Journal of Great Lakes Research xxx (xxxx) xxx
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Journal of Great Lakes Research
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How ancient is Lake Lugu (Yunnan, China)? The gastropods’ viewpoint with focus on Radix (Lymnaeidae) ⇑ Robert Wiese a, , Catharina Clewing b, Christian Albrecht b, Carolin Rabethge a, Hucai Zhang c, Frank Riedel a,c a Institute of Geological Sciences, Freie Universität Berlin, D-12249 Berlin, Germany b Department of Animal Ecology & Systematics, Justus Liebig University Giessen, D-35392 Giessen, Germany c Institute for Ecological Research and Pollution Control of Plateau Lakes, School of Ecology and Environmental Science, Yunnan University, Kunming 650500, China article info abstract
Article history: Lake Lugu has been termed an ‘‘ancient lake” in several publications. Ancient lakes, such as Baikal or Received 7 February 2020 Tanganyika have in common an age of several million years and an outstanding biodiversity and rate Accepted 9 June 2020 of endemism. Lake Lugu’s age is unknown, however, and has been inferred from the presumed Available online xxxx Pliocene increased tectonic activity on the Yunnan-Guizhou Plateau. The lake was thus considered to Communicated by Casim Umba Tolo be of tectonic origin, but supporting studies do not exist. Here we report and describe seven endemic spe- cies. The endemic gastropod Gyraulus luguhuensis exhibits an aberrant pseudo-dextral shell morphology, which is predominantly known from undisputed ancient lakes. To better understand the origin of the lake Keywords: and of its biodiversity, we present a preliminary geological study, which shows that Lake Lugu is a Ecosystem structure Tectonic setting tectonic-solution lake. During a survey of the aquatic habitats up to 21 gastropod morphospecies could Endemic species be differentiated macro-morphologically. An aberrant neritid-like Radix was genetically studied for the Molecular-clock first time. The genetic data suggest that Lugu-Radix, typical and neritid shell shapes, constitute a clade, comprising four possibly endemic evolutionary lineages, which potentially represent four different spe- cies. The molecular-clock approach indicates a Late Pliocene to Early Pleistocene origin of the clade, which we consider the minimum age of Lake Lugu. Our study reveals that the biodiversity in general and that of gastropods in particular is significantly higher than previously known. Against this back- ground and considering the co-occurrence of aberrant Gyraulus and Radix with an evolutionary history of more than two million years, Lugu is putatively an ancient lake. Ó 2020 International Association for Great Lakes Research. Published by Elsevier B.V. All rights reserved.
Introduction been considered ancient due to its tectonic origin and its high diversity of cichlid fish (Fryer and Iles, 1972; Fryer, 1997; but, since Lake Lugu (Lugu Hu) is located on the northern Yunnan- the relatively young age of the current lake stand was demon- Guizhou Plateau (Fig. 1). It has been considered to be an ancient strated (Johnson et al., 1996; Stager and Johnson, 2008) most lake (e.g. Shu et al., 2013; Zhang et al., 2015; Cheng et al., 2018), authors no longer consider it as an ancient lake (e.g. Wilke et al., such as Baikal, Tanganyika, Ohrid or Biwa (Martens et al., 1994; 2008b). In respect of Lake Lugu neither the geological age is known Rossiter and Kawanabe, 2000; Ivanov et al., 2003; Coulter et al., nor has the biodiversity been studied in some detail. Lake Lugu has 2006; Wilke et al., 2008a, Hampton et al., 2018). These lakes have been considered a tectonic lake (e.g. Shu et al., 2013; Zhang et al., in common a great geological age of several million years, and they 2013; Sheng et al., 2015) likely based on general tectonic concepts represent biodiversity hotspots with high rates of endemism. How- of the Yunnan-Guizhou Plateau, which represents an extension of ever, there exist a couple of smaller potential or putative ancient the Tibetan Plateau, suggesting that major tectonic activity started lakes with higher biodiversity and endemism as the average with between 5 Ma (Westaway, 2009) and 2 Ma (Wang and Burchfiel, an age of several hundred thousand or possibly a few million years, 2000). The Lugu drainage basin is located in a back-arc region such as Lake Prespa (Albrecht et al., 2008), Lake Trichonis (Albrecht (Fan and Zhang, 1994); the principle compressive stress is consid- et al., 2009), Lake Lanao (Stelbrink et al., 2019) or Lake Eg˘irdir ered NW-SE (Shen et al., 2003) or N-S (Shi et al., 2009). Possibly, (Wilke et al., 2007). In contrast, Lake Victoria, e.g., has formerly the idea that Lake Lugu is geologically old was derived from such large-scale tectonic settings. There are no data published, however, which have actually focused on the tectonic setting of the Lake ⇑ Corresponding author. Lugu area proper. On the other hand, the age of tectonic processes E-mail address: [email protected] (R. Wiese). https://doi.org/10.1016/j.jglr.2020.06.003 0380-1330/Ó 2020 International Association for Great Lakes Research. Published by Elsevier B.V. All rights reserved.
Please cite this article as: R. Wiese, C. Clewing, C. Albrecht et al., How ancient is Lake Lugu (Yunnan, China)? The gastropods’ viewpoint with focus on Radix (Lymnaeidae), Journal of Great Lakes Research, https://doi.org/10.1016/j.jglr.2020.06.003 2 R. Wiese et al. / Journal of Great Lakes Research xxx (xxxx) xxx
Fig. 1. Location of Lake Lugu and general outline of the lake (upper right). is not necessarily in phase with the age of a corresponding lake, at an elevation of ca. 2,690 m a.s.l. and has a larger northern basin which may have developed much later. and a smaller southern basin, separated by a tapering peninsula The bedrocks of the Lugu lake basin mainly consist of Permian (Wang et al., 2016; Figs. 1–4). The lake spans a total area of ca. and Triassic limestones, mudstones and sandstones (Chengdu 50 km2; the catchment area is ca. 170 km2 (Wu et al., 1997; Institute of Geology and Mineral Resources & China Geological Wang et al., 2016). The northern lake basin has a maximum depth Survey, 2004; Sheng et al., 2015). The lake lies in an alpine setting of ca. 100 m, the southern basin does not exceed 60 m water depth
Fig. 2. Bathymetric chart of Lake Lugu (after Department of Environmental Protection, 2010), including sample locations of all genetically analysed Radix specimens.
Please cite this article as: R. Wiese, C. Clewing, C. Albrecht et al., How ancient is Lake Lugu (Yunnan, China)? The gastropods’ viewpoint with focus on Radix (Lymnaeidae), Journal of Great Lakes Research, https://doi.org/10.1016/j.jglr.2020.06.003 R. Wiese et al. / Journal of Great Lakes Research xxx (xxxx) xxx 3
Fig. 3. Digital elevation model (SRTM; m a.s.l.) topography of the larger Lake Lugu area with preliminary documentation of major tectonic faults based on field studies and remote sensing. The main tectonic compression is from the north.
(Department of Environmental Protection, 2010; Fig. 2). The lake´s The state of the art of the biodiversity of the lake is difficult to outflow behaviour appears to vary significantly because the lake outline because the miscellaneous groups of organisms have been is either considered closed from September to May (Wang et al., studied in quite different detail. Twelve species of fish have been 2014, 2015) or semi-closed from January to May (Zhao et al., described. Three of the fish species are endemic, but eight are exo- 2008). The outflow, the Gaizu River, drains the lake via the Caohai tic (Kong et al., 2006). In gastropods the diversity is less well- wetland (Wang et al., 2015, 2016; Figs. 2–4). The lake is monomic- known. Shu et al. (2013), e.g., listed four Radix species for Lake tic with a strong thermal stratification during the summer months Lugu referring to Zhang et al. (1997) who, however, did not clearly (Wang et al., 2016, Wen et al., 2016). The water retention time has assign these species to the lake but to the region in general. Zhang been calculated to ca. 18 years (Wu et al., 1997). The water temper- et al. (1997) listed 18 Radix species for Yunnan in total, while ature ranges from ca. 7 °Cto23°C(Zhang et al., 2013; Wang et al., Aksenova et al. (2018) estimated only 1–2 species. Among the Lake 2016; Cheng et al., 2018). Due to a Secchi-disk inferred water Lugu macro-invertebrates the larvae of chironomid insects are transparency of up to 15 m the lake is oligotrophic (Whitmore likely most diverse (Zhang et al., 2013), but altogether only the gas- et al., 1997; Wu et al., 2008; Wang et al., 2015). No exceptional tropod Gyraulus luguhuensis (Fig. 4 panel 8) and two gammarid hydro-chemical features have been described (Wu et al., 1997, species are considered endemic (Hou and Li, 2003; Shu et al., 2008). The pH ranges from 7.4 to 9.6 (Wu et al., 2008; Zhang 2013). The gastropod Valvata ‘‘luguensis” is another potentially et al., 2013, Wen et al., 2016). Water pollution caused by tourism endemic species, but was only mentioned by Du et al. (2017) and and agriculture has increased significantly during the last two dec- not formally described or depicted. ades (Wu et al., 2008; Liu et al., 2019). The climate exhibits mon- The viviparid gastropod Margarya, which occurs in Lake Lugu soon seasonality with highest precipitation during summer was considered endemic to the Yunnan-Guizhou Plateau (Nevill, months. The amount of annual precipitation ranges from ca. 800 1877; Mabille, 1886; Zhang et al., 1997; Zhang et al., 2015) but to 1000 mm (Sheng et al., 2015; Wang et al., 2016). Mean July tem- recent studies exhibited a more complex situation (Stelbrink perature is 17.5 °C and mean January temperature 5.2 °C(Sheng et al., 2020). Lake Lugu micro-invertebrates such as ostracods are et al., 2015). often known at the generic level only (Zhu et al., 2015). Gom-
Please cite this article as: R. Wiese, C. Clewing, C. Albrecht et al., How ancient is Lake Lugu (Yunnan, China)? The gastropods’ viewpoint with focus on Radix (Lymnaeidae), Journal of Great Lakes Research, https://doi.org/10.1016/j.jglr.2020.06.003 4 R. Wiese et al. / Journal of Great Lakes Research xxx (xxxx) xxx
Fig. 4. Overview of the Lake Lugu ecosystem with selected habitats. Panel 1) View from Gemu Mountain to the eastern part of the northern lake basin; yellow arrow points at Anna Er (Dazui) Island (sample point 5 in Fig. 2); panel 2) View from Gemu Mountain to the western parts of the northern and southern basins; Liwubi Island (red arrow, sample point 6 in Fig. 2) lies at the morphological boundary of the two main basins; yellow arrow points at Xiewa Er (Heiwawu) Island (sample point 12 in Fig. 2), just in front of which the lake is deepest (ca. 100 m); blue arrow points at Lige Island; panel 3) View along the northern shore of the lake; yellow arrow points at Anna Er (Dazui) Island), red arrow at Lise Island; panel 4) View to the south across the northern basin; yellow arrow points at Xiewa Er (Heiwawu) Island, red arrow at Liwubi Island; panel 5) View from the south with Gemu Mountain in the background; blue arrow points at Lige Island, yellow arrow at Xiewa Er (Heiwawu) Island and red arrow at Liwubi Island; panel 6) Transition between the lake in the southern basin and the Caohai wetland (sample point 10 in Fig. 2); panel 7) Characteristic limestone boulder littoral; panel 8) An undescribed keeled Gyraulus (arrow) likely related to the endemic Gyraulus luguhuensis grazes over the submersed root of a camphor tree (Cinnamomum camphora). (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.) phosinica lugunsis represents the single known diatom, endemic to the geological setting to get first ideas about the lake-basin forma- the lake (Cheng et al., 2018). The total number of seven endemic tion and dynamics, respectively; b) the ecosystem structure to bet- species appears low in comparison to well-known ancient lakes ter outline the aquatic habitat diversity; c) the morphological (e.g. Wilke et al., 2008a). Because the fauna and flora of Lake Lugu, biodiversity of the aquatic gastropods to estimate species numbers with the possible exception of fish diversity, have not been exam- and identify potential endemics; d) the genetic analysis of poten- ined in depth, the chance to identify further endemic taxa is quite tially endemic morphotypes of the gastropod genus Radix; e) the high, particularly by applying genetic methods. genetic diversity of Lake Lugu Radix in the context of Eurasian The main aim of the study is to test the hypothesis that Lake Radix in general and f) applied the molecular-clock approach to Lugu represents an ancient lake. We therefore have studied a) infer the approximate minimum age of the lake.
Please cite this article as: R. Wiese, C. Clewing, C. Albrecht et al., How ancient is Lake Lugu (Yunnan, China)? The gastropods’ viewpoint with focus on Radix (Lymnaeidae), Journal of Great Lakes Research, https://doi.org/10.1016/j.jglr.2020.06.003 R. Wiese et al. / Journal of Great Lakes Research xxx (xxxx) xxx 5
Materials and methods 7.2.5 (Hall, 1999) resulting in a final length of 600 bp. The non- coding gene fragment 16S was aligned with the online tool MAFFT Sampling [https://www.ebi.ac.uk/Tools/msa/mafft;(Katoh and Standley, 2013); default settings] resulting in a final partition length of Field campaigns at Lake Lugu and outside the drainage basin 447 bp. were conducted in October 2011, September to October 2014 and August 2015. Geological structures were examined using a micro- Molecular-clock analysis structure compass, a geological hammer, and by more general observations with photographic documentation e.g. of extension Reconstruction of phylogenetic relationships and estimation of and patterns of rock types, anticlines, and faults, including under divergence times were performed with BEAST version 1.8.4 water observations by snorkel diving. The habitat and biological (Drummond et al., 2012) on the CIPRES Science Gateway web por- diversity was screened in shallow littoral areas by optical means tal (Miller et al., 2010). Substitution models were selected using and manual collection of the gastropods with the aid of a sieve jModelTest version 2.1.4 (Darriba et al., 2012) by using the cor- (1.5 mm mesh size). Sampling by snorkel diving was down to rected Akaike information criterion (AICc) which selected the 6 m water depth. Sampling was successful down to 25 m water HKY + I + C model for the COI partition and GTR + I + C model depth by using a dredge pulled behind a boat. The Caohai wetland for 16S partition. was entered by boat from the lake and on foot from the terrestrial In order to time calibrate the phylogenetic tree, we selected edges and a bridge. Generally numerous sites were checked. Bio- Radix socialis with an estimated age of 16.5 Ma [record from logical samples from Lake Lugu and the Caohai wetland are from Salvador & Rasser (2014)]. Age estimation after Aksenova et al. 35 studied locations. Biological samples were preserved in 90% (2018)], was used to calibrate the MRCA (most recent common ethanol and are deposited in the University Giessen Systematics ancestor) of Radix s. str. The analyses were run using the following and Biodiversity (UGSB) collection (Justus Liebig University Gies- settings: substitution and clock models unlinked, monophyly of sen, Germany) and the Natural History Museum in Berlin (Ger- ingroup, speciation = birth–death process, calibration point with many). Rock samples were kept in plastic bags and are deposited a gamma distribution prior: offset = 16.5, scale = 4.5; uniform prior at Yunnan University (Kunming, China). for substitution rates; number of MCMC generations = 20,000,000; sample frequency = 1,000. DNA isolation, PCR, and sequencing Two analyses were performed using either the strict-clock model and the uncorrelated lognormal relaxed-clock model. Tree Genomic DNA was extracted from a total of 19 Radix individuals files were summarized in TreeAnnotator version 1.8.4 (BEAST using the CTAB protocol described by Wilke et al. (2006).We package; node heights = mean heights). Effective sample size amplified two partial mitochondrial genes: (1) cytochrome oxidase (ESS) values were visualized on Tracer version 1.5 (Drummond c subunit I (COI) and (2) large ribosomal subunit (mtLSU rRNA or and Rambaut, 2007), showing ESS values >300 for the strict-clock 16S). Primers for the 16S fragment (16Sar and 16Sbr) were taken model and ESS values <300 for the relaxed-clock model. from Palumbi et al. (1991). For the COI fragment, we developed two internal primers RadixInt-F (50-AGAGGNCCWATYGCH Genetic distances CAYGGNGG-30) and RadixInt-R (50-GCNCCTAAAATTCTNGATA-30) which are used in combination with the primers of Meyer (2003; The mean genetic distances (p-distances) between Lake Lugu- dgHCO2198 and dgLCO1490). PCR cycling conditions were as fol- subclades A–D were calculated for each partition (COI and 16S) lows: an initial denaturation step at 95 °C for 60 s, followed by using MEGA version 6.06 (Tamura et al., 2013). 35 amplification cycles (denaturation at 95 °C for 30 s, annealing at 52 °C for 30 s, and elongation at 72 °C for 30 s), terminated by Digital image processing a final extension step at 72 °C for 180 s. PCR products (forward and reverse sequences) were visualized on an ABI3730XL sequen- Digital elevation modelling is based on USGS SRTM data, using cer at LGC Genomics (Berlin, Germany) using the Big Dye Termina- sheet n27_e100_1arc_v3, available in GeoTiff format (U.S. tor Kit (Life Technologies). DNA and specimen vouchers are stored Geological Survey, 2017, retrieved in November 2019). The data in the UGSB collection (see Table 1 for voucher numbers). were processed with ArcGIS Desktop 10 (ESRI Inc., 2010) and later on processed with Photoshop 4 and Inkscape 0.92.3. Dataset compilation and alignment Photos for shell descriptions and size measurements were taken with a Keyence VHX-1000 digital microscope. Pictures of micro- For comparison, our molecular dataset (19 COI and 6 16S sculpture and protoconchs were taken with the aid of a ZEISS scan- sequences) was complemented with sequences available in NCBI ning electron microscope at the Freie Universität Berlin. Proto- GenBank (29 COI and 31 16S sequences, see Table 1). We only conch whorls were counted after Riedel (1993). focused on species belonging to the subgenus Radix s. str. The final Plates were arranged with Adobe Photoshop CS4 and Inkscape dataset (excluding the outgroup) consists of 56 specimens repre- 0.92.3. senting 7 nominal species and Radix spp. from 15 countries scat- tered across Eurasia (for details see Table 1). The following Results specimens, which represent the closest relatives of the subgenus Radix s. str. according to Aksenova et al. (2018), were used as out- Geological setting and ecosystem structure group taxa: Ampullaceana fontinalis (GenBank accession number COI: EU818802/ GenBank accession number 16S: JN794347), Cera- The upper lithosphere of the Lugu Lake area is heavily fractured sina oxiana (JN794506/JN794336), Orientogalba ollula (JN794492/ by tectonics, representing the main control of surface processes e.g. JN794301), Radix rufescens (–/JN794309), and Tibetoradix hookeri water flow causing valley incisions. Major faults are preferably (JN794429/JN794204). trending in approximately N-S and W-E directions (Fig. 3). This is The alignment of the protein-coding gene fragment COI was in phase with several studied anticlines, roughly trending W-E done by eye using the sequence alignment editor BioEdit version and exhibiting major compression from the north. Stronger devia-
Please cite this article as: R. Wiese, C. Clewing, C. Albrecht et al., How ancient is Lake Lugu (Yunnan, China)? The gastropods’ viewpoint with focus on Radix (Lymnaeidae), Journal of Great Lakes Research, https://doi.org/10.1016/j.jglr.2020.06.003 6 R. Wiese et al. / Journal of Great Lakes Research xxx (xxxx) xxx
Table 1 List of genetically studied specimens including taxon, specimen code, locality information, voucher number (stored at the UGSB database), and GenBank accession numbers. All newly sequenced specimens are highlighted in bold.
Species Specimen Location/Site Number Lake Lugu (Fig. 2) Coordinates Voucher GenBank accession GenBank accession no. code (°N/°E) no. no. COI 16S rRNA R. alticola NP03/1 Nepal, Bagmati, Taudaha Lake 27.65000/ UGSB JN794495 JN794321 85.15000 7507 TJ02/1 Tajikistan N/A Mlym142 MH189953 1 R. auricularia AM01/1 Armenia, Kotayk Province 40.49962/ UGSB JN794351 JN794125 44.73923 7318 AM02/1 Armenia, Gegharkunik Province 40.18082/ UGSB JN794353 JN794127 45.22989 7320 CN19/1 China, Qinghai 35.43374/ UGSB JN794427 JN794202 93.60115 7395 CN44/1 China, Tibet 29.27210/ UGSB JN794471 JN794246 88.89421 7439 DE01/1 Germany, Thuringia 50.67280/ UGSB EU818800 JN794284 11.48558 0300 RU01/1 Russia, Krasnodar Krai 45.29897/ UGSB JN794508 JN794338 37.29839 7524 RU03/1 Russia, Omsk Oblast 54.91667/ UGSB JN794509 JN794341 73.36667 7527 TJ01/1 Tajikistan, Gorno-Badakhshan, Lake Karakul 39.02164/ UGSB JN794513 JN794346 37.48873 7532 R. brevicauda CN03/1 China, Tibet, Yamdrok Yumtso 29.03494/ UGSB JN794364 JN794138 90.42122 7331 CN06/3 China, Tibet, Tso Nak 32.02789/ UGSB JN794381 JN794155 91.53130 7348 CN35/1 China, Tibet 30.51992/ UGSB JN794459 JN794234 82.60483 7427 CN39/1 China, Tibet 33.41844/ UGSB JN794464 JN794239 79.64039 7432 CN43/1 China, Tibet, Yadang Tso 29.63267/ UGSB JN794470 JN794245 85.74019 7438 CN46/1 China, Tibet, Kyering Tso 30.76610/ UGSB JN794475 JN794251 85.01230 7444 R. euphratica TJ03/1 Tajikistan, Lake Bazovskoe N/A Mlym138 MH189943 1 R. makhrovi CN72/1 China, Tibet, Brahmaputra River basin 29.35667/ Mlym35 MH189860 90.71528 CN72/2 China, Tibet, Brahmaputra River basin 29.35667/ Mlym36 MH189861 90.71528 R. plicatula CN53/1 China, Yunnan, Lake Xingyun 24.38078/ UGSB JN794482 JN794269 102.80719 7462 CN54/2 China, Yunnan, Lake Qilu 24.19123/ UGSB JN794485 JN794273 102.81068 7466 CN55/1 China, Yunnan, Lake Yangzong 24.86115/ UGSB JN794487 JN794275 102.99083 7468 CN56/2 China, Yunnan, Lake Yangzong 24.87302/ UGSB JN794489 JN794279 103.00794 7472 R. rubiginosa ID02/1 Indonesia, Flores Island, Lake Sano Ngoang N/A Mlym108 MH189926 TH02/1 Thailand N/A IEPN- KM067685 G360.9 Radix sp. CN59/1 China, Yunnan, Lake Lugu (3) 27.74004/ UGSB MT344016 (subclade A) 100.76496 23379 CN60/1 China, Yunnan, Lake Lugu, Liwubi Island 27.68700/ UGSB MT344013 MT345554 (south) (6) 100.78417 23369 CN60/2 China, Yunnan, Lake Lugu, Liwubi Island 27.68700/ UGSB MT344014 (south) (6) 100.78417 23370 CN61/1 China, Sichuan, Lake Lugu (10) 27.68850/ UGSB MT344020 100.83417 23389 CN62/1 China, Yunnan, Lake Lugu, Xiewa Er Island 27.70667/ UGSB MT344017 (12) 100.77500 23381 CN63/1 China, Sichuan, Lake Lugu, Anna Er Island 27.74233/ UGSB MT345553 (5) 100.79933 24255 CN64/1 China, Sichuan, Lake Lugu, House of 27.69817/ UGSB MT344023 Princess Island (9) 100.82033 24259 CN65/1 China, Sichuan, Lake Lugu (4) 27.74433/ UGSB MT344015 100.78717 23,377 CN66/1 China, Sichuan, Lake Lugu (7) 27.69167/ UGSB MT344021 100.79800 2391 CN67/1 China, Yunnan, Lake Lugu (2) 27.72733/ UGSB MT344018 100.75767 23383
Please cite this article as: R. Wiese, C. Clewing, C. Albrecht et al., How ancient is Lake Lugu (Yunnan, China)? The gastropods’ viewpoint with focus on Radix (Lymnaeidae), Journal of Great Lakes Research, https://doi.org/10.1016/j.jglr.2020.06.003 R. Wiese et al. / Journal of Great Lakes Research xxx (xxxx) xxx 7
Table 1 (continued)
Species Specimen Location/Site Number Lake Lugu (Fig. 2) Coordinates Voucher GenBank accession GenBank accession no. code (°N/°E) no. no. COI 16S rRNA CN68/1 China, Yunnan, Lake Lugu (11) 27.67533/ UGSB MT344019 100.82283 23387 Radix sp. CN63/2 China, Sichuan, Lake Lugu, Anna Er Island 27.74233/ UGSB MT344008 MT345557 (subclade B) (5) 100.79933 23357 CN63/3 China, Sichuan, Lake Lugu, Anna Er Island 27.74233/ UGSB MT344009 (5) 100.79933 23358 Radix sp. CN69/1 China, Yunnan, Lake Lugu, Liwubi Island 27.68848/ UGSB MT344010 (subclade C) (north) (6) 100.78628 23359 CN69/2 China, Yunnan, Lake Lugu, Liwubi Island 27.68848/ UGSB MT344011 MT345556 (north) (6) 100.78628 23360 CN60/3 China, Yunnan, Lake Lugu, Liwubi Island 27.68700/ UGSB MT344024 (south) (6) 100.78417 24265 CN70/1 China, Yunnan, Lake Lugu (1) 27.71517/ UGSB MT344025 100.75550 2467 Radix sp. CN71/1 China, Sichuan, Lake Lugu, ‘Neighbour’ 27.69583/ UGSB MT344012 MT345555 (subclade D) Island (8) 100.81650 23366 Radix sp. CN45/2 China, Sichuan 30.66032/ UGSB JN794249 104.05583 7442 CN48/1 China, Yunnan, Lake Yilong 23.65618/ UGSB JN794258 102.62479 7451 CN52/1 China, Yunnan, Lake Fuxian 24.43796/ UGSB JN794266 102.85104 7459 CN57/1 China, Beijing 40.40722/ UGSB JN794281 116.31833 7474 GR01/1 Greece, Aetoloakarnania, Lake Trichonis 38.58893/ UGSB EU818823 JN794286 21.46703 0308 ID01/1 Indonesia, South Sulawesi 4.62763/ UGSB JN794287 119.62700 7477 IQ01/1 Iraq, Maysan Governorate 31.20037/ UGSB JN794292 46.99545 7482 JP01/1 Japan, Kyushu 33.42330/ UGSB JN794298 130.53200 7488 LA02/1 Laos, Vientiane 19.11667/ UGSB MT344026 MT345558 102.23333 14083 MM05/1 Myanmar, Shan, Lake Inle 20.52425/ UGSB JN794313 96.89895 7500 PH01/1 Philippines, Mindanao Island, Lake Lanao 7.88492/ UGSB MH319869 MH304361 124.31941 19912 PH01/2 Philippines, Mindanao Island, Lake Lanao 7.88492/ UGSB MH319870 MH304362 124.31941 19913 VN01/1 Vietnam, Kon Tum Province 14.98970/ UGSB JN794514 JN794348 107.75500 7533
tions from the general directions can be found in the mountain Opposite Liwubi Island and the main peninsula, an active alluvial ranges north and northwest of the lake and in the drainage basin fan penetrates the lake. Less extended fluvial-alluvial and slope proper. A NW-SE fault runs along the north-eastern flank of Gemu deposits can be found in several areas and usually represent more Mountain (3752 m), a second one ca. 6 km further to the northeast extended shallow lake habitats with partly dense vegetation. In and a third one ca. 10 km to the southwest at Yongning town some areas, e.g. around Xiewa Er Island, submerged roots of living (Fig. 3). About 10 km NNE from Yongning, a hot spring is related trees characterize the littoral (Fig. 4 panel 8). Characea meadows to a fracture. The south-eastern shore of the lake’s northern basin were found down to 25 m water depth e.g. in Lige Bay. The water is partly controlled by NE-SW trending faults. transparency was generally higher in the northern basin (12–14 m) The faults controlling the southern lake basin, including the than in the southern basin (6–8 m). The outflow of the lake, Gaizu Caohai wetland, trend from ENE-WSW. The fault along the north- River (Fig. 3), was active in July as well as in October. ern boundary of the wetland is considered normal. East of the wet- land, two faults are crossing without significant shearing, however. Field observations with focus on Lake Lugu gastropods Liwubi Island (Fig. 4.5) sheared dextrally from the main peninsula and thus represents its former tip. During the study of the aquatic habitats, the focus was on the The hard rocks in the lake basin mainly consist of gray lime- gastropods, but some additional observations are included. Ten stone, black mudstone and yellowish or reddish sandstone. Locally, gastropod genera of seven families could be identified (Table 2). basalts and volcanic breccia can be found. The shoreline is either We present the first record of a pomatiopsid species, which was characterized by the rocks or by their weathering products. Karsti- dredged in Lige Bay from Characea meadows in a water depth of fication of limestone is evident all over the area. All islands except 14–25 m. The number of gastropod species (15–21) compiled in Lige Island consist mainly of limestone and partly exhibit the shape Table 2 represents an estimation based on supposed macro- of a cone karst top, e.g. Anna Er and Xiewa Er islands (Fig. 4). The morphological differences. The largest gastropods living in Lake lake shores are generally steep, except for the transition to Caohai Lugu, the viviparids Cipangopaludina and Margarya were mainly wetland and in areas with fluvial-alluvial deposits. The largest allu- found on boulders and pebbles, sometimes on soft substrates, pre- vium interacts with the western Caohai wetland (Fig. 4 panel 6). dominantly in the upper 3 m of the lake. Denser populations could
Please cite this article as: R. Wiese, C. Clewing, C. Albrecht et al., How ancient is Lake Lugu (Yunnan, China)? The gastropods’ viewpoint with focus on Radix (Lymnaeidae), Journal of Great Lakes Research, https://doi.org/10.1016/j.jglr.2020.06.003 8 R. Wiese et al. / Journal of Great Lakes Research xxx (xxxx) xxx
Table 2 Estimated number of gastropod morphotypes and their distribution and their qualitative abundance within Lake Lugu, based on field observations and intensive sampling (see Materials and methods). Distribution categories: widespread: found at numerous sites, Patchy: found at few sites, Restricted: found only at one site. Abundance categories: High >10, medium: 2–10, low: 1.
Family Genus Morphs Distribution Abundance Viviparidae Lamarck, 1809 Cipangopaludina Hannibal 1912 1–2 Widespread High Margarya Nevill, 1877 1–2 Widespread High Sinotaia Haas, 1939 1–2 Widespread High Bithyniidae Troschel, 1857 aff. Hydrobioides Nevill, 1884 1–2 Patchy High Pomatiopsidae Stimpson, 1865 genus indet. 1 Restricted Low Valvatidae Gray, 1840 Lymnaeidae Rafinesque, 1815 Valvata O.F. Müller, 1773 1 Patchy Low Radix Montfort, 1810 3–4 Widespread High (incl. neritid-like morphotype) Galba Schrank, 1803 1 Restricted Medium Planorbidae Rafinesque, 1815 Gyraulus Charpentier, 1837 4–5 Widespread Medium to high (incl. G. luguhuensis) Physidae Fitzinger, 1833 Physa Draparnaud, 1801 1 Widespread Medium
be found around Lise and Anna Er islands but locally also in pro- relatively high numbers on carbonatic rock at the air–water- tected bays of the lake shore or at the transition to the Caohai wet- interface, often exposed to the wave surge. The aberrant Radix land. Differences in shell morphology such as angulation of whorls has not been mentioned in literature and is therefore the focus of and prominence of spiral sculpture suggest that each of the two genetic and more detailed morphological studies. genera may comprise two species living in Lake Lugu. Populations were partly intermixed. Fish (Schizothorax spp.) were observed to Phylogenetic relationships and time of divergence attack Margarya and Cipangopaludina by crashing the shell from the aperture as well as from the apex. The third viviparid genus, The Radix specimens found in Lake Lugu cluster within clade 3 the significantly smaller Sinotaia, was mainly found in the upper (Bayesian Posterior Probability, BPP = 1.00, see Fig. 5) containing R. 1 m of the lake. Generally, specimens had either well-rounded or alticola from Nepal and Tajikistan, R. euphratica from Tajikistan, R. slightly but significantly angulated whorls. The populations out- plicatula from China, and Radix spp. from Vietnam, China, Indone- numbered those of Margarya and Cipangopaludina. Near settle- sia, Japan, Laos, Myanmar, Iraq, and Greece. Clade 3 is sister to ments, populations were particularly dense. Locally, Sinotaia was clade 1 (R. auricularia from Armenia, China, Germany, Russia, and sympatric with Margarya and/or Cipangopaludina. A bithyniid Tajikistan), clade 2 and 13 (R. brevicauda and R. makhrovi, respec- resembling Hydrobioides, from here-on called Hydrobioides, was tively; both endemic to the Tibetan Plateau, China), and clade 14 often found in large numbers in shallow water, on boulders and (R. rubiginosa and Radix sp. from Indonesia, Philippines and Thai- pebbles. The shell shape somewhat varied between populations. land). All mentioned clades are highly supported (BPP = 1.00; see At one site, in ca. 25 m water depth, few Hydrobioides individuals Fig. 5) and their relationships are consistent with previous molec- were found, but egg masses of the genus were abundant. At this ular phylogenetic studies on Radix (Oheimb et al., 2011; Clewing site a palaeo-shoreline could be identified, characterized by flat- et al., 2016). Note that the clades (except for clade 14) are named tened gravels and shell detritus. It is noteworthy that sponges were according to Oheimb et al. (2011) and Clewing et al. (2016). living in the same habitat. Among the pulmonate gastropods, Physa For the Lake Lugu specimens, our phylogeny revealed the exis- was found attached to water plants in a couple of shallow water tence of four well-supported subclades (A–D; = 0.70–1.00; see habitats including the Caohai wetland. The sampled Physa speci- Fig. 5), however, their relationships remain uncertain mens did not show recognizable shell morphological differences (BPP = 0.55). While subclade A consists of specimens with typical and were therefore considered a single morpho-species. Radix shells, clades B, C and D, which do not form a monophyletic Gyraulus was present in the lake proper with two typical shell group, consist of specimens with a neritid-like shell form. types: a larger one which was found in several locations in shallow The split between the Lake Lugu clades (node N1; see Fig. 5) and water on pebbles and water plants, and a smaller type which was the sister was estimated to have occurred 4.69 Ma (95% highest found locally in Lige Bay attached to Characea in a water depth of posterior density, 95% HPD = 5.61–2.61 Ma), whereas the splitting about 19 m. The aberrant pseudo-dextral Gyraulus luguhuensis rep- of the Lake Lugu clades (node N2; see Fig. 5) was estimated at resents a third shell type. The shell morphology differed signifi- 3.62 Ma (95% HPD = 5.09–2.37 Ma). cantly between certain habitats, however. Shells of specimens The mean genetic distance between the Lake Lugu clades ran- living around Xiewa Island were distinctly keeled (Fig. 4 panel 8), ged from minimum 3.5% (between subclades A and D) to maxi- while in other habitats the keel was little developed or even miss- mum 4.7% (between subclades A and B) in COI (see Table 3) and ing. The Xiewa Island Gyraulus luguhuensis was more common on from minimum 0.9% (between subclades A and C) to maximum submersed tree roots than on pebbles. Another, relatively large 2.5% (between subclades A and B) in 16S rRNA (see Table 3). Gyraulus morphotype was sampled from submersed Caohai wet- land vegetation. Shell morphologies and habitats of Radix subclades The genus Radix exhibited two morphotypes: a typical shell and a relatively small, aberrant, neritid-like shell. The typical Radix was Radix Lugu subclade A (Fig. 6A, 7A; 11 specimens examined) found on most shallow-water hard substrates including water Habitat: Littoral waters with depths of up to 1.5 m, attached to plants and partly sympatric with the neritid-like Radix, e.g. around all types (carbonatic, basaltic, etc.) of available rocks, boulders, Buwa (House of Princess) Island in the southern lake basin (sample pebbles, gravels, and attached to water plants. Distribution: Found point 6 in Fig. 2) or around Liwubi Island (Fig. 4 panel 5). With the at several locations along the shores of the lake (see Fig. 2). Shell exception of the exposed tip of a peninsula (sample location 1 in description: Maximum height 22 mm, maximum width 12 mm; Fig. 2), the neritid-like Radix was found around the islands only up to 4.5 whorls (including protoconch, largest specimen); aper- (except for Lige Island). In all sites the neritid-like Radix lived in ture height 12 mm, aperture width 7 mm; high, pointed spira (ap-
Please cite this article as: R. Wiese, C. Clewing, C. Albrecht et al., How ancient is Lake Lugu (Yunnan, China)? The gastropods’ viewpoint with focus on Radix (Lymnaeidae), Journal of Great Lakes Research, https://doi.org/10.1016/j.jglr.2020.06.003 R. Wiese et al. / Journal of Great Lakes Research xxx (xxxx) xxx 9
Fig. 5. BEAST MCC tree showing the phylogenetic relationships of the genus Radix s. str. based on a concatenated dataset of COI and 16S rRNA. Lake Lugu specimens are highlighted with coloured boxes (turquoise box = normal shell shape; green boxes = neritid-like shell shape), subclades A–D are shown. Specimens are indicated by specimen codes (for details see Table 3). Bayesian posterior probabilities (<0.50) are provided next to the respective branch. Clade 1–3 were named according to Oheimb et al. (2011), the two R. makhrovi from Tibet resemble clade 13 from Clewing et al. (2016), while clade 14 is renamed in this study. The fossil calibration is based on Aksenova et al. (2018). (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)
proximately 1/4 of the shell height); convex body whorl, pointed Table 3 Mean genetic p-distances (%) between Lake Lugu-subclades A–D based on the apex, egg-shaped aperture with kinked columellar margin; robust mitochondrial COI and 16S rRNA fragment (COI/16S). shell with smooth surface. Protoconch: 1.3 whorls, maximum diameter 0.6 mm, with spiral lirae. Clade A B C D Radix Lugu subclade B (Fig. 6B, 7B; 2 specimens examined) A– Habitat: Attached to littoral limestone rocks and boulders, directly B 4.7/2.5 – C 4.2/0.9 4.0/2.1 – at the wave surge. Distribution: Identified in sample location 5 (see D 3.5/1.3 4.5/2.2 4.5/1.3 – Fig. 2) Shell description: Maximum height 7 mm, maximum width 8 mm; up to 3 whorls (including protoconch, largest specimen);
Please cite this article as: R. Wiese, C. Clewing, C. Albrecht et al., How ancient is Lake Lugu (Yunnan, China)? The gastropods’ viewpoint with focus on Radix (Lymnaeidae), Journal of Great Lakes Research, https://doi.org/10.1016/j.jglr.2020.06.003 10 R. Wiese et al. / Journal of Great Lakes Research xxx (xxxx) xxx
Fig. 6. Shells of the four genetically analysed Radix subclades A–D. Scale bars: 0.5 cm. aperture height 5 mm, aperture width 6 mm; low, almost flattened almost flattened spira (approximately 1/6 of the shell height); spira (approximately 1/6 of the shell height). With rounded apex; rounded apex, egg-shaped, neritid-like aperture with straight col- egg-shaped, neritid-like aperture with straight columellar margin umellar margin and a steep outer lip; robust shell with smooth and a steep outer lip; robust shell with smooth surface. Proto- surface. Protoconch: 1.4 whorls, maximum diameter 0.7 mm, conch: 1.2 whorls, maximum diameter 0.6 mm, with spiral lirae. smooth surface except for growth increments. Radix Lugu subclade C (Fig. 6C, 7C; 2 specimens examined) Radix Lugu subclade D (Fig. 6D, 7D; 1 specimen examined) Habitat: Attached to littoral limestone rocks and boulders, directly Habitat: Attached to littoral limestone rocks and boulders, directly at the wave surge. Distribution: Identified in sample locations 1 at the wave surge. Distribution: Identified in sample location 8 (see and 6 (see Fig. 2). Shell description: Maximum height 8 mm, max- Fig. 2). Shell description: Height 6 mm, width 0.5 mm; 3 whorls imum width 7 mm; up to 3 whorls (including protoconch, largest (including protoconch); aperture height 0.5 mm, aperture width specimen); aperture height 6 mm, aperture width 5 mm; low, 3.5 mm; intermediately high spira (approximately 1/5 of the shell
Please cite this article as: R. Wiese, C. Clewing, C. Albrecht et al., How ancient is Lake Lugu (Yunnan, China)? The gastropods’ viewpoint with focus on Radix (Lymnaeidae), Journal of Great Lakes Research, https://doi.org/10.1016/j.jglr.2020.06.003 R. Wiese et al. / Journal of Great Lakes Research xxx (xxxx) xxx 11 height); rounded apex, egg-shaped, neritid-like aperture with an 2019). Possibly, the palaeo-shoreline discovered by us in ca. almost straight columellar margin and a convex outer lip; thin 25 m water depth corresponds with the LGM lake lowstand. shell with smooth surface. Protoconch: 1.1 whorls, maximum Lake Lugu is quite small for a potential ancient lake. Size appar- diameter 0.6 mm, smooth surface except for growth increments. ently matters when comparing the large (ca. 31,500 km2) and deep (max. ca. 1,650 m) Siberian Lake Baikal with about 1,500 endemic animal species (Kozhova and Izmest’eva, 1998; Gurkov et al., 2019) Discussion e.g., with Balkan Lake Ohrid (ca. 360 km2, max. depth ca. 290 m; Albrecht and Wilke, 2008), which is almost ninety times smaller Quite a few lakes of the Yunnan-Guizhou Plateau have been ter- by area. Lake Ohrid, however, still comprises about 185 endemic med ‘‘ancient” (Shu et al., 2013), but they all have in common that animal species (Albrecht and Wilke, 2008, Föller et al., 2015). It neither geological nor limnobiological studies have actually has been suggested that taking surface area and volume into demonstrated their ancient character. The term ‘‘ancient” was pos- account Lake Ohrid should be considered the lake with the highest sibly promoted because of the conspicuous and morphologically biodiversity worldwide (Albrecht and Wilke, 2008; Budzakovska- diverse viviparid gastropod ‘‘Margarya”, which, although poly- Gjoreska et al., 2014). Lake Lugu is approximately seven times phyletic (Du et al., 2013), has been considered endemic to the smaller by area than Lake Ohrid, and maximum water depth is Yunnan-Guizhou Plateau (Nevill, 1877; Mabille, 1886; Zhang about three times shallower, but these two lakes exhibit a couple et al., 1997; Zhang et al., 2015). Stelbrink et al. (2020) outlined that of common characteristics. Both are oligotrophic tectonic- the situation is taxonomically more complex and further studies solution lakes dominated by limestone karstification. In both cases, are required. Our own preliminary studies of these lakes show that geological and geomorphological climate-coupled processes of the only Lake Fuxian, which is much larger and deeper than Lake Lugu drainage basins have created highly diverse habitats for macro- (Li et al., 2010), may comprise a similarly high gastropod biodiver- fauna and -flora. Lake Ohrid and Lake Lugu have also in common sity. Regarding Lake Lugu, we therefore have started to build a geo- the occurrence of an endemic pseudo-dextral planorbid gastropod logical framework, which allows us to integrate our habitat and Gyraulus species (Radoman, 1985; Gorthner, 1992; Shu et al., 2013; biological studies and to propose a substantiated hypothesis on Albrecht et al., 2019; Fig. 4 panel 8). It is noteworthy that pseudo- its ancient lake status. dextral Planorbidae have also been found in ancient lakes Baikal Our studies of the geological setting of Lake Lugu suggest that and Biwa (Alexandrowicz, 1993; Nishino and Watanabe, 2000; the southern lake basin lies in a graben-like structure which com- Röpstorf and Riedel, 2004), but so far not in lakes Prespa, Lanao, prises a large syncline. Subsidence is indicated by normal faulting Trichonis or Eg˘irdir. and extension, e.g. by dextral shearing of Liwubi Island. The north- On the other hand, based on Balkan lake studies, Glöer and Pešic´ ern part of the northern lake basin exhibits a similar setting. Much (2008) suggested that endemic Radix species are characteristic of more detailed work, however, is needed to understand the suppos- ancient lakes. Following this line, the finding of an aberrant edly complex tectonic behaviors of both basins. The Lake Lugu neritid-like Radix in Lake Lugu triggered our genetic studies. Inter- basins are not controlled by tectonics alone but obviously also by estingly, this aberrant Radix form is not only apparently endemic to karstification of the widely distributed limestone. Four out of seven the lake, but it comprises three different subclades which might islands are considered to represent tops of cone karst. Therefore, even represent three different species. The genetic distances found the basins of Lake Lugu have at least partly been formed by solu- between the different subclades of Lake Lugu are clearly in the tion. The general geological setting is thus in phase with the idea range of mitochondrial variation at interspecific level found in that Lake Lugu may have existed for a long time. The palaeo- other lymnaeids (e.g. von Oheimb et al., 2011). The genetic data shoreline, which was detected ca. 25 m below modern lake level (Fig. 5) rather indicates that neritid-like Radix subclade B is sister has several implications. During that lake lowstand, all islands to typical Radix subclade A and not to the other neritid-like Radix except for Xiewa Er (Fig. 4 panel 5) were connected with the main- subclades C and D (Fig. 6). Although the general shell shapes and land. The outflow through the Caohai wetland was not active dur- sizes of subclades A and B differ greatly, the development of weak ing that time; the lake was endorheic and increased salinity would spiral lirae on the protoconchs (Fig. 7A and B) tentatively supports be expected. On the other hand, the fossil shells from the palaeo- the sister relationship of subclades A and B indicated by genetic shoreline represented the same gastropod morphotypes, which data. This protoconch sculpture was not found in subclades C were found alive in the modern littoral. This evidence supports and D (Fig. 7C and D). In this context it is noteworthy that the three the idea that the salinity of Lake Lugu did not increase significantly, neritid-like Radix subclades have in common a specific limestone either because it was a short-term lowstand only or, more likely, habitat at the air–water interface, while the typical Radix subclade because the lake has or had an underwater outflow via the karst. A has occupied a wide range of lake habitats. The neritid-like shell The relatively small catchment area of Lake Lugu, which is little shape thus appears to be primarily controlled by the specific envi- more than three times larger than the lake surface area may hint ronment, in the case of subclades A and B superimposing genetic at significant groundwater inflow and likely also originating from relationship. Radix pinteri, which is endemic to Balkan Lake Prespa, neighboring drainage basins. The deepest part of the lake is very and Radix onychia, endemic to Lake Biwa, exhibit neritid-like pointed (Fig. 2) and further investigation may show that it repre- shapes too (Albrecht et al., 2008, Yoshiba, 1965). These species sents a sinkhole. Although the real size of the Lugu drainage area are not closely related to Lake Lugu Radix. As such the shell shape may be much larger than can be seen from surface studies, a represents a parallel pattern. Although R. pinteri is ecologically long-term permanent lake ecosystem still requires a relatively broader than the Lugu subclades B–D, it can also be found com- stable climate. Data on vegetation dynamics suggest that the gen- monly on rocks and exposed to the surge (Albrecht et al., 2008). eral climate setting has not much changed since the Late Pliocene The same applies to R. onychia, which lives alongside the shoreline (e.g. Sun et al., 2011), and lake-desiccation events during the last of Lake Biwa and its adjacent river systems (Yoshiba, 1965). It can 3–2 Ma are thus unlikely. This presumption is in line with be speculated that the shells have been eco-phenotypically modu- sediment-core studies across the Last Glacial Maximum, which lated by this high energy habitat. However, aberrant shell mor- indicate that lake level and water temperature dropped during this phologies in Radix species, resembling neritid shells seem to be period of climate deterioration, but sedimentation continued and fostered in ancient lakes. freshwater organisms such as diatoms and cladocerans lived in All four Lake Lugu Radix subclades are most likely endemic. the lake, with a predominance of littoral taxa, (Wang et al., 2014, Interestingly, they are not closely related to the Tibetan Plateau
Please cite this article as: R. Wiese, C. Clewing, C. Albrecht et al., How ancient is Lake Lugu (Yunnan, China)? The gastropods’ viewpoint with focus on Radix (Lymnaeidae), Journal of Great Lakes Research, https://doi.org/10.1016/j.jglr.2020.06.003 12 R. Wiese et al. / Journal of Great Lakes Research xxx (xxxx) xxx
Fig. 7. Protoconchs of the four described Radix subclades A–D. Red arrows indicate the supposed transition between proto- and teleoconch. White arrows indicate spiral lirae on the protoconchs of subclades A and B. Subclade C is represented by two different specimens; C1: Transition between proto- and teleoconch; C2 and D1: Growth increments clearly visible; D2: Transition between proto- and teleoconch is clearly visible in the tipped-over view. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.) clades (von Oheimb et al., 2011) although the Yunnan Plateau rep- studies will have to test whether the ancestors of the Lugu sub- resents an extension of the Tibetan Plateau (Westaway, 2009). The clades have a (sub-)tropical Oriental origin. sister group of the Lake Lugu Radix clade is not a Yunnan specific Acknowledging the low node support in this part of the phylo- one but includes a wide range of Oriental populations and even genetic tree, the split between Radix Lugu clades A/B and C/D was some Palearctic lineages (von Oheimb et al., 2011; Clewing et al., used to infer the divergence time and thus the minimum age of 2016). Clewing et al. (2014) found that Lake Lugu Valvata is also Lake Lugu, which is ca. 2.4 Ma. This age is in phase with the geolog- not closely related to Valvata sp. from the Tibetan Plateau. Future ical and climate history of the north-western Yunnan Plateau
Please cite this article as: R. Wiese, C. Clewing, C. Albrecht et al., How ancient is Lake Lugu (Yunnan, China)? The gastropods’ viewpoint with focus on Radix (Lymnaeidae), Journal of Great Lakes Research, https://doi.org/10.1016/j.jglr.2020.06.003 R. Wiese et al. / Journal of Great Lakes Research xxx (xxxx) xxx 13
(Westaway, 2009; Sun et al., 2011). Our preliminary assessment of Albrecht, C., Wilke, T., 2008. Ancient Lake Ohrid: biodiversity and evolution. gastropod morphotype diversity (Table 2) with 21 in number Hydrobiologia 615, 103–140. Albrecht, C., Stelbrink, B., Clewing, C., 2019. Planorbidae Rafinesque, 1815. In: appears to be rather low for an ancient lake. However, this number Lydeard, C., Cummings, K.S. (eds.). Freshwater mollusks of the world. Johns should be treated with caution, because Lake Lugu is an alpine lake Hopkins University Press, Baltimore, USA, 181–186. with a comparably small size and the potentially existing cryptic Albrecht, C., Wolff, C., Glöer, P., Wilke, T., 2008. Concurrent evolution of ancient sister lakes and sister species: the freshwater gastropod genus Radix in lakes diversity, which has not been detected so far and therefore, cannot Ohrid and Prespa. Hydrobiologia 615, 157–167. be easily compared to tropical ancient lakes. Thus, the gastropod Albrecht, C., Hauffe, T., Schreiber, K., Trajanovski, S., Wilke, T., 2009. Mollusc diversity of Lake Lugu is in the range of other potential ancient biodiversity and endemism in the potential ancient lake Trichonis, Greece. Malacologia 51 (2), 357–375. lakes, such as those on the Balkans in Europe (Albrecht et al., Albrecht, C., Hauffe, T., Schreiber, K., Wilke, T., 2012. Mollusc biodiversity in a 2009). The genetic analysis of Radix hints at a potential species European ancient lake system: lakes Prespa and Mikri Prespa in the Balkans. flock and ongoing speciation. The finding of a distinctly keeled Hydrobiologia 682 (1), 47–59. Alexandrowicz, S.W., 1993. Biometrical study of Choanomphalus maacki Gersfeldt, pseudo-dextral Gyraulus at the central island (Xiewa Er; Fig. 4 1859 from the Baikal Lake. Folia Malacologica 5, 97–107. panel 2) and of shell morphs intermediate between the new mor- Budzakovska-Gjoreska, B., Trajanovski, S., Trajanovska, S., 2014. Comparative photype and the unkeeled Gyraulus luguhuensis (Shu et al., 2013, biocenological analysis of Gastropoda on the Macedonian part of Lake Ohrid described from a single mainland-shore location) may hint at and its watershed. Biologia 69 (8), 1023–1029. Cheng, Y., Liu, Y., Kociolek, J.P., You, Q., Fan, Y., 2018. A new species of Gomphosinica another Lake Lugu gastropod species flock. A comparable high (Bacillariophyta) from Lugu Lake, Yunnan Province, SW China. Phytotaxa 348 amount of Gyraulus morphotypes is known from Miocene sedi- (2), 118–124. ments of the Steinheim palaeolake, in southern Germany Chengdu Institute of Geology and Mineral Resources & China Geological Survey, 2004. Geological map of Qinghay-Xizang (Tibet) Plateau and adjacent areas. (Hilgendorf, 1866; Rasser, 2014). 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Please cite this article as: R. Wiese, C. Clewing, C. Albrecht et al., How ancient is Lake Lugu (Yunnan, China)? The gastropods’ viewpoint with focus on Radix (Lymnaeidae), Journal of Great Lakes Research, https://doi.org/10.1016/j.jglr.2020.06.003