Original Papers: Animal Diversity

Response of fish diversity to hydrological connectivity of typical tidal creek system in the Yellow River Delta based on environmental DNA metabarcoding

  • Zhiyuan Dong ,
  • Linlin Chen ,
  • Naipeng Zhang ,
  • Li Chen ,
  • Debin Sun ,
  • Yanmei Ni ,
  • Baoquan Li
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  • 1. Key Laboratory of Coastal Biology and Bioresource Utilization, Yantai Institute of Coastal Zone Research, Chinese Academy of Sciences, Yantai, Shandong 264003
    2. University of Chinese Academy of Sciences, Beijing 100049
    3. School of Ocean, Yantai University, Yantai, Shandong 264003
    4. Dongying Municipal Hydrology Center, Dongying, Shandong 257000

Received date: 2023-03-09

  Accepted date: 2023-04-18

  Online published: 2023-04-26

Abstract

Aims: Hydrological connectivity is essential for maintaining biodiversity in coastal wetlands, and it is important to understand the response of fish diversity, as a major component of biodiversity, to different hydrological connectivity intensities. This study aimed to investigate the response of fish diversity to hydrological connectivity in the typical tidal creek system and verify the applicability of eDNA metabarcoding for monitoring and conserving fish diversity in the Yellow River Delta.

Methods: Water samples were collected from six sites in a typical tidal creek system in the Yellow River Delta in September 2022. Fish diversity was analyzed by using eDNA metabarcoding, in which, eDNA extracted from the water samples source were amplified by PCR using the 12S rRNA classical fish primers MiFish-E and high-throughput sequencing was performed by Illumina Miseq. The OTU representative sequences were aligned to the NCBI nucleotide sequence database to obtain species taxonomic annotation information. Thirteen environmental physicochemical indicators were measured in the water column. The relationship between fish communities and environmental factors was explored based on redundancy analysis.

Results: A total of 55 fish species were detected, including 27 native and 28 non-native fish species, and Perciformes dominated the fish composition. The fishes with high sequence abundance at each sample site included Acanthogobius hasta, Planiliza haematocheilu, Acanthogobius elongatus, etc. Fish diversity of the tidal creeks with different hydrological connectivity was different. Significantly higher community diversity and richness index, the highest number of species and a more even distribution of the number of individual species were found in the secondary tidal creek than in the other two tidal creeks. SiO32--Si, NO3--N, pH, salinity, NH4+-N, and dissolved oxygen were significantly correlated (P < 0.05) with fish community structure shown by RDA analysis. Acanthogobius hasta with higher sequence abundance was positively correlated with silicate, and the sequence abundance of Planiliza haematocheilus was negatively correlated with salinity.

Conclusion: This study confirmed the feasibility of using environmental DNA metabarcoding to monitor fish diversity of typical tidal water bodies in the Yellow River estuary by comparing it with previous traditional sampling data and indicated that hydrological connectivity of tidal creek systems has a significant impact on fish community structure and diversity. The results of this study are helpful to further understand the influence mechanism of coastal wetland hydrological connectivity on biological communities.

Cite this article

Zhiyuan Dong , Linlin Chen , Naipeng Zhang , Li Chen , Debin Sun , Yanmei Ni , Baoquan Li . Response of fish diversity to hydrological connectivity of typical tidal creek system in the Yellow River Delta based on environmental DNA metabarcoding[J]. Biodiversity Science, 2023 , 31(7) : 23073 . DOI: 10.17520/biods.2023073

References

[1] Balasingham KD, Walter RP, Mandrak NE, Heath DD (2018) Environmental DNA detection of rare and invasive fish species in two Great Lakes tributaries. Molecular Ecology, 27, 112-127.
[2] Chen WF, Zhou WZ, Shi YX (2003) Crisis of wetlands in the Yellow River Delta and its protection. Journal of Agro-Environmental Science, 22, 499-502. (in Chinese with English abstract)
[2] [陈为峰, 周维芝, 史衍玺 (2003) 黄河三角洲湿地面临的问题及其保护. 农业环境科学学报, 22, 499-502.]
[3] Connell JH (1978) High diversity of trees and corals is maintained only in a nonequilibrium state. Science, 199, 1302-1310.
[4] Creer S, Deiner K, Frey S, Porazinska D, Taberlet P, Thomas WK, Potter C, Bik HM (2016) The ecologist's field guide to sequence-based identification of biodiversity. Methods in Ecology and Evolution, 7, 1008-1018.
[5] Cui BS, Cai YZ, Xie T, Ning ZH, Hua YY (2016) Ecological effects of wetland hydrological connectivity: Problems and prospects. Journal of Beijing Normal University (Natural Science), 52, 738-746. (in Chinese with English abstract)
[5] [崔保山, 蔡燕子, 谢湉, 宁中华, 华妍妍 (2016) 湿地水文连通的生态效应研究进展及发展趋势. 北京师范大学学报(自然科学版), 52, 738-746.]
[6] Deiner K, Bik HM, M?chler E, Seymour M, Lacoursière- Roussel A, Altermatt F, Creer S, Bista I, Lodge DM, de Vere N, Pfrender ME, Bernatchez L (2017) Environmental DNA metabarcoding: Transforming how we survey animal and plant communities. Molecular Ecology, 26, 5872-5895.
[7] Dong R, Wang YY, Lü C, Lei GC, Xue BL, Chen QK (2020) Effects of hydrological connectivity on the community structure of macrobenthos in West Dongting Lake. Acta Ecologica Sinica, 40, 8336-8346. (in Chinese with English abstract)
[7] [董芮, 王玉玉, 吕偲, 雷光春, 薛彬林, 陈乾阔 (2020) 水文连通性对西洞庭湖大型底栖动物群落结构的影响. 生态学报, 40, 8336-8346.]
[8] Evangelisti M, D'Amelia D, Di Lallo GD, Thaller MC, Migliore L (2013) The relationship between salinity and bacterioplankton in three relic coastal ponds (Macchiatonda Wetland, Italy). Journal of Water Resource and Protection, 5, 859-866.
[9] Evans NT, Olds BP, Renshaw MA, Turner CR, Li YY, Jerde CL, Mahon AR, Pfrender ME, Lamberti GA, Lodge DM (2016) Quantification of mesocosm fish and amphibian species diversity via environmental DNA metabarcoding. Molecular Ecology Resources, 16, 29-41.
[10] Fan HY, Ji YP, Zhang SH, Yuan CT, Gao TX (2005) Research of fishery biology of the neritic fish Synechogobius ommaturus in the area of the Huanghe Delta. Periodical of Ocean University of China (Natural Science), 35, 733-736. (in Chinese with English abstract)
[10] [范海洋, 纪毓鹏, 张士华, 苑春亭, 高天翔 (2005) 黄河三角洲斑尾复虾虎鱼渔业生物学的研究. 中国海洋大学学报(自然科学版), 35, 733-736.]
[11] Freeman MC, Pringle CM, Jackson CR (2007) Hydrologic connectivity and the contribution of stream headwaters to ecological integrity at regional scales. Journal of the American Water Resources Association, 43, 5-14.
[12] Gao XC, Jiang W (2021) The construction and application of BLAST database of DNA barcode for common fish in the Three Gorges Reservoir. Genomics and Applied Biology, 40, 1952-1960. (in Chinese with English abstract)
[12] [郜星辰, 姜伟 (2021) 三峡库区常见鱼类DNA条形码本地BLAST数据库的构建和应用. 基因组学与应用生物学, 40, 1952-1960.]
[13] Garwood JA, Allen DM, Kimball ME, Boswell KM (2019) Site fidelity and habitat use by young-of-the-year transient fishes in salt marsh intertidal creeks. Estuaries and Coasts, 42, 1387-1396.
[14] Jardine TD, Pettit NE, Warfe DM, Pusey BJ, Ward DP, Douglas MM, Davies PM, Bunn SE (2012) Consumer-resource coupling in wet-dry tropical rivers. Journal of Animal Ecology, 81, 310-322.
[15] Ji FF, Han DY, Yan L, Yan SH, Zha JM, Shen JZ (2022) Assessment of benthic invertebrate diversity and river ecological status along an urbanized gradient using environmental DNA metabarcoding and a traditional survey method. Science of the Total Environment, 806, 150587.
[16] Jiang PW, Li M, Zhang S, Chen ZZ, Xu SN (2022) Investigating the fish diversity in Pearl River Estuary based on environmental DNA metabarcoding and bottom trawling. Acta Hydrobiologica Sinica, 46, 1701-1711. (in Chinese with English abstract)
[16] [蒋佩文, 李敏, 张帅, 陈作志, 徐姗楠 (2022) 基于环境DNA宏条码和底拖网的珠江河口鱼类多样性. 水生生物学报, 46, 1701-1711.]
[17] Jiang WZ, Sui KG (2015) Study on ecological pond aquaculture technology of Tachysurus fulvidraco in saline-alkali land. Hebei Fisheries, (11), 32-33. (in Chinese)
[17] [蒋万钊, 隋凯港 (2015) 盐碱地黄颡鱼池塘生态养殖技术研究. 河北渔业, (11), 32-33.]
[18] Jo TS (2023) Correlation between the number of eDNA particles and species abundance is strengthened by warm temperature: Simulation and meta-analysis. Hydrobiologia, 850, 39-50.
[19] Knight R, Vrbanac A, Taylor BC, Aksenov A, Callewaert C, Debelius J, Gonzalez A, Kosciolek T, McCall LI, McDonald D, Melnik AV, Morton JT, Navas J, Quinn RA, Sanders JG, Swafford AD, Thompson LR, Tripathi A, Xu ZZJ, Zaneveld JR, Zhu QY, Caporaso JG, Dorrestein PC (2018) Best practices for analysing microbiomes. Nature Reviews Microbiology, 16, 410-422.
[20] Kume M, Lavergne E, Ahn H, Terashima Y, Kadowaki K, Ye F, Kameyama S, Kai Y, Henmi YM, Yamashita Y, Kasai A (2021) Factors structuring estuarine and coastal fish communities across Japan using environmental DNA metabarcoding. Ecological Indicators, 121, 107216.
[21] Lamb PD, Fonseca VG, Maxwell DL, Nnanatu CC (2022) Systematic review and meta-analysis: Water type and temperature affect environmental DNA decay. Molecular Ecology Resources, 22, 2494-2505.
[22] Li DX, Li YQ, Zhang KH, Ma X, Zhang SY, Liu WH, Che CG, Cui BS (2020) Characteristics of carbon and nitrogen distribution in typical tidal creeks of the Yellow River Delta. Journal of Natural Resources, 35, 460-471. (in Chinese with English abstract)
[22] [李冬雪, 李雨芩, 张珂豪, 马旭, 张树岩, 刘伟华, 车纯广, 崔保山 (2020) 黄河口典型潮沟土壤碳氮分布特征规律. 自然资源学报, 35, 460-471.]
[23] Li F, Lü ZB, Wei ZH, Wang TT, Xu BQ, Wang ZQ (2013) Seasonal changes in the community structure of the demersal fishery in Laizhou Bay. Journal of Fishery Sciences of China, 20, 137-147. (in Chinese with English abstract)
[23] [李凡, 吕振波, 魏振华, 王田田, 徐炳庆, 王忠全 (2013) 2010年莱州湾底层渔业生物群落结构及季节变化. 中国水产科学, 20, 137-147.]
[24] Li F, Xu BQ, Lü ZB, Wang TT (2018) Ecological niche of dominant species of fish assemblages in Laizhou Bay, China. Acta Ecologica Sinica, 38, 5195-5205. (in Chinese with English abstract)
[24] [李凡, 徐炳庆, 吕振波, 王田田 (2018) 莱州湾鱼类群落优势种生态位. 生态学报, 38, 5195-5205.]
[25] Li HT, Zou KS, Zhang S, Cao YT, Lu ZC, Chen ZZ, Li M (2022) Species composition of fishes in the Pearl River Estuary based on environmental DNA metabarcoding. Journal of Shanghai Ocean University, 31, 1423-1433. (in Chinese with English abstract)
[25] [李红婷, 邹柯姝, 张帅, 曹漪婷, 卢芷程, 陈作志, 李敏 (2022) 基于环境DNA宏条形码的珠江河口鱼类种类组成. 上海海洋大学学报, 31, 1423-1433.]
[26] Li MD, Wang XL, Lü X (1997) Mullet. China Ocean Press, Beijing. (in Chinese)
[26] [李明德, 王秀玲, 吕宪 (1997) 梭鱼. 海洋出版社, 北京.]
[27] Li W, Cui LJ, Zhao XS, Zhang MY, Ma MY, Kang XM, Wang YF (2014) An overview of Chinese coastal wetland and their ecosystem services. Forest Inventory and Planning, 39(4), 24-30. (in Chinese with English abstract)
[27] [李伟, 崔丽娟, 赵欣胜, 张曼胤, 马牧源, 康晓明, 王义飞 (2014) 中国滨海湿地及其生态系统服务功能研究概述. 林业调查规划, 39(4), 24-30.]
[28] Liu J, Chen YX, Ma L (2015) Fishes of the Bohai Sea and Yellow Sea. Science Press, Beijing. (in Chinese)
[28] [刘静, 陈咏霞, 马琳 (2015) 黄渤海鱼类图志. 科学出版社, 北京.]
[29] Luo M, Wang Q, Qiu DD, Shi W, Ning ZH, Cai YZ, Song ZF, Cui BS (2018) Hydrological connectivity characteristics and ecological effects of a typical tidal channel system in the Yellow River Delta. Journal of Beijing Normal University (Natural Science), 54, 17-24. (in Chinese with English abstract)
[29] [骆梦, 王青, 邱冬冬, 施伟, 宁中华, 蔡燕子, 宋振峰, 崔保山 (2018) 黄河三角洲典型潮沟系统水文连通特征及其生态效应. 北京师范大学学报(自然科学版), 54, 17-24.]
[30] Ma QZ, Zhang TT, Zhao F, Zhang T, Yang G, Wang SK (2023) Effects of tidal creek connectivity on fish communities in the Yangtze estuary wetlands. Chinese Journal of Ecology, http://kns.cnki.net/kcms/detail/21.1148.Q.20230311.1446.006.html. (in Chinese with English abstract)
[30] [马巧珍, 张婷婷, 赵峰, 张涛, 杨刚, 王思凯 (2023) 长江口湿地潮沟连通程度对鱼类群落的影响. 生态学杂志, http://kns.cnki.net/kcms/detail/21.1148.Q.20230311.1446.006.html.]
[31] Miya M, Gotoh RO, Sado T (2020) MiFish metabarcoding: A high-throughput approach for simultaneous detection of multiple fish species from environmental DNA and other samples. Fisheries Science, 86, 939-970.
[32] Miya M, Nishida M (2000) Use of mitogenomic information in teleostean molecular phylogenetics: A tree-based exploration under the maximum-parsimony optimality criterion. Molecular Phylogenetics and Evolution, 17, 437-455.
[33] Miya M, Sato Y, Fukunaga T, Sado T, Poulsen JY, Sato K, Minamoto T, Yamamoto S, Yamanaka H, Araki H, Kondoh M, Iwasaki W (2015) MiFish, a set of universal PCR primers for metabarcoding environmental DNA from fishes: Detection of more than 230 subtropical marine species. Royal Society Open Science, 2, 150088.
[34] Murakami H, Yoon S, Kasai A, Minamoto T, Yamamoto S, Sakata MK, Horiuchi T, Sawada H, Kondoh M, Yamashita Y, Masuda R (2019) Dispersion and degradation of environmental DNA from caged fish in a marine environment. Fisheries Science, 85, 327-337.
[35] Nakagawa H, Yamamoto S, Sato Y, Sado T, Minamoto T, Miya M (2018) Comparing local- and regional-scale estimations of the diversity of stream fish using eDNA metabarcoding and conventional observation methods. Freshwater Biology, 63, 569-580.
[36] O'Donnell JL, Kelly RP, Shelton AO, Samhouri JF, Lowell NC, Williams GD (2017) Spatial distribution of environmental DNA in a nearshore marine habitat. PeerJ, 5, e3044.
[37] Qu JY, Yang GMM, Fang Z, Chen XJ (2021) A review of research advancement on fisheries biology of Japanese Spanish Mackerel Scomberomorus niphonius. Fisheries Science, 40, 643-650. (in Chinese with English abstract)
[37] [瞿俊跃, 杨光明媚, 方舟, 陈新军 (2021) 蓝点马鲛渔业生物学研究进展. 水产科学, 40, 643-650.]
[38] Sales NG, Wangensteen OS, Carvalho DC, Deiner K, Pr?bel K, Coscia I, McDevitt AD, Mariani S (2021) Space-time dynamics in monitoring neotropical fish communities using eDNA metabarcoding. Science of the Total Environment, 754, 142096.
[39] Sard NM, Herbst SJ, Nathan L, Uhrig G, Kanefsky J, Robinson JD, Scribner KT (2019) Comparison of fish detections, community diversity, and relative abundance using environmental DNA metabarcoding and traditional gears. Environmental DNA, 1, 368-384.
[40] Schofield KA, Alexander LC, Ridley CE, Vanderhoof MK, Fritz KM, Autrey BC, DeMeester JE, Kepner WG, Lane CR, Leibowitz SG, Pollard AI (2018) Biota connect aquatic habitats throughout freshwater ecosystem mosaics. Journal of the American Water Resources Association, 54, 372-399.
[41] Shaw JLA, Clarke LJ, Wedderburn SD, Barnes TC, Weyrich LS, Cooper A (2016) Comparison of environmental DNA metabarcoding and conventional fish survey methods in a river system. Biological Conservation, 197, 131-138.
[42] Shen M, Guo NN, Luo ZL, Guo XC, Sun G, Xiao NW (2022) Explore the distribution and influencing factors of fish in major rivers in Beijing with eDNA metabarcoding technology. Biodiversity Science, 30, 22240. (in Chinese with English abstract)
[42] [沈梅, 郭宁宁, 罗遵兰, 郭晓晨, 孙光, 肖能文 (2022) 基于eDNA metabarcoding探究北京市主要河流鱼类分布及影响因素. 生物多样性, 30, 22240.]
[43] Sousa WP (1979) Disturbance in marine intertidal boulder fields: The nonequilibrium maintenance of species diversity. Ecology, 60, 1225-1239.
[44] Strickler KM, Fremier AK, Goldberg CS (2015) Quantifying effects of UV-B, temperature, and pH on eDNA degradation in aquatic microcosms. Biological Conservation, 183, 85-92.
[45] Sun JF, Liu QZ (2010) Research on comprehensive development and utilization of geothermal resources in Dongying. Journal of Hebei Agricultural Sciences, 14(2), 91-93, 96. (in Chinese with English abstract)
[45] [孙金凤, 刘清志 (2010) 东营市地热资源综合开发与利用研究. 河北农业科学, 14(2), 91-93, 96.]
[46] Sun PF, Shan XJ, Wu Q, Chen YL, Jin XS (2014) Seasonal variations in fish community structure in the Laizhou Bay and the Yellow River Estuary. Acta Ecologica Sinica, 34, 367-376. (in Chinese with English abstract)
[46] [孙鹏飞, 单秀娟, 吴强, 陈云龙, 金显仕 (2014) 莱州湾及黄河口水域鱼类群落结构的季节变化. 生态学报, 34, 367-376.]
[47] Sun ZG, Mou XJ, Chen XB, Wang LL, Song HL, Jiang HH (2011) Actualities, problems and suggestions of wetland protection and restoration in the Yellow River Delta. Wetland Science, 9, 107-115. (in Chinese with English abstract)
[47] [孙志高, 牟晓杰, 陈小兵, 王玲玲, 宋红丽, 姜欢欢 (2011) 黄河三角洲湿地保护与恢复的现状、问题与建议. 湿地科学, 9, 107-115.]
[48] Thomsen PF, Kielgast J, Iversen LL, M?ller PR, Rasmussen M, Willerslev E (2012a) Detection of a diverse marine fish fauna using environmental DNA from seawater samples. PLoS ONE, 7, e41732.
[49] Thomsen PF, Kielgast J, Iversen LL, Wiuf C, Rasmussen M, Gilbert MTP, Orlando L, Willerslev E (2012b) Monitoring endangered freshwater biodiversity using environmental DNA. Molecular Ecology, 21, 2565-2573.
[50] Tsuji S, Takahara T, Doi H, Shibata N, Yamanaka H,(2019) The detection of aquatic macroorganisms using environmental DNA analysis—A review of methods for collection, extraction, and detection. Environmental DNA, 1, 99-108.
[51] Valentini A, Taberlet P, Miaud C, Civade R, Herder J, Thomsen PF, Bellemain E, Besnard A, Coissac E, Boyer F, Gaboriaud C, Jean P, Poulet N, Roset N, Copp GH, Geniez P, Pont D, Argillier C, Baudoin JM, Peroux T, Crivelli AJ, Olivier A, Acqueberge M, Le Brun M, M?ller PR, Willerslev E, Dejean T (2016) Next-generation monitoring of aquatic biodiversity using environmental DNA metabarcoding. Molecular Ecology, 25, 929-942.
[52] Wang P, Jiao Y, Ren YP, Zhong CJ, Yu H (1999) Investigation of biodiversity from spring catch in coastal waters of Laizhou Bay and Huanghe Estuary. Transaction of Oceanology and Limnology, (1), 40-44. (in Chinese with English abstract)
[52] [王平, 焦燕, 任一平, 仲崇俊, 于浩 (1999) 莱州湾、黄河口水域春季近岸渔获生物多样性特征的调查研究. 海洋湖沼通报, (1), 40-44.]
[53] Wang RX, Yang G, Geng Z, Zhao F, Feng XS, Zhang T (2023) Application of environmental DNA technology in fish diversity analysis in the Yangtze River estuary. Acta Hydrobiologica Sinica, 47, 365-375. (in Chinese with English abstract)
[53] [王汝贤, 杨刚, 耿智, 赵峰, 冯雪松张涛 (2023) 环境DNA技术在长江口鱼类多样性分析中的应用. 水生生物学报, 47, 365-375.]
[54] Wang XY, Yan JG, Bai JH, Cui BS (2019) Influence of hydrological connectivity of coastal wetland on the biological connectivity of macrobenthos in the Yellow River Estuary. Journal of Natural Resources, 34, 2544-2553. (in Chinese with English abstract)
[54] [王新艳, 闫家国, 白军红, 崔保山 (2019) 黄河口滨海湿地水文连通对大型底栖动物生物连通的影响. 自然资源学报, 34, 2544-2553.]
[55] Yamamoto S, Masuda R, Sato Y, Sado T, Araki H, Kondoh M, Minamoto T, Miya M (2017) Environmental DNA metabarcoding reveals local fish communities in a species-rich coastal sea. Scientific Reports, 7, 40368.
[56] Yamamoto S, Minami K, Fukaya K, Takahashi K, Sawada H, Murakami H, Tsuji S, Hashizume H, Kubonaga S, Horiuchi T, Hongo M, Nishida J, Okugawa Y, Fujiwara A, Fukuda M, Hidaka S, Suzuki KW, Miya M, Araki H, Yamanaka H, Maruyama A, Miyashita K, Masuda R, Minamoto T, Kondoh M (2016) Environmental DNA as a ‘snapshot' of fish distribution: A case study of Japanese Jack Mackerel in Maizuru Bay, Sea of Japan. PLoS ONE, 11, e0149786.
[57] Yin S, Bai JH, Wang X, Wang XY, Zhang GL, Jia J, Li XW, Liu XH (2020) Hydrological connectivity and herbivores control the autochthonous producers of coastal salt marshes. Marine Pollution Bulletin, 160, 111638.
[58] Yuan J, Cohen MJ, Kaplan DA, Acharya S, Larsen LG, Nungesser MK (2015) Linking metrics of landscape pattern to hydrological process in a lotic wetland. Landscape Ecology, 30, 1893-1912.
[59] Zhan AB, Hulák M, Sylvester F, Huang XT, Adebayo AA, Abbott CL, Adamowicz SJ, Heath DD, Cristescu ME, MacIsaac HJ (2013) High sensitivity of 454 pyrosequencing for detection of rare species in aquatic communities. Methods in Ecology and Evolution, 4, 558-565.
[60] Zhang DY, Chai XJ, Ruan ZC, Zhang Y, Wang YB (2020) Effects of long time low salinity on the growth and physiology in the juvenile of Liza haematocheila. Journal of Zhejiang Ocean University (Natural Science), 39, 296-302. (in Chinese with English abstract)
[60] [张鼎元, 柴学军, 阮泽超, 张燕, 王跃斌 (2020) 长期低盐胁迫对梭鱼生长及生理的影响. 浙江海洋大学学报(自然科学版), 39, 296-302.]
[61] Zhang XX, Yao QZ, Chen HT, Mi TZ, Tan JQ, Yu ZG (2010) Seasonal variation and fluxes of nutrients in the lower reaches of the Yellow River. Periodical of Ocean University of China, 40(7), 82-88. (in Chinese with English abstract)
[61] [张晓晓, 姚庆祯, 陈洪涛, 米铁柱, 谭加强, 于志刚 (2010) 黄河下游营养盐浓度季节变化及其入海通量研究. 中国海洋大学学报(自然科学版), 40(7), 82-88.]
[62] Zhao XY, Li X, Yu M, Yu JB, Wang XH (2019) Actualities of wetland hydrological connectivity blocked in the Yellow River Delta. Regional Governance, (49), 78-81. (in Chinese)
[62] [赵心怡, 李晓, 于淼, 于君宝, 王雪宏 (2019) 黄河三角洲湿地水文连通受阻现状. 区域治理, (49), 78-81.]
[63] Zou KS, Chen JW, Ruan HT, Li ZH, Guo WJ, Li M, Liu L (2020) eDNA metabarcoding as a promising conservation tool for monitoring fish diversity in a coastal wetland of the Pearl River Estuary compared to bottom trawling. Science of the Total Environment, 702, 134704.
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