Morphological and genetic variation of Artemia sinica in Yuncheng Salt Lake over the past 30 years
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摘要: 卤虫是海水鱼类及甲壳类苗种培育中重要的活饵料，90%以上来源于野生卤虫资源。为探究近30 a环境变化与独特养殖管理模式对中国运城盐湖卤虫形态学及遗传特征的影响，本研究对1993年（YC-1993）、2019年（YC-2019）和2023年（YC-2023）采自运城盐湖的卤虫卵进行孵化并饲养至成体，进行卤虫卵和成虫的形态学测量；同时采用特定位点扩增片段测序（SLAF-seq）技术进行群体遗传学分析。结果表明，YC-2023群体的体长、腹长、卵囊宽、复眼间距、复眼直径、第二触角长、抱握器外周长等形态学指标上均极显著大于YC-1993群体，而YC-2023群体卵径显著小于YC-1993群体。遗传分析显示，YC-2023群体的遗传多样性最低；3个群体的多态信息含量（PIC）介于0.252～0.305之间，属于中度多态（0.25 < PIC < 0.5）。YC-2019和YC-2023群体间的遗传分化系数Fst值为0.087，属于中度遗传分化（0.05 < Fst < 0.15）。而YC-1993与另外两个种群间的Fst值为0.151，属于高度遗传分化（0.15 < Fst < 0.25）。系统发育树、主成分分析、亲缘关系热图及Admixture分析进一步揭示，虽然3个群体间存在一定遗传分化，但均起源于单一共同祖先。运城卤虫的形态性状与遗传变异，可能源于运城盐湖近年来经历的环境变化以及独特养殖和管理模式所导致的遗传选择与遗传漂变。本研究为运城盐湖卤虫种质资源的保护与利用提供了理论支撑。Abstract: Artemia is important live bait in the cultivation of marine fish and crustacean seedlings, with more than 90% derived from wild Artemia resources. In order to study the effects of environmental changes and the unique aquaculture and harvest management on the morphometrical and genetic characteristics of Artemia in Yuncheng Salt Lake, Shanxi Province in the past 30 years, Artemia cysts collected in 1993 (YC-1993), 2019 (YC-2019) and 2023 (YC-2023) from Yuncheng Salt Lake were cultured and morphometrical measurements were conducted. Specific-locus amplified fragments sequencing (SLAF-seq) was used for population genetics analysis. The results showed that the YC-2023 group was extremely significantly larger than the YC-1993 group in terms of body length, abdominal length, ovary width, interocular distance, eye diameter, second antenna length, and peripheral claspers, while the cyst diameter of the YC-2023 group was significantly smaller than that of the YC-1993 group. The results of genetic analysis showed that the YC-2023 group had the lowest genetic diversity. The polymorphism information content (PIC) of three populations was between 0.252 and 0.305, showing moderate polymorphism (0.25 < PIC < 0.5). The Fst value of the genetic differentiation coefficient between the YC-2019 and YC-2023 populations is 0.087, indicating moderate genetic differentiation (0.05 < Fst < 0.15). However, the Fst value between the YC-1993 and the other two populations is 0.151, indicating a high degree of genetic differentiation (0.15 < Fst < 0.25). Phylogenetic tree, principal component analysis, the kinship heat map and Admixture analysis further revealed that although there was a certain degree of genetic differentiation among the three populations, their genetic information originated from the same original ancestor. The morphometrical traits and genetic variations of Yuncheng Artemia may result from genetic selection and genetic drift caused by the environmental changes that Yuncheng Salt Lake has undergone in recent years, and unique aquaculture and harvest management. This study will provide theoretical support for the conservation and utilization of Artemia germplasm resources in Yuncheng Salt Lake.
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Key words:
- Yuncheng Salt Lake /
- Artemia /
- genetic diversity /
- genetic structure /
- germplasm
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图 1 3个卤虫群体的形态学差异分析
F. 雌性; M. 雄性. 图中纵坐标为标准化值，标准化值=形态学指标/头宽。*、**、***分别表示两组间差异显著（p < 0.05）、非常显著（p < 0.01）、极显著（p < 0.001）
Fig. 1 Morphometrical variation analysis of three Artemia populations
F. Female, M. Male. The y-axis represents standardized values, calculated as each morphological trait divided by head width. *, ** and *** respectively indicates a significant (p < 0.05), a very significant (p < 0.01), an extremely significant (p < 0.001) difference between the two groups
图 2 3个卤虫群体形态学参数主成分分析（A. 雌性; B. 雄性）
a. 体长, b. 腹长, c. 体宽, d. 复眼间距, e. 复眼直径, f. 头宽, g. 生殖节长, h. 抱握器外周长, i. 额结节长, j. 卵囊宽, k. 第二触角长
Fig. 2 Principal component analysis of morphometrical data of three Artemia populations (A. Female; B. Male)
a. Body length, b. abdominal length, c. body width, d. distance between compound eyes, e. diameter of compound eyes, f. head width, g. genital segment length, h. outer circumference of the clasping organ, i. frontal tubercle length, j. ovary width, k. length of the second antenna
图 3 基于SNP的3个卤虫群体主成分分析（a）；3个卤虫群体的邻接系统发育树（b）
Fig. 3 Principal component analysis of three Artemia populations based on SNPs (a); Neighbor-Joining phylogenetic tree of three Artemia populations (b)
图 4 Admixture 分析的群体分组结果（K = 1 至 10）（a）；交叉验证错误率（b）
(a) 中不同颜色代表模型推断出的不同祖先遗传组分，每个个体的条形图中不同颜色的占比表示其对应祖先成分的比例
Fig. 4 Model-based population assignment by Admixture analysis for K = 1 to 10 (a); cross validation error rate (b)
Each color represents an inferred ancestral genetic component in (a); the proportion of each color in an individual bar indicates the individual’s estimated membership coefficient for that component
图 5 3个卤虫群体的亲缘关系热图
图中颜色梯度对应亲缘系数，颜色由蓝色向红色过渡表示亲缘关系系数逐渐升高，个体间遗传相似度逐渐增强
Fig. 5 Heat map of kinship of three Artemia populations
The color gradient in the figure corresponds to the coefficient of kinship. The transition from blue to red indicates a gradual increase in the coefficient of kinship, meaning the genetic similarity between individuals gradually strengthens
表 1 样品来源及相关信息
Tab. 1 Sample source and information
样品缩写 样品来源 采集年份 AR-ARC种质库编号 物种名称 YC-1993 中国运城盐湖 1993 CHN-SL-29 A. sinica YC-2019 中国运城盐湖 2019 CHN-SL-66 A. sinica YC-2023 中国运城盐湖 2023 CHN-SL-94 A. sinica 
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表 2 3个卤虫群体的遗传多样性指数
Tab. 2 Genetic diversity indexes of three Artemia populations
群体 期望等位
基因数（Ea）观测等位
基因（Oa）期望杂合
度（He）观测杂合
度（Ho）基因多样性
指数（Nei）多态性信息
含量（PIC）香农−威纳
指数（I）YC-1993 1.554 1.850 0.374 0.421 0.409 0.297 0.553 YC-2019 1.519 1.769 0.385 0.286 0.423 0.305 0.567 YC-2023 1.357 1.700 0.310 0.375 0.310 0.252 0.476
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表 A1 3个卤虫群体的水合卵径
Tab. A1 Hydrated cyst diameter of three Artemia populations
群体 YC-1993 YC-2019 YC-2023 平均卵径/μm 254.28±12.95a 252.51±12.18ab 250.35±12.73b 注：表中数据以平均值±标准差表示；数据右上角不同小写字母表示不同群体间差异显著（p < 0.05），含有相同字母表示差异不显著。
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表 A2 30个卤虫样本最终组装的SLAF数据汇总
Tab. A2 Summary of SLAF data collected in the final assembly of 30 samples of Artemia
群体 样品 ID 总Reads 数 GC 含量/% Q30 比例 (%) SLAF 数量 总测序深度 平均测序深度 YC-2019 YC19-1 7730082 36.96 91.89 128700 2693397 20.9277 YC-2019 YC19-2 9128422 36.50 91.87 134211 3195396 23.8087 YC-2019 YC19-3 8677512 37.23 92.31 134580 3039460 22.5850 YC-2019 YC19-4 7565912 36.68 92.06 129481 2651116 20.4749 YC-2019 YC19-5 9054058 36.63 91.90 132390 3145646 23.7605 YC-2019 YC19-6 10202738 36.61 92.07 138366 3542986 25.6060 YC-2019 YC19-7 10577008 37.14 91.72 140711 3726514 26.4835 YC-2019 YC19-8 7837192 36.89 91.56 133090 2739000 20.5801 YC-2019 YC19-9 10243238 37.20 91.56 149720 3553052 23.7313 YC-2019 YC19-10 8848634 37.20 91.55 141781 3115994 21.9775 YC-2023 YC23-1 3813192 38.35 95.51 158604 1004285 6.3320 YC-2023 YC23-2 4431566 36.13 95.43 178285 1509089 8.4645 YC-2023 YC23-3 4187818 36.72 95.45 177335 1367148 7.7094 YC-2023 YC23-4 4496128 36.37 95.33 181340 1494317 8.2404 YC-2023 YC23-5 3418262 36.23 95.53 163679 1133275 6.9238 YC-2023 YC23-6 3722144 37.55 95.70 163969 1082619 6.6026 YC-2023 YC23-7 3568966 37.69 95.67 160624 1035437 6.4463 YC-2023 YC23-8 4270412 37.38 95.38 170823 1257894 7.3637 YC-2023 YC23-9 3507526 37.48 95.49 163502 1008386 6.1674 YC-2023 YC23-10 4805234 38.10 95.15 160080 826324 5.1619 YC-1993 YC93-1 3045370 36.90 95.33 49050 373637 7.6175 YC-1993 YC93-2 4008736 36.52 95.46 53772 500266 9.3035 YC-1993 YC93-3 3343790 36.42 95.65 49779 425918 8.5562 YC-1993 YC93-4 3491636 36.74 95.51 168186 1137129 6.7611 YC-1993 YC93-5 3505134 36.83 95.71 165605 1139004 6.8778 YC-1993 YC93-6 2390254 36.81 95.45 140956 772447 5.4801 YC-1993 YC93-7 3771782 36.73 95.28 176151 1195748 6.7882 YC-1993 YC93-8 3827588 37.26 95.82 48863 428842 8.7764 YC-1993 YC93-9 2987962 36.83 95.70 155639 962015 6.1811 YC-1993 YC93-10 3110194 36.52 95.56 48361 384469 7.9500
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[1] Sorgeloos P, Dhert P, Candreva P. Use of the brine shrimp, Artemia spp. , in marine fish larviculture[J]. Aquaculture, 2001, 200(1/2): 147−159. [2] Van Stappen G, Sorgeloos P, Rombaut G. Manual on Artemia production and use[R]. Rome: Food and Agriculture Organization of the United Nations, 2024. [3] Wurtsbaugh W A, Maciej Gliwicz Z. Limnological control of brine shrimp population dynamics and cyst production in the Great Salt Lake, Utah[J]. Hydrobiologia, 2001, 466(1/3): 119−132. doi: 10.1007/978-94-017-2934-5_11 [4] Van Stappen G, Sui Liying, Hoa V N, et al. Review on integrated production of the brine shrimp Artemia in solar salt ponds[J]. Reviews in Aquaculture, 2020, 12(2): 1054−1071. doi: 10.1111/raq.12371 [5] Aladin N V, Gontar V I, Zhakova L V, et al. The zoocenosis of the Aral Sea: six decades of fast-paced change[J]. Environmental Science and Pollution Research, 2019, 26(3): 2228−2237. doi: 10.1007/s11356-018-3807-z [6] Asem A, Eimanifar A, van Stappen G, et al. The impact of one-decade ecological disturbance on genetic changes: a study on the brine shrimp Artemia urmiana from Urmia Lake, Iran[J]. PeerJ, 2019, 7: e7190. doi: 10.7717/peerj.7190 [7] Li Wenjie, Chen Panpan, Sui Liying, et al. Temporal genetic variation mediated by climate change-induced salinity decline, a study on Artemia (Crustacea: Anostraca) from Kyêbxang Co, a high altitude salt lake on the Qinghai-Tibet Plateau[J]. Gene, 2024, 902: 148160. doi: 10.1016/j.gene.2024.148160 [8] Wang Feipeng, Feng Jia, Wang Jie, et al. Phylogenetic and morphological investigation of a dunaliella strain isolated from Yuncheng Salt Lake, China[J]. Acta Geologica Sinica - English Edition, 2014, 88(S1): 106−107. doi: 10.1111/1755-6724.12266_26 [9] Zheng Mianping. Resources and eco-environmental protection of salt lakes in China[J]. Environmental Earth Sciences, 2011, 64(6): 1537−1546. doi: 10.1007/s12665-010-0601-8 [10] 王传旭, 杨静, 王卓, 等. 运城盐湖细菌群落结构及生态多样性分析[J]. 微生物学报, 2024, 64(6): 1906−1921. doi: 10.13343/j.cnki.wsxb.20230636Wang Chuanxu, Yang Jing, Wang Zhuo, et al. Community structure and ecological diversity of bacteria in Yuncheng Salt Lake[J]. Acta Microbiologica Sinica, 2024, 64(6): 1906−1921. doi: 10.13343/j.cnki.wsxb.20230636 [11] Li Xin, Yu Yinghui. Biodiversity and screening of halophilic bacteria with hydrolytic and antimicrobial activities from Yuncheng Salt Lake, China[J]. Biologia, 2015, 70(2): 151−156. doi: 10.1515/biolog-2015-0033 [12] Zhang Lei, King C E. Genetic variation in sympatric populations of diploid and polyploid brine shrimp (Artemia parthenogenetica)[J]. Genetica, 1992, 85(3): 211−221. doi: 10.1007/BF00132273 [13] Eimanifar A, Wink M. Fine-scale population genetic structure in Artemia urmiana (Günther, 1890) based on mtDNA sequences and ISSR genomic fingerprinting[J]. Organisms Diversity & Evolution, 2013, 13(4): 531−543. doi: 10.1007/s13127-013-0135-5 [14] Saad Y M, El-Sebaie H E A, Mahoud N H, et al. Reconstruction of phylogenetic relations among some Artemia species[J]. Life Science Journal, 2014, 11(8): 822−826. [15] Han Xuekai, Xu Ruyi, Zheng Yuyu, et al. Development of EST-SSR markers and genetic diversity analysis among three Artemia species from different geographic populations[J]. Crustaceana, 2019, 92(7): 841−851. doi: 10.1163/15685403-00003916 [16] Li Ke, Zhang Rui, Sui Liying, et al. Genetic structure of ten Artemia populations from China: cumulative effects of ancient geological events, climatic changes, and human activities[J]. Frontiers in Marine Science, 2024, 11: 1375641. doi: 10.3389/fmars.2024.1375641 [17] 李科. 世界主要产区卤虫种群的群体遗传学研究、品系鉴定及物种分布模型构建[D]. 天津: 天津科技大学, 2024.Li Ke. Artemia population genetics analysis, strains identification, and species distribution modeling of Artemia populations in world main production areas[D]. Tianjin: Tianjin University of Science and Technology, 2024. [18] 唐立群, 肖层林, 王伟平. SNP分子标记的研究及其应用进展[J]. 中国农学通报, 2012, 28(12): 154−158.Tang Liqun, Xiao Cenglin, Wang Weiping. Research and application progress of SNP markers[J]. Chinese Agricultural Science Bulletin, 2012, 28(12): 154−158. [19] 李科, 任翊卓, 韩学凯, 等. 无效基因fruitless参与卤虫Artemia franciscana的生殖调控研究[J]. 海洋学报, 2023, 45(10): 114−122.Li Ke, Ren Yizhuo, Han Xuekai, et al. Reproductive regulation of fruitless gene in brine shrimp Artemia franciscana[J]. Haiyang Xuebao, 2023, 45(10): 114−122. [20] Cohen R G, Rodríguez Gil S G, Vélez C G. The post-embryonic development of Artemia persimilis Piccinelli & Prosdocimi[J]. Hydrobiologia, 1998, 391(1/3): 63−80. [21] Sun Xiaowen, Liu Dongyuan, Zhang Xiaofeng, et al. SLAF-seq: an efficient method of large-scale de novo SNP discovery and genotyping using high-throughput sequencing[J]. PLoS One, 2013, 8(3): e58700. doi: 10.1371/journal.pone.0058700 [22] Li Heng, Durbin R. Fast and accurate short read alignment with Burrows–Wheeler transform[J]. Bioinformatics, 2009, 25(14): 1754−1760. doi: 10.1093/bioinformatics/btp324 [23] McKenna A, Hanna M, Banks E, et al. The Genome Analysis Toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data[J]. Genome Research, 2010, 20(9): 1297−1303. doi: 10.1101/gr.107524.110 [24] Li Heng, Handsaker B, Wysoker A, et al. The sequence alignment/map format and SAMtools[J]. Bioinformatics, 2009, 25(16): 2078−2079. doi: 10.1093/bioinformatics/btp352 [25] Catchen J, Hohenlohe P A, Bassham S, et al. Stacks: an analysis tool set for population genomics[J]. Molecular Ecology, 2013, 22(11): 3124−3140. doi: 10.1111/mec.12354 [26] Price A L, Patterson N J, Plenge R M, et al. Principal components analysis corrects for stratification in genome-wide association studies[J]. Nature Genetics, 2006, 38(8): 904−909. doi: 10.1038/ng1847 [27] Kumar S, Stecher G, Li M, et al. MEGA X: molecular evolutionary genetics analysis across computing platforms[J]. Molecular Biology and Evolution, 2018, 35(6): 1547−1549. doi: 10.1093/molbev/msy096 [28] Alexander D H, Novembre J, Lange K. Fast model-based estimation of ancestry in unrelated individuals[J]. Genome Research, 2009, 19(9): 1655−1664. doi: 10.1101/gr.094052.109 [29] Yang Jian, Lee S H, Goddard M E, et al. GCTA: a tool for genome-wide complex trait analysis[J]. The American Journal of Human Genetics, 2011, 88(1): 76−82. doi: 10.1016/j.ajhg.2010.11.011 [30] Botstein D, White R L, Skolnick M, et al. Construction of a genetic linkage map in man using restriction fragment length polymorphisms[J]. American Journal of Human Genetics, 1980, 32(3): 314−331. [31] Lavergne S, Mouquet N, Thuiller W, et al. Biodiversity and climate change: integrating evolutionary and ecological responses of species and communities[J]. Annual Review of Ecology, Evolution, and Systematics, 2010, 41: 321−350. doi: 10.1146/annurev-ecolsys-102209-144628 [32] Velasco J, Gutiérrez-Cánovas C, Botella-Cruz M, et al. Effects of salinity changes on aquatic organisms in a multiple stressor context[J]. Philosophical Transactions of the Royal Society B: Biological Sciences, 2019, 374(1764): 20180011. doi: 10.1098/rstb.2018.0011 [33] Ge Qianqian, Li Zhengdao, Li Jitao, et al. Effects of acute salinity stress on the survival and prophenoloxidase system of Exopalaemon carinicauda[J]. Acta Oceanologica Sinica, 2020, 39(4): 57−64. doi: 10.1007/s13131-020-1582-4 [34] Yao Xiaocui, Meng Lifang, Zhao Wangli, et al. Changes in the morphology traits, anatomical structure of the leaves and transcriptome in Lycium barbarum L. under salt stress[J]. Frontiers in Plant Science, 2023, 14: 1090366. doi: 10.3389/fpls.2023.1090366 [35] Manfra L, Savorelli F, Di Lorenzo B, et al. Intercalibration of ecotoxicity testing protocols with Artemia franciscana[J]. Ecological Indicators, 2015, 57: 41−47. doi: 10.1016/j.ecolind.2015.04.021 [36] Ravanbakhsh R, Agh N, Nouraein M, et al. Prolonged ecological changes can affect morphometrics and gene expression profile? Focusing on Hsp-70 and NLHS-induced Hsp-70 of Artemia urmiana[J]. Environmental Research, 2023, 238: 117254. doi: 10.1016/j.envres.2023.117254 [37] Litvinenko L I, Boyko E G. The morphological characteristics of Artemia shrimps from Siberian populations[J]. Inland Water Biology, 2008, 1(1): 37−45. doi: 10.1007/s12212-008-1007-0 [38] Naceur H, Jenhani A, Romdhane M. Influence of environmental factors on the life cycle and morphology of Artemia salina (Crustacea: Anostraca) in Sabkhet El Adhibet (SE Tunisia)[J]. Biological Letters, 2011, 48(1): 67−83. doi: 10.2478/v10120-011-0008-6 [39] Pais-Costa A J, Lievens E J P, Redón S, et al. Phenotypic but no genetic adaptation in zooplankton 24 years after an abrupt +10°C climate change[J]. Evolution Letters, 2022, 6(4): 284−294. doi: 10.1002/evl3.280 [40] Kappas I, Abatzopoulos T J, Van Hoa N, et al. Genetic and reproductive differentiation of Artemia franciscana in a new environment[J]. Marine Biology, 2004, 146(1): 103−117. doi: 10.1007/s00227-004-1420-9 [41] He Qicheng, Zhang Zhihao, Zhang Yuan, et al. Spatiotemporal evolution and driving mechanisms of ecological risk in the Yuncheng Salt Lake Wetland, China[J]. Water, 2025, 17(4): 524. doi: 10.3390/w17040524 [42] 刘畅, 马超. 运城市盐湖区31年植被与水体指标变化及驱动力分析[J]. 河南理工大学学报(自然科学版), 2021, 40(5): 80−89,180.Liu Chang, Ma Chao. On the change of vegetation and water indicators and driving forces in Yanhu district of Yuncheng city in the past 31 years[J]. Journal of Henan Polytechnic University (Natural Science), 2021, 40(5): 80−89,180. [43] 韩学凯, 张睿, 扎西拉姆, 等. 气候变暖诱发青藏高原盐湖变淡对拉果错卤虫形态变化和遗传变异的影响[J]. 中国水产科学, 2024, 31(8): 978−987. doi: 10.12264/JFSC2024-0210Han Xuekai, Zhang Rui, Lhamo T, et al. Effects of climate warming-induced desalination of salt lakes on morphological changes and genetic variation of Artemia in Lagkor Co, Qinghai-Tibet Plateau[J]. Journal of Fishery Sciences of China, 2024, 31(8): 978−987. doi: 10.12264/JFSC2024-0210 [44] 林峰, 冯民权, 李鸿彬. 运城盐湖浮游生物群落结构及多样性的季节差异[J]. 环境科学与技术, 2025, 48(11): 37−49. doi: 10.19672/j.cnki.1003-6504.0344.25.338Lin Feng, Feng Minquan, Li Hongbin. Seasonal differences in the plankton community structure and diversity in Yuncheng Salt Lake[J]. Environmental Science & Technology, 2025, 48(11): 37−49. doi: 10.19672/j.cnki.1003-6504.0344.25.338 [45] 景晓娜. 运城盐湖卤虫开发现状及建议[J]. 盐科学与化工, 2020, 49(3): 1−2.Jing Xiaona. Development status and suggestions of Artemia in Yuncheng Salt Lake[J]. Journal of Salt Science and Chemical Industry, 2020, 49(3): 1−2. [46] 张宇, 张婕, 郭东罡. 运城盐湖生物多样性研究: 过去、挑战与未来[J]. 新兴科学和技术趋势, 2024, 3(4): 333−344. doi: 10.12405/j.issn.2097-1486.2024.04.003Zhang Yu, Zhang Jie, Guo Donggang. Research on biodiversity in Yuncheng salt lake: the past, the challenges, and the future[J]. Emerging Science and Technology, 2024, 3(4): 333−344. doi: 10.12405/j.issn.2097-1486.2024.04.003 [47] Mathur S, DeWoody J A. Genetic load has potential in large populations but is realized in small inbred populations[J]. Evolutionary Applications, 2021, 14(6): 1540−1557. doi: 10.1111/eva.13216 [48] Wright S. Evolution and the Genetics of Populations. Volume 2: The Theory of Gene Frequencies[M]. Chicago: The University of Chicago Press, 1969. -
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