 39.81 39.87 39.79 39.55 39.81 39.88 39.76 39.85 40.02 39.85 39.98 39.81 39.83 39.85 39.83 39.76 39.82 39.85 39.94 39.80 39.85 39.81 39.91 39.88
1276 1216 1207 1298 1208 1276 1288 1288 1152 1207 1182 1152 1156 1179 1146 1159 1173 1178 1181 1208 1146 1158 1184 1140 1153 1140 1146 1146 1173 1181 1173 1179 1170 1157 1152 1192 1160 1169 1165 1155
8.54 9.75 9.53 10.01 10.11 10.05 10.31 9.86 9.93 9.87 8.62 9.28 9.30 9.71 9.45 8.67 9.69 9.80 9.61 8.95 9.58 9.48 9.33 9.04 9.51 9.30 9.29 9.68 9.68 9.65 9.80 9.19 9.85 9.54 9.40 9.90 9.67 9.46 9.28 9.37
91.20 89.60 66.00 79.30 92.80 79.80 84.20 88.40 73.50 91.60 90.00 105.10 91.30 92.30 109.30 105.00 101.50 93.70 37.50 81.10 68.10 80.50 95.10 90.30 107.50 91.50 104.30 91.30 80.40 93.70 60.00 103.50 88.20 100.30 103.30 51.20 102.80 56.80 100.00 102.20
4.0 4.4 5.3 5.9 6.2 6.4 6.8 9.1 10.0 11.0 104.3 106.4 126.0 122.0 126.0 125.0 205.0 127.0 130.0 147.0 170.0 189.0 154.0 158.8 179.0 182.0 183.0 183.0 190.0 190.0 200.0 200.0 201.0 203.0 208.0 212.0 215.0 225.0 230.0 235.0
2.7 2.9 3.5 3.7 4.2 4.3 4.4 6.0 7.2 8.3 67.0 70.2 74.0 80.0 83.0 83.0 85.0 85.5 90.0 97.0 100.0 102.0 102.0 104.7 118.0 120.0 120.0 121.0 125.0 125.0 130.0 132.0 133.0 134.0 137.0 140.0 145.0 148.0 152.0 155.5
67–155 g/L and subsaline/freshwater TDS 2.7–8.3 g/L). This general character is also visible in PCA (Fig. 2b) where the saline lakes plot to the right hand side of the biplot, whereas less saline lakes plot to the left. The first component is the salinity axis whereas the second component seems to be oxygen gradient. Eigenvalue for component 1 was 0.782 and variance was 98.6%. Eigenvalue for component 2 was 0.009 and variance was 1.2%. The site locations and measured water
Monospilus dispar Sars, 1862 and Alonopsis elongata Sars, 1861) were detected only from a single lake. The cladoceran proportional abundances are presented in Fig. 2a and total counts and photographic illustrations in supplementary material (Appendix 1; Table S1, Fig. S1). The salinity, presented as electrical conductivity (EC) of the studied lakes varied between 4 and 235 mS/cm and pH varied between 8.5 and 10.3. Lakes fall into two categories regarding salinity (saline; TDS
Fig. 2. (a) Cladoceran distribution in surface sediment samples. The lakes are sorted from the lowest pH to the highest pH. The Diatom richness values are digitized from Rioual et al., (2013). Diatom data was not available for lake BDJL-07. (b) PCA biplot for lake data. Only the lakes with cladocera are coded. 3
Journal of Arid Environments 177 (2020) 104133
Y. Li, et al.
chemistry are presented in Table 1. The cladoceran remains were always absent from saline lakes and always present in subsaline/freshwater lakes. Cladoceran species richness does not show any clear connections with diatom species richness in Badain Jaran lakes (Fig. 2a).
and in saline lakes the cladocera are not present. The number of species in subsaline lakes varied between 1 and 6. The ability of many cladoceran species to inhabit highly alkaline systems (pH > 10) is remarkable and should be studied in more detail.
5. Discussion
CRediT authorship contribution statement
The cladoceran species identified in the Badain Jaran lakes are reported to be at least Palaearctic in distribution (Catalogue of life, 2019) and several are considered to be nearly cosmopolitan. All Badain Jaran cladoceran species are benthic and fall within the size range of ~0.5–1 mm (Rizo et al., 2019). Therefore, they are probably similarily affected by predation (e.g. predator aquatic insects). All species except M. dispar, which is often reported in bare bottoms, prefer vegetated habitats. This is in good agreement with our results because all lakes where cladocera were recorded did exhibit vast aquatic vegetation providing plehtora of habitats. All species except A. intermedia are noted to tolerate brackish water (Bledzki and Rybak, 2016). Interestingly, BDJL-31, where A. intermedia was detected, is not the least saline lake in our lake set. Hence, the salinity tolerance of this species seems to be higher than previously assumed. Most of the species are known to inhabit oligo -and eutrophic water systems, but A. elongata is reported to prefer oligotrophic and acidic lakes (Bledzki and Rybak, 2016). The fact that this taxon was found at BJDL-34 where the pH is 10.05 suggests, that the pH range of A. elongata is actually very wide. The factors governing the variation of cladoceran species assemblages in Badain Jaran lakes is not easily resolved and it is likely affected by multiple factors, such as salinity, pH and predation. In general, cladocerans exhibit wide tolerance on salinity, but most of the species are restricted to fresh waters (Frey, 1993) hence the lack of cladoceran remains in the most saline lakes in our dataset is not surprising. In fact, the most saline (salinity > 80 g/L) Badain Jaran lakes are also devoid of diatoms (Rioual et al., 2013) which highlights the extreme conditions in these lakes. The lack of typical saline water cladoceran species, e.g. Daphnia tibetiana is interesting, but Daphnia is known to preserve poorly in lake sediments and thus may have been missed in sediment samples even if it was present in some of our study lakes. The most common species (C.sphaericus, Alona guttata/Coronatella rectangula) in Badain Jaran lakes are also routinely detected in subsaline lakes in China (Zhao, 1992; Zhao et al., 2005; Lin et al., 2017). The more interesting issue is the ability of these species to inhabit such alkaline systems (pH > 10) since pH ~10.5 have been noted as the maximum pH for cladocera in multiple papers (see e.g. O'Brien and deNoyelles, 1972 and references therein) including research conducted in China (He et al., 1989). It is interesting to note that the cladoceran communities in Badain Jaran lakes are most diverse in lakes with pH > 10 whereas in lakes with a pH < 10, only 2 species were detected. In general, the invertebrate communities are not diverse in alkaline lakes and Mengistou (2016) reported only few cladoceran species from east African soda lakes (Moina spp., Alona spp., Coronatella rectangula, Moina belli, Ceriodaphnia cornuta and Macrothrix triseralis). He et al. (1989) reported Alona diaphana from high pH (10.3) environments in the Jinnan and Yinchuan regions in North China. We did not encounter any remains which resembled A. diaphana. Thus, the Badain Jaran cladoceran communities, reported here for the first time, are possibly one of the most alkaline environments where some of the species have ever been recorded. It must be noted that the cladoceran systematics (e.g. Korovchinsky, 1996) and biogeography are under constant revision. Therefore, the comparisons of species environmental preferences or tolerance levels across continents is extremely difficult. In that sense, Badain Jaran lakes represent extremely interesting ecosystems, where e.g. the pH tolerance among Asian cladoceran taxa can be studied with great detail.
Yuan Li: Conceptualization, Investigation, Writing - review & editing. Hui Zhao: Supervision, Funding acquisition. Ling Hu: Investigation. Jaakko Johannes Leppänen: Conceptualization, Writing - original draft. Declaration of competing interest The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper. Acknowledgments This research was supported by the Strategic Priority Research Program of Chinese Academy of Sciences (grant No. XDA20090000), Foundation for Excellent Youth Scholars of “Northwest Institute of EcoEnvironment and Resources”, CAS and the National Natural Science Foundation of China (grant 41901103). Leppänen, JJ is supported by The Finnish Cultural Foundation. Appendix A. Supplementary data Supplementary data to this article can be found online at https:// doi.org/10.1016/j.jaridenv.2020.104133. References Arp, G., Hofman, J., Reitner, J., 1998. Microbial fabric formation in spring mounds (“Microbialites”) of alkaline salt lakes in the Badain Jaran Sand Sea, PR China. Palaios 13, 581–592. Banda, J.F., Lu, Y., Hao, C., Pei, L., Du, Z., Zhang, Y., Wei, P., Dong, H., 2020. The effects of salinity and pH on microbial community diversity and distribution pattern in the brines of soda lakes in Badain Jaran desert, China. Geomicrobiol. J. 37, 1–12. Belyaeva, M., Deneke, R., 2007. Colonization of acidic mining lakes: Chydorus sphaericus and other Cladocera within a dynamic horizontal pH gradient (pH 3-7) in Lake Senftenberger See (Germany). Hydrobiologia 594, 97–108. Bledzki, L.A., Rybak, J.I., 2016. Freshwater Crustacaean Zooplankton in Europe. Cladocera & Copepoda (Calanoida, Cyclopoida) Key to Species Identification, with Notes on Ecology, Distribution, Methods and Introduction to Data Analysis. Springer Nature. Catalogue of life, 2019. 2019 Annual Checklist. Indexing the World's Known Species. Internet page. Available at: http://www.catalogueoflife.org/, Accessed date: 18 December 2019. Chen, J., Li, L., Wang, J., Barry, D.A., Sheng, X., Gu, W., Zhao, X., Chen, L., 2004. Water resources: groundwater maintains dune landscape. Nature 432, 459–460. Cole, G.A., 1968. Desert limnology. In: In: Brown, G.W. (Ed.), Desert Biology. Special Topics on the Physical and Biological Aspects of Arid Regions, vol. 1. Elsevier, pp. 423–486. Frey, D.G., 1993. The penetration of cladocerans into saline waters. Hydrobiologia 267, 233–248. Hammer, Ø., Harper, D.A.T., Ryan, P.D., 2001. PAST-PAlaeontological Statistics, ver. 189. Palaeontol. Electron. 4, 1–9. He, Z., Qin, J., Wang, H., Wang, Z., Xia, X., 1989. Studies on the saline and hypersaline zooplankton from Jinnan and Yinchuan regions. Acta Hydrobiol. Sin. 13, 24–38 (in Chinese). Hofmann, J., 1996. The lakes in the SE part of Badain Jaran Shamo, their limnology and geochemistry. Geowissenschaften 14, 275–278. Korhola, A., Rautio, M., 2001. Cladocera and other Branchiopod crustaceans. In: Smol, J.P., Birks, J.B., Last, W.M. (Eds.), Tracking Environmental Change Using Lake Sediments. Zoological Indicators. Kluwer, Dordrecht, pp. 5–41. Korovchinsky, N., 1996. How many species of Cladocera there are? Hydrobiologia 321, 191–204. Li, L., Hao, C., Wang, L., Pei, L., 2015. Microbial diversity of salt lakes in Badain Jaran desert. Acta Microbiol. Sin. 55, 412–424 (in Chinese). Lin, Q., Xu, L., Hou, J., Liu, Z., Jeppesen, E., Han, B., 2017. Responses of trophic structure and zooplankton community to salinity and temperature in Tibetan lakes: implications for the effect of climate warming. Water Res. 124, 618–629. Mengistou, S., 2016. Invertebrates of east African soda lakes. In: Schagerl, M. (Ed.), Soda
6. Conclusion The cladoceran communities in Badain Jaran lakes is species poor 4
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Sarmaja-Korjonen, K., Szeroczyñska, K., 2007. Atlas of Subfossil Cladocera from Central and Northern Europe. Friends of Lower Vistula Society, Świecie. Wang, X., Zhao, H., Sheng, Y., Geng, J., Wang, K., Yang, H., 2019. Groundwater net discharge rates estimated from lake level change in Badain Jaran Desert,Northwest China. Sci. China Earth Sci. 62. Zhao, W., 1992. A review of the cladocera in inland saline waters. J. Dalian Fish. Coll. 6, 31–41 (in Chinese). Zhao, W., Zheng, M., Xu, X., Liu, X., Guo, G., He, Z., 2005. Biological and ecological features of saline lakes in northern Tibet, China. Hydrobiologia 541, 189–203. Zhu, Z., Wu, Z., Liu, S., Di, X., 1980. An Outline of Chinese Deserts (In Chinese). Science Press, Beijing.
Lakes of East Africa. Springer, Cham. Murphy, A.L., Pavlova, A., Thompson, R., Davis, J., Sunnucks, P., 2015. Swimming through sand: connectivity of aquatic fauna in deserts. Ecol. Evol. 22, 5252–5264. O'Brien, W.J., deNoyelles, F., 1972. Photosynthetically elevated pH as a factor in zooplankton mortality in nutrient enriched ponds. Ecology 53, 605–614. Rioual, P., Lu, Y., Yang, H., Scuderi, L., Chu, G., Holmes, J., Zhu, B., Yang, X., 2013. Diatom-environment relationships and a transfer function for conductivity in lakes of the Badain Jaran desert, Inner Mongolia, China. J. Paleolimnol. 50, 207–229. Rizo, E.J., Xu, S., Tang, Q., Papa, R.D.S., Dumont, H.J., Qian, S.S., Han, B.-P., 2019. A global analysis of cladoceran body size and its variation linking to habitat, distribution and taxonomy. Zool. J. Linn. Soc. 187, 1119–1130.
5
Contents lists available at ScienceDirect
Journal of Arid Environments journal homepage: www.elsevier.com/locate/jaridenv
Cladoceran communities in soda lakes of the Badain Jaran desert, NW China a
a
b
Yuan Li , Hui Zhao , Ling Hu , Jaakko Johannes Leppänen
T
c,∗
a
Key Laboratory of Desert and Desertification, Northwest Institute of Eco-Environment and Resources, Chinese Academy of Sciences, Lanzhou, 730000, China MOE Key Laboratory of Western China's Environmental Systems, College of Earth and Environmental Sciences, Lanzhou University, Lanzhou, 730000, China Environmental Change Research Unit (ECRU), Ecosystems and Environment Research Programme, Faculty of Biological and Environmental Sciences, University of Helsinki, P.O. Box 65, 00014, Finland
b c
A R T I C LE I N FO
A B S T R A C T
Keywords: Zooplankton Alkaline lakes Paleolimnology
Desert lakes are among the world's most threatened ecosystems, but they are clearly less studied when compared to lakes in more moist regions. The Badain Jaran desert is an exceptional desert due to the presence of numerous megadunes and over hundred small lakes which exhibit large variation in pH and salinity. These lakes have received surprisingly small attention in terms of aquatic ecology and only few biota groups have been studied so far. Here, we present results on the cladoceran communities based on the study of 40 lakes in the Badain Jaran desert. Surface sediment samples were analysed in order to obtain species inventories as complete as possible. Unsurprisingly, we found the most saline lakes devoid of cladocerans, but the subsaline lakes harbor few salt tolerant species. The most interesting finding is the ability of these species to thrive in highly alkaline conditions. The Badain Jaran desert lakes should be studied in more detail (e.g. complete zooplankton and phytoplankton inventories) in order to understand these interesting ecosystems.
1. Introduction Desert lakes, which provide habitats for aquatic biota in arid regions, are among the world's most threatened biomes but remain less well studied when compared to those in wetter regions (Murphy et al., 2015). In desert environments the evaporation exceeds the precipitation, thus there is higher influence of climatic variation on lakes when compared to regions that are more humid. In many cases, they lack permanent surface inflow and are recharged via groundwater input or precipitation. Due to excessive evaporation, desert lakes are commonly high in electrolytes resulting in elevated salinity and pH values (Cole, 1968). High fluctuation in climatic conditions (and subsequent changes in water chemistry), high pH and salinity, and nearly constant input of fine sand in many desert lakes results in low biodiversity (i.e. few dominating taxa) when compared to e.g. boreal or temperate lakes (Cole, 1968). In ecosystems that are dominated by only a few species while other taxa are extremely rare, a complete sampling is sometimes difficult to achieve as rare (due to seasonality or overall low abundance) species are easily missed. Luckily, paleolimnological methods can be used to study biological communities in such environments. This is because sediment samples typically contain material accumulated during a number of years efficiently removing the sampling problems related to seasonal occurrence or overall rarity of species. In many ∗
cases, multiple biological groups are preserved allowing the reconstruction of the species communities. Cladocera are a group of microscopic crustacean zooplankton, which are usually highly abundant in lakes. Cladocerans leave identifiable and well preserving subfossil remains into the sediment upon death or molting allowing the analysis of historical populations (Korhola and Rautio, 2001). The surface sediment represents samples that are integrated in time and space. The cladocerans are of utmost importance in the ecology of the lakes, because they sit in the middle of food webs, transporting energy from primary producers (e.g. phytoplankton) to higher trophic levels (e.g. invertebrate predators, fish, and waterfowl). In addition, cladocerans exhibit species-level preferences towards environmental variables (Korhola and Rautio, 2001), allowing the reconstruction of the lake histories and future predictions. Hence, the group represents extremely useful indicator in environmental studies. Whereas the sediment cores retrieved from mid-lake locations are usually dominated by few planktonic taxa, the littoral samples may provide better representation of chydorid taxa and thus more complete species inventories in terms of species richness. Some cladoceran species are noted as being able to survive highly acidic conditions and the species composition along the acidity gradient has been studied (minimum in situ pH; Belyaeva and Deneke, 2007). However, alkaline conditions have received less attention. The cladoceran diversity has been assessed only from a handful of naturally
Corresponding author. E-mail address: jaakko.leppanen@helsinki.fi (J.J. Leppänen).
https://doi.org/10.1016/j.jaridenv.2020.104133 Received 19 October 2019; Received in revised form 13 February 2020; Accepted 14 February 2020 0140-1963/ © 2020 Published by Elsevier Ltd.
Journal of Arid Environments 177 (2020) 104133
Y. Li, et al.
Fig. 1. Study site data. (a) Sampled sites in the Badain Jaran desert. Inset: Location of the Badain Jaran desert. (b) Close-up view of the lake BDJL-40. (c) Instrumental data of monthly mean precipitation and mean temperature near lake BDJL-24 based on 2014–2017 data (Wang et al., 2019).
low intensity Badain Jaran Desert, consisting of grazing by the animals of Mongolian herdsmen.
alkaline (e.g. pH > 9) lakes, e.g. soda lakes in East Africa (Mengistou, 2016) and saline and hypersaline lakes in China (He et al., 1989). The Badain Jaran desert is located in the western part of the Alxa Plateau in northern China. It covers an area of about 49000 km2 (Zhu et al., 1980), and is considered to be the third largest desert in China (Fig. 1a). The desert contains the highest sand dunes on the earth, the highest of which can exceed 400 m. The inter-dune depressions contain a large number of seepage lakes (Fig. 1b). Many of the lakes are saline while others are subsaline or freshwater lakes. The water chemistry in these lakes is also characterized by high alkalinity across the salinity gradient (Hofmann, 1996). In the Badain Jaran desert, the research in recent decades has concentrated on megadune evolution and lake hydrology (e.g. Chen et al., 2004). Surprisingly few studies have considered biological diversity in these lakes (diatom algae; Rioual et al., 2013, bacterial and archaeal communities; Li et al., 2015, microbial communities; Arp et al., 1998; Banda et al., 2020). The aim of this study is to assess the cladoceran community structure in Badain Jaran Desert lakes using paleolimnological methods by sampling lakes with varying water chemistry characteristics. Our research contributes to the understudied arid lakes food web research, namely in alkaline systems, which are prone to climate change –induced ecological changes.
3. Materials and methods In July 2018, the pH, dissolved oxygen (DO) concentration, conductivity (EC) and total dissolved solids (TDS) of lake water were measured using a portable water quality analyzer (Aquaread AP-1000). Surface-sediment samples (the uppermost 1 cm) were collected from the littoral zones (~0.2 m depth) of each lake. Cladoceran subfossils in these samples were analysed according to standard methods (Korhola and Rautio, 2001). In brief, the sediment samples were heated (90 °C) in a 10% KOH bath for 1 h. The KOH treatment was followed by sieving the sediment sample with tap water (50 μm mesh). The residue was stained with safranin, and gelatin glycerol was applied to produce permanent slides. Cladoceran species were identified using a light microscope at 100–300× magnification. Nomenclature and identification are based on Sarmaja-Korjonen and Szeroczyñska (2007). The number of cladoceran individuals was based on most numerous component (e.g. headshields, shell valves, postabdomens) for each species. We used diatom data (species richness) digitized from Rioual et al. (2013) in order to assess any connections between cladoceran and diatom communities in Badain Jaran lakes. We used principal component analysis (PCA) to assess the general environmental variation between the lakes. The data (lake chemistry data and altitude) was log-transformed prior to PCA analysis. The PCA was conducted using PAST statistics 3.06 (Hammer et al., 2001).
2. Study site The 40 lakes included in this study represent two types of Badain Jaran lakes (i.e. saline and subsaline/fresh). These lakes are relatively small and shallow, and have no surface runoff. Only low salinity lakes freeze during winter whereas the saline lakes stay mostly ice-free (Hofmann, 1996). Charophytes and Potamogeton spp. are commonly observed in Badain Jaran lakes and dense reed beds (Phragmites communis) are present. According to Hofmann (1996) the subsaline/nearly freshwater lakes in the Badain Jaran desert have an established fish fauna (carps, Cyprinidae), whereas regarding the zooplankton, brine shrimp (Artemia sp.) is noted to occur in high salinity Badain Jaran lakes. The meteorological data for the hinterland of the Badain Jaran desert suggest that the mean annual temperature is ~13.5 °C and the mean annual precipitation was ~93 mm (Fig. 1c). Most of the precipitation falls in June and July (Fig. 1c). The annual potential evaporation is around 2600 mm (Hofmann, 1996). Human activity is of
4. Results The sediment samples are mainly composed of sand-rich debris. The cladoceran remains in the sediments were fragmented and rare. Out of the total number (40) of samples (i.e. studied lakes), only 10 contained cladoceran remains (Table 1) and the total number of species was 8. The highest species number was detected in BDJL-31 (6 species; Fig. 2a). The most common species was Alona guttata Sars, 1862/Coronatella rectangula Sars, 1862 pair (10 lakes), followed by Chydorus sphaericus O.F. Muller, 1776) (8 lakes), Alona costata Sars, 1862 (3 lakes) and Oxyurella tenuicaudis Sars, 1862 (2 lakes). Other species (Alona intermedia Sars, 1862; Graptoleberis testidunaria Fischer, 1848; 2
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Table 1 Study lake characteristics. DO is dissolved oxygen, EC is electrical conductivity, TDS is total dissolved solids. The lakes are sorted from lowest TDS to highest TDS. The lakes from where cladocerans were found are marked in italics. Lake name
Longitude
Latitude
Altitude (m.a.s.l)
pH
DO (%)
EC (mS/cm)
TDS (g/L)
BDJL-35 BDJL-36 BDJL-37 BDJL-31 BDJL-40 BDJL-34 BDJL-33 BDJL-32 BDJL-07 BDJL-38 BDJL-28 BDJL-06 BDJL-11 BDJL-27 BDJL-08 BDJL-12 BDJL-25 BDJL-24 BDJL-26 BDJL-39 BDJL-01 BDJL-14 BDJL-30 BDJL-03 BDJL-09 BDJL-04 BDJL-10 BDJL-02 BDJL-19 BDJL-23 BDJL-22 BDJL-29 BDJL-20 BDJL-16 BDJL-05 BDJL-21 BDJL-15 BDJL-18 BDJL-13 BDJL-17
102.48 102.44 102.39 102.52 102.37 102.48 102.49 102.49 102.15 102.39 102.49 102.15 102.21 102.47 102.19 102.27 102.43 102.46 102.43 102.37 101.99 102.26 102.52 102.02 102.22 102.02 102.22 101.99 102.35 102.44 102.42 102.49 102.37 102.27 102.10 102.38 102.23 102.33 102.30 102.30
39.60 39.59 39.59 39.62 39.55 39.60 39.61 39.61 40.00 39.59 39.77 40.00 39.90 39.78 40.03 39.91 39.81 39.87 39.79 39.55 39.81 39.88 39.76 39.85 40.02 39.85 39.98 39.81 39.83 39.85 39.83 39.76 39.82 39.85 39.94 39.80 39.85 39.81 39.91 39.88
1276 1216 1207 1298 1208 1276 1288 1288 1152 1207 1182 1152 1156 1179 1146 1159 1173 1178 1181 1208 1146 1158 1184 1140 1153 1140 1146 1146 1173 1181 1173 1179 1170 1157 1152 1192 1160 1169 1165 1155
8.54 9.75 9.53 10.01 10.11 10.05 10.31 9.86 9.93 9.87 8.62 9.28 9.30 9.71 9.45 8.67 9.69 9.80 9.61 8.95 9.58 9.48 9.33 9.04 9.51 9.30 9.29 9.68 9.68 9.65 9.80 9.19 9.85 9.54 9.40 9.90 9.67 9.46 9.28 9.37
91.20 89.60 66.00 79.30 92.80 79.80 84.20 88.40 73.50 91.60 90.00 105.10 91.30 92.30 109.30 105.00 101.50 93.70 37.50 81.10 68.10 80.50 95.10 90.30 107.50 91.50 104.30 91.30 80.40 93.70 60.00 103.50 88.20 100.30 103.30 51.20 102.80 56.80 100.00 102.20
4.0 4.4 5.3 5.9 6.2 6.4 6.8 9.1 10.0 11.0 104.3 106.4 126.0 122.0 126.0 125.0 205.0 127.0 130.0 147.0 170.0 189.0 154.0 158.8 179.0 182.0 183.0 183.0 190.0 190.0 200.0 200.0 201.0 203.0 208.0 212.0 215.0 225.0 230.0 235.0
2.7 2.9 3.5 3.7 4.2 4.3 4.4 6.0 7.2 8.3 67.0 70.2 74.0 80.0 83.0 83.0 85.0 85.5 90.0 97.0 100.0 102.0 102.0 104.7 118.0 120.0 120.0 121.0 125.0 125.0 130.0 132.0 133.0 134.0 137.0 140.0 145.0 148.0 152.0 155.5
67–155 g/L and subsaline/freshwater TDS 2.7–8.3 g/L). This general character is also visible in PCA (Fig. 2b) where the saline lakes plot to the right hand side of the biplot, whereas less saline lakes plot to the left. The first component is the salinity axis whereas the second component seems to be oxygen gradient. Eigenvalue for component 1 was 0.782 and variance was 98.6%. Eigenvalue for component 2 was 0.009 and variance was 1.2%. The site locations and measured water
Monospilus dispar Sars, 1862 and Alonopsis elongata Sars, 1861) were detected only from a single lake. The cladoceran proportional abundances are presented in Fig. 2a and total counts and photographic illustrations in supplementary material (Appendix 1; Table S1, Fig. S1). The salinity, presented as electrical conductivity (EC) of the studied lakes varied between 4 and 235 mS/cm and pH varied between 8.5 and 10.3. Lakes fall into two categories regarding salinity (saline; TDS
Fig. 2. (a) Cladoceran distribution in surface sediment samples. The lakes are sorted from the lowest pH to the highest pH. The Diatom richness values are digitized from Rioual et al., (2013). Diatom data was not available for lake BDJL-07. (b) PCA biplot for lake data. Only the lakes with cladocera are coded. 3
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chemistry are presented in Table 1. The cladoceran remains were always absent from saline lakes and always present in subsaline/freshwater lakes. Cladoceran species richness does not show any clear connections with diatom species richness in Badain Jaran lakes (Fig. 2a).
and in saline lakes the cladocera are not present. The number of species in subsaline lakes varied between 1 and 6. The ability of many cladoceran species to inhabit highly alkaline systems (pH > 10) is remarkable and should be studied in more detail.
5. Discussion
CRediT authorship contribution statement
The cladoceran species identified in the Badain Jaran lakes are reported to be at least Palaearctic in distribution (Catalogue of life, 2019) and several are considered to be nearly cosmopolitan. All Badain Jaran cladoceran species are benthic and fall within the size range of ~0.5–1 mm (Rizo et al., 2019). Therefore, they are probably similarily affected by predation (e.g. predator aquatic insects). All species except M. dispar, which is often reported in bare bottoms, prefer vegetated habitats. This is in good agreement with our results because all lakes where cladocera were recorded did exhibit vast aquatic vegetation providing plehtora of habitats. All species except A. intermedia are noted to tolerate brackish water (Bledzki and Rybak, 2016). Interestingly, BDJL-31, where A. intermedia was detected, is not the least saline lake in our lake set. Hence, the salinity tolerance of this species seems to be higher than previously assumed. Most of the species are known to inhabit oligo -and eutrophic water systems, but A. elongata is reported to prefer oligotrophic and acidic lakes (Bledzki and Rybak, 2016). The fact that this taxon was found at BJDL-34 where the pH is 10.05 suggests, that the pH range of A. elongata is actually very wide. The factors governing the variation of cladoceran species assemblages in Badain Jaran lakes is not easily resolved and it is likely affected by multiple factors, such as salinity, pH and predation. In general, cladocerans exhibit wide tolerance on salinity, but most of the species are restricted to fresh waters (Frey, 1993) hence the lack of cladoceran remains in the most saline lakes in our dataset is not surprising. In fact, the most saline (salinity > 80 g/L) Badain Jaran lakes are also devoid of diatoms (Rioual et al., 2013) which highlights the extreme conditions in these lakes. The lack of typical saline water cladoceran species, e.g. Daphnia tibetiana is interesting, but Daphnia is known to preserve poorly in lake sediments and thus may have been missed in sediment samples even if it was present in some of our study lakes. The most common species (C.sphaericus, Alona guttata/Coronatella rectangula) in Badain Jaran lakes are also routinely detected in subsaline lakes in China (Zhao, 1992; Zhao et al., 2005; Lin et al., 2017). The more interesting issue is the ability of these species to inhabit such alkaline systems (pH > 10) since pH ~10.5 have been noted as the maximum pH for cladocera in multiple papers (see e.g. O'Brien and deNoyelles, 1972 and references therein) including research conducted in China (He et al., 1989). It is interesting to note that the cladoceran communities in Badain Jaran lakes are most diverse in lakes with pH > 10 whereas in lakes with a pH < 10, only 2 species were detected. In general, the invertebrate communities are not diverse in alkaline lakes and Mengistou (2016) reported only few cladoceran species from east African soda lakes (Moina spp., Alona spp., Coronatella rectangula, Moina belli, Ceriodaphnia cornuta and Macrothrix triseralis). He et al. (1989) reported Alona diaphana from high pH (10.3) environments in the Jinnan and Yinchuan regions in North China. We did not encounter any remains which resembled A. diaphana. Thus, the Badain Jaran cladoceran communities, reported here for the first time, are possibly one of the most alkaline environments where some of the species have ever been recorded. It must be noted that the cladoceran systematics (e.g. Korovchinsky, 1996) and biogeography are under constant revision. Therefore, the comparisons of species environmental preferences or tolerance levels across continents is extremely difficult. In that sense, Badain Jaran lakes represent extremely interesting ecosystems, where e.g. the pH tolerance among Asian cladoceran taxa can be studied with great detail.
Yuan Li: Conceptualization, Investigation, Writing - review & editing. Hui Zhao: Supervision, Funding acquisition. Ling Hu: Investigation. Jaakko Johannes Leppänen: Conceptualization, Writing - original draft. Declaration of competing interest The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper. Acknowledgments This research was supported by the Strategic Priority Research Program of Chinese Academy of Sciences (grant No. XDA20090000), Foundation for Excellent Youth Scholars of “Northwest Institute of EcoEnvironment and Resources”, CAS and the National Natural Science Foundation of China (grant 41901103). Leppänen, JJ is supported by The Finnish Cultural Foundation. Appendix A. Supplementary data Supplementary data to this article can be found online at https:// doi.org/10.1016/j.jaridenv.2020.104133. References Arp, G., Hofman, J., Reitner, J., 1998. Microbial fabric formation in spring mounds (“Microbialites”) of alkaline salt lakes in the Badain Jaran Sand Sea, PR China. Palaios 13, 581–592. Banda, J.F., Lu, Y., Hao, C., Pei, L., Du, Z., Zhang, Y., Wei, P., Dong, H., 2020. The effects of salinity and pH on microbial community diversity and distribution pattern in the brines of soda lakes in Badain Jaran desert, China. Geomicrobiol. J. 37, 1–12. Belyaeva, M., Deneke, R., 2007. Colonization of acidic mining lakes: Chydorus sphaericus and other Cladocera within a dynamic horizontal pH gradient (pH 3-7) in Lake Senftenberger See (Germany). Hydrobiologia 594, 97–108. Bledzki, L.A., Rybak, J.I., 2016. Freshwater Crustacaean Zooplankton in Europe. Cladocera & Copepoda (Calanoida, Cyclopoida) Key to Species Identification, with Notes on Ecology, Distribution, Methods and Introduction to Data Analysis. Springer Nature. Catalogue of life, 2019. 2019 Annual Checklist. Indexing the World's Known Species. Internet page. Available at: http://www.catalogueoflife.org/, Accessed date: 18 December 2019. Chen, J., Li, L., Wang, J., Barry, D.A., Sheng, X., Gu, W., Zhao, X., Chen, L., 2004. Water resources: groundwater maintains dune landscape. Nature 432, 459–460. Cole, G.A., 1968. Desert limnology. In: In: Brown, G.W. (Ed.), Desert Biology. Special Topics on the Physical and Biological Aspects of Arid Regions, vol. 1. Elsevier, pp. 423–486. Frey, D.G., 1993. The penetration of cladocerans into saline waters. Hydrobiologia 267, 233–248. Hammer, Ø., Harper, D.A.T., Ryan, P.D., 2001. PAST-PAlaeontological Statistics, ver. 189. Palaeontol. Electron. 4, 1–9. He, Z., Qin, J., Wang, H., Wang, Z., Xia, X., 1989. Studies on the saline and hypersaline zooplankton from Jinnan and Yinchuan regions. Acta Hydrobiol. Sin. 13, 24–38 (in Chinese). Hofmann, J., 1996. The lakes in the SE part of Badain Jaran Shamo, their limnology and geochemistry. Geowissenschaften 14, 275–278. Korhola, A., Rautio, M., 2001. Cladocera and other Branchiopod crustaceans. In: Smol, J.P., Birks, J.B., Last, W.M. (Eds.), Tracking Environmental Change Using Lake Sediments. Zoological Indicators. Kluwer, Dordrecht, pp. 5–41. Korovchinsky, N., 1996. How many species of Cladocera there are? Hydrobiologia 321, 191–204. Li, L., Hao, C., Wang, L., Pei, L., 2015. Microbial diversity of salt lakes in Badain Jaran desert. Acta Microbiol. Sin. 55, 412–424 (in Chinese). Lin, Q., Xu, L., Hou, J., Liu, Z., Jeppesen, E., Han, B., 2017. Responses of trophic structure and zooplankton community to salinity and temperature in Tibetan lakes: implications for the effect of climate warming. Water Res. 124, 618–629. Mengistou, S., 2016. Invertebrates of east African soda lakes. In: Schagerl, M. (Ed.), Soda
6. Conclusion The cladoceran communities in Badain Jaran lakes is species poor 4
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