Otolith microchemical evidence revealing multiple spawning site origination of the anadromous tapertail anchovy (<i>Coilia nasus</i>) in the Changjiang (Yangtze) River Estuary

Zhongya Xuan; Tao Jiang; Hongbo Liu; Xiubao Chen; Jian Yang

doi:10.1007/s13131-022-2135-9

doi: 10.1007/s13131-022-2135-9

^{1, 2},
²,
²,
²,
^{1, 2, ,}

计量
- 文章访问数: 292
- HTML全文浏览量: 111
- PDF下载量: 13
- 被引次数: 0
出版历程
- 收稿日期: 2021-09-16
- 录用日期: 2022-04-23
- 网络出版日期: 2022-12-29
- 刊出日期: 2023-01-25

Otolith microchemical evidence revealing multiple spawning site origination of the anadromous tapertail anchovy (Coilia nasus) in the Changjiang (Yangtze) River Estuary

Zhongya Xuan^{1, 2},
Tao Jiang²,
Hongbo Liu²,
Xiubao Chen²,
Jian Yang^{1, 2
, ,}

1.
Wuxi Fisheries College, Nanjing Agricultural University, Wuxi 214081, China
2.
Key Laboratory of Fishery Ecological Environment Assessment and Resource Conservation in Middle and Lower Reaches of the Yangtze River, Freshwater Fisheries Research Center, Chinese Academy of Fishery Sciences, Wuxi 214081, China

Funds: The National Natural Science Foundation of China under contract No. 31602159; the Agricultural Finance Special Project under contract No. CJDC-2017-22; the Scientific Research Foundation of Wuxi City for Returned Oversea Chinese Scholars under contract No. CZ2019231400.

More Information

Corresponding author: jiany@ffrc.cn

摘要

- /
- /
- /
- /
Abstract: The estuarine tapertail anchovy (Coilia nasus) is a high-value commercial fish. Estimating the spawning site or hatchery origin and habitat is essential for its conservation. This study aimed to determine the habitat use and life history characteristics of C. nasus from the Changjiang River Estuary. We investigated the environmental signatures of strontium (Sr) and calcium (Ca) in the otoliths of the collected specimens using electron probe microanalysis; additionally, we examined their gonadal maturity stage. Our results indicate that the 31 adult C. nasus specimens used in this study could be classified into two types based on their otolith Sr:Ca concentration ratios and their gonadal maturity stage. The long freshwater early life history type (Type LF) had wider central region in the otolith with low Sr:Ca concentration ratios ranging from 1.24±0.62 to 1.92±0.78 and a bluish pattern of low Sr content level. These fish are of riverine origin and had a relatively long early life history in freshwater and low gonadal maturation when captured. The short freshwater early life history type (Type SF) had a shorter central region in the otolith with low Sr:Ca concentration ratios ranging from 1.35±0.5 to 2.82±0.97 and a correspondingly bluish pattern. These fish also had a relatively short-term early life history in freshwater and high gonadal maturation when captured. The results of the otolith microchemical analysis indicated that Type LF and Type SF originated in spawning/hatching sites far from and close to the estuary, respectively. The mature gonads of Type SF fish indicated that they may breed in areas close to the estuary, whereas the immature gonads of Type LF fish indicated that they may breed in areas far from the estuary. This study is the first to reveal that the Changjiang River Estuary contains stocks of anadromous C. nasus originating in different spawning sites during the same season. The estuarine habitat plays a critical role in the connectivity between freshwater recruitment and the marine resources available to adult spawners of this commercially valued species. From a conservation perspective, this study provides important information for identifying anadromous C. nasus stocks originating in different spawning sites in the Changjiang River Basin.
- Coilia nasus /
- otolith /
- migration /
- connectivity /
- spawning site

HTML全文

Figure 1. Map of the sampling site of Coilia nasus in the Changjiang River Estuary. The red box in the right figure indicates the sampling range.

下载: 全尺寸图片幻灯片

Figure 2. Fluctuation (grey line) and shift (black line) of the otolith Sr:Ca concentration ratios along line transects from the core (0 μm) to the edge of the sagittal plane of Type LF Coilia nasus, which bred far from the Changjiang River Estuary. The position of the vertical dashed lines represents the annulus.

下载: 全尺寸图片幻灯片

Figure 3. Fluctuation (grey line) and shift (black line) of the otolith Sr:Ca concentration ratios along the line transects from the core (0 μm) to the edge of the sagittal plane of Type SF Coilia nasus, which bred close to the Changjiang River Estuary. The position of the vertical dashed lines represents the annulus.

下载: 全尺寸图片幻灯片

Figure 4. Two-dimensional strontium (Sr) concentration imaging of the sagittal otoliths of two Coilia nasus types using X-ray electron microprobe analyses.

下载: 全尺寸图片幻灯片

Figure 5. The freshwater coefficient (F_C) of two Coilia nasus types from the Changjiang River Estuary. The different letters indicate significant differences at P<0.01 (one-way ANOVA). Type LF: the long freshwater early life history type; Type SF: the short freshwater early life history type.

下载: 全尺寸图片幻灯片

Figure 6. Diagrammatic model of Coilia nasus migration from the Changjiang River Estuary based on Sr:Ca concentration ratio analyses. The lines with the arrows represent possible dispersion patterns. Type LF: the long freshwater early life history type; Type SF: the short freshwater early life history type.

下载: 全尺寸图片幻灯片

Table 1. The proportions of Coilia nasus specimens collected from the waters of the Changjiang River Estuary, throughout their freshwater life history

Type	Individual code	Total length/ mm	Body weight/g	Supermaxilla:Head length ratio	Sex	Age^a	Gonadal maturity stage	L_f^b/μm	L_T^c/μm	F_C^d
Type LF	17CMCN08	387	140.00	1.09	♂	2+	II	910	2 290	0.40
	17CMCN12	314	98.11	1.12	♀	2+	II	550	1 770	0.31
	17CMCN13	309	104.01	1.24	♀	2+	II	1 100	2 310	0.48
	17CMCN14	310	94.61	1.30	♂	2+	II	980	2 020	0.49
	17CMCN15	317	103.62	1.26	♂	2+	II	980	2 100	0.47
	17CMCN16	300	97.79	1.20	♀	2+	II	910	2 100	0.43
	17CMCN17	322	115.69	1.18	♂	2+	II	660	2 160	0.31
	17CMCN18	320	116.83	1.13	♀	2+	II	970	2 100	0.46
	17CMCN19	294	94.36	1.21	♂	2+	II	690	1 960	0.35
	17CMCN20	315	107.69	1.16	♀	3	II	510	1 830	0.28
	17CMCN21	310	99.81	1.16	♀	2+	II	1 130	2 190	0.52
	17TJSCN03	323	111.89	1.15	♀	2+	III	920	2 390	0.38
	17TJSCN06	275	67.44	1.13	♂	2	III	890	1 920	0.46
	17TJSCN08	333	155.13	1.22	♂	2+	II	1 690	2 270	0.74
Type SF	17CMCN01	325	115.81	1.24	♀	2+	IV	220	2 320	0.09
	17CMCN02	230	31.48	1.29	♂	2+	V	290	1 860	0.16
	17CMCN03	306	100.01	1.27	♀	2+	IV	480	2 250	0.21
	17CMCN04	281	71.55	1.12	♀	2+	IV	650	1 950	0.33
	17CMCN05	302	70.71	1.31	♂	2+	IV	660	2 270	0.29
	17CMCN06	305	93.59	1.16	♂	2+	IV	440	2 080	0.21
	17CMCN10	333	126.22	1.17	♀	2+	IV	270	1 930	0.14
	17CMCN11	312	123.67	1.20	♂	2+	IV	670	1 990	0.37
	17TJSCN01	322	148.16	1.14	♀	3+	IV	200	2 200	0.09
	17TJSCN02	305	98.13	1.23	♀	2+	IV	200	2 370	0.08
	17TJSCN04	278	72.32	1.22	♂	2	IV	270	2 120	0.13
	17TJSCN05	295	89.19	1.35	♀	2+	IV	200	2 060	0.10
	17TJSCN09	305	98.28	1.21	♂	2	IV	370	1 940	0.19
	17TJSCN10	331	124.57	1.22	♂	3+	IV	150	2 350	0.06
	17CMCN07	293	74.21	1.17	♀	2+	IV	0	2 160	0
	17CMCN09	331	109.87	1.19	♀	3+	V	0	2 120	0
	17TJSCN07	276	50.18	1.24	♀	2+	IV	0	1 970	0
Note: Type LF: the long freshwater early life history type; Type SF: the short freshwater early life history type. Age^a is estimated using the otolith rings; L_f^b: the length of the first freshwater stage of the low Sr:Ca concentration ratio line of the otolith microchemical line analysis or the length of the low Sr bluish central regions of the Sr mapping analysis; L_T^c: the radius of the entire otolith microchemical line analysis measurement line along the line down the longest axis of each otolith from the core; F_C^d: freshwater coefficient.

下载: 导出CSV

参考文献(51)

Asaduzzaman M, Igarashi Y, Wahab M A, et al. 2020. Population genomics of an anadromous hilsa shad Tenualosa ilisha species across its diverse migratory habitats: discrimination by fine-scale local adaptation. Genes, 11(1): 46. doi: 10.3390/genes11010046

Aykanat T, Johnston S E, Orell P, et al. 2015. Low but significant genetic differentiation underlies biologically meaningful phenotypic divergence in a large Atlantic salmon population. Molecular Ecology, 24(20): 5158–5174. doi: 10.1111/mec.13383

Brown R J, Severin K P. 2009. Otolith chemistry analyses indicate that water Sr:Ca is the primary factor influencing otolith Sr:Ca for freshwater and diadromous fish but not for marine fish. Canadian Journal of Fisheries and Aquatic Sciences, 66(10): 1790–1808. doi: 10.1139/F09-112

Chen Tingting, Jiang Tao, Liu Hongbo, et al. 2017. Do all long supermaxilla-type estuarine tapertail anchovies (Coilia nasus Temminck et Schlegel, 1846) migrate anadromously?. Journal of Applied Ichthyology, 33(2): 270–273. doi: 10.1111/jai.13309

Chen Tingting, Jiang Tao, Lu Mingjie, et al. 2016. Microchemistry analysis of otoliths of Coilia nasus and Coilia brachygnathus from the Jingjiang section of the Yangtze River. Journal of Lake Sciences (in Chinese), 28(1): 149–155. doi: 10.18307/2016.0117

Cheng Fangyuan, Wang Qian, Delser P M, et al. 2019. Multiple freshwater invasions of the tapertail anchovy (Clupeiformes: Engraulidae) of the Yangtze River. Ecology and Evolution, 9(21): 12202–12215. doi: 10.1002/ece3.5708

Dai Libin, Hodgdon C, Tian Siquan, et al. 2020. Comparative performance of modelling approaches for predicting fish species richness in the Yangtze River Estuary. Regional Studies in Marine Science, 35: 101161. doi: 10.1016/j.rsma.2020.101161

Dou Shuozeng, Yokouchi K, Yu Xin, et al. 2012. The migratory history of anadromous and non-anadromous tapertail anchovy Coilia nasus in the Yangtze River Estuary revealed by the otolith Sr:Ca ratio. Environmental Biology of Fishes, 95(4): 481–490. doi: 10.1007/s10641-012-0042-1

Filina E A, Budanova L K. 2015. On the finding of mature individuals of the Greenland halibut Reinhardtius hippoglossoides (Pleuronectidae) in the Kara Sea. Journal of Ichthyology, 55(1): 138–142. doi: 10.1134/S0032945214060058

Gao Lei, Cheng Fei, Song Yiqing, et al. 2018. Patterns of larval fish assemblages along the direction of freshwater input within the southern branch of the Yangtze Estuary, China: implications for conservation. Journal of Freshwater Ecology, 33(1): 97–114. doi: 10.1080/02705060.2018.1426503

Ge Keke, Zhong Junsheng. 2010. Daily-age structure and growth characteristics of Coilia nasus larvae and juveniles in the surf zone of Yangtze River Estuary. Acta Hydrobiologica Sinica (in Chinese), 34(4): 716–721. doi: 10.3724/SP.J.1035.2010.00716

Hall C J, Jordaan A, Frisk M G. 2012. Centuries of anadromous forage fish loss: consequences for ecosystem connectivity and productivity. BioScience, 62(8): 723–731. doi: 10.1525/bio.2012.62.8.5

Hou Xuejiao, Feng Lian, Tang Jing, et al. 2020. Anthropogenic transformation of Yangtze Plain freshwater lakes: patterns, drivers and impacts. Remote Sensing of Environment, 248: 111998. doi: 10.1016/j.rse.2020.111998

Huang Liangliang, Li Jianhua. 2016. Status of freshwater fish biodiversity in the Yangtze River Basin, China. In: Nakano S I, Yahara T, Nakashizuka T, eds. Aquatic Biodiversity Conservation and Ecosystem Services. Singapore: Springer, 13–30

Huang Liangliang, Wu Zhiqiang, Li Jianhua. 2013. Fish fauna, biogeography and conservation of freshwater fish in Poyang Lake Basin, China. Environmental Biology of Fishes, 96(10): 1229–1243. doi: 10.1007/s10641-011-9806-2

Jiang Tao, Liu Hongbo, Huang Honghui, et al. 2019. Migration patterns and habitat use of the tapertail anchovy Coilia mystus in the Oujiang River Estuary and the Zhujiang River Estuary, China. Acta Oceanologica Sinica, 38(8): 35–40. doi: 10.1007/s13131-019-1436-0

Jiang Tao, Liu Hongbo, Lu Mingjie, et al. 2016. A possible connectivity among estuarine tapertail anchovy (Coilia nasus) populations in the Yangtze River, Yellow Sea, and Poyang Lake. Estuaries and Coasts, 39(6): 1762–1768. doi: 10.1007/s12237-016-0107-z

Jiang Tao, Liu Hongbo, Shen Xinqiang, et al. 2014. Life history variations among different populations of Coilia nasus along the Chinese coast inferred from otolith microchemistry. Journal of the Faculty of Agriculture, Kyushu University, 59(2): 383–389,

Jiang Tao, Liu Hongbo, Yang Jian. 2015a. Characteristics of C and O stable isotope in otolith of juvenile Coilia nasus from the Changjiang River Estuary. Marine Sciences (in Chinese), 39(6): 48–53. doi: 10.11759//hykx20140622001

Jiang Xiaoming, Pan Baozhu, Sun Zhiwei, et al. 2020. Application of taxonomic distinctness indices of fish assemblages for assessing effects of river-lake disconnection and eutrophication in floodplain lakes. Ecological Indicators, 110: 105955. doi: 10.1016/j.ecolind.2019.105955

Jiang Tao, Yang Jian, Liu Hongbo, et al. 2012. Life history of Coilia nasus from the Yellow Sea inferred from otolith Sr:Ca ratios. Environmental Biology of Fishes, 95(4): 503–508. doi: 10.1007/s10641-012-0066-6

Jiang Tao, Yang Jian, Lu Mingjie, et al. 2017. Discovery of a spawning area for anadromous Coilia nasus Temminck et Schlegel, 1846 in Poyang Lake, China. Journal of Applied Ichthyology, 33(2): 189–192. doi: 10.1111/jai.13293

Jiang Xuelian, Zhang Yu, Zhong Junsheng, et al. 2015b. Study on relationship between distribution of zooplankton and Coilia nasus larvae feeding features in the surf zone of Yangtze River Estuary. Resources and Environment in the Yangtze Basin (in Chinese), 24(9): 1507–1513

Karakulak S, Oray I, Corriero A, et al. 2004. Evidence of a spawning area for the bluefin tuna (Thunnus thynnus L. ) in the eastern Mediterranean. Journal of Applied Ichthyology, 20(4): 318–320. doi: 10.1111/j.1439-0426.2004.00561.x

Kayaba T, Wada T, Kamiyama K, et al. 2014. Gonadal maturation and spawning migration of stocked female barfin flounder Verasper moseri off the Pacific coast of northern Japan. Fisheries Science, 80(4): 735–748. doi: 10.1007/s12562-014-0764-4

Keller D H, Zelanko P M, Gagnon J E, et al. 2018. Linking otolith microchemistry and surface water contamination from natural gas mining. Environmental Pollution, 240: 457–465. doi: 10.1016/j.envpol.2018.04.026

Khumbanyiwa D D, Li Mengmeng, Jiang Tao, et al. 2018. Unravelinghabitat use of Coilia nasus from Qiantang River of China by otolith microchemistry. Regional Studies in Marine Science, 18: 122–128. doi: 10.1016/j.rsma.2018.02.001

Li Mengmeng, Jiang Tao, Khumbanyiwa D D, et al. 2017. Reconstructing habitat history of Coilia nasus from the Hexian section of the Yangtze River in Anhui Province by otolith microchemistry. Acta Hydrobiologica Sinica (in Chinese), 41(5): 1054–1061

Li Yuxuan, Xie Songguang, Li Zhongjie, et al. 2007. Gonad development of an anadromous fish Coilia ectenes (Engraulidae) in lower reach of Yangtze River, China. Fisheries Science, 73(6): 1224–1230. doi: 10.1111/j.1444-2906.2007.01459.x

Liang Cui, Pauly D. 2017. Growth and mortality of exploited fishes in China’s coastal seas and their uses for yield-per-recruit analyses. Journal of Applied Ichthyology, 33(4): 746–756. doi: 10.1111/jai.13379

Limburg K E, Waldman J R. 2009. Dramatic declines in North Atlantic diadromous fishes. BioScience, 59(11): 955–965. doi: 10.1525/bio.2009.59.11.7

Littrell K A, Ellis D, Gephard S R, et al. 2018. Evaluating the potential for prezygotic isolation and hybridization between landlocked and anadromous alewife (Alosa pseudoharengus) following secondary contact. Evolutionary Applications, 11(9): 1554–1566. doi: 10.1111/eva.12645

Liu Hongbo, Jiang Tao, Yang Jian. 2018. Unravelling habitat use of Coilia nasus from the Rokkaku River and Chikugo River estuaries of Japan by otolith strontium and calcium. Acta Oceanologica Sinica, 37(6): 52–60. doi: 10.1007/s13131-018-1190-8

Liu Fei, Lin Pengcheng, Li Mingzheng, et al. 2019. Situations and conservation strategies of fish resources in the Yangtze River Basin. Acta Hydrobiologica Sinica (in Chinese), 43: 144–156. doi: 10.7541/2019.177

Ložys L, Shiao J C, Iizuka Y, et al. 2017. Habitat use and migratory behaviour of pikeperch Sander lucioperca in Lithuanian and Latvian waters as inferred from otolith Sr:Ca ratios. Estuarine, Coastal and Shelf Science, 198: 43–52,

Mattocks S, Hall C J, Jordaan A. 2017. Damming, lost connectivity, and the historical role of anadromous fish in freshwater ecosystem dynamics. BioScience, 67(8): 713–728. doi: 10.1093/biosci/bix069

McDowall R M. 2001. Diadromy, diversity and divergence: implications for speciation processes in fishes. Fish and Fisheries, 2(3): 278–285. doi: 10.1046/j.1467-2960.2001.00050.x

Mei Zhigang, Cheng Peilin, Wang Kexiong, et al. 2020. A first step for the Yangtze. Science, 367(6484): 1314. doi: 10.1126/science.abb5537

Rodionov S, Overland J E. 2005. Application of a sequential regime shift detection method to the Bering Sea ecosystem. ICES Journal of Marine Science, 62(3): 328–332. doi: 10.1016/j.icesjms.2005.01.013

Santana F M, Morize E, Labonne M, et al. 2018. Connectivity between the marine coast and estuary for white mullet (Mugil curema) in northeastern Brazil revealed by otolith Sr: Ca ratio. Estuarine, Coastal and Shelf Science, 215: 124–131,

Sokta L, Jiang Tao, Liu Hongbo, et al. 2020. Loss of Coilia nasus habitats in Chinese freshwater lakes: an otolith microchemistry assessment. Heliyon, 6(8): e04571. doi: 10.1016/j.heliyon.2020.e04571

Suzuki K W, Kanematsu Y, Nakayama K, et al. 2014. Microdistribution and feeding dynamics of Coilia nasus (Engraulidae) larvae and juveniles in relation to the estuarine turbidity maximum of the macrotidal Chikugo River Estuary, Ariake Sea, Japan. Fisheries Oceanography, 23(2): 157–171. doi: 10.1111/fog.12051

Taddese F, Reid M R, Closs G P. 2019. Direct relationship between water and otolith chemistry in juvenile estuarine triplefin Forsterygion nigripenne. Fisheries Research, 211: 32–39. doi: 10.1016/j.fishres.2018.11.002

Wynne M L P, Wilson K A, Limburg K E. 2015. Retrospective examination of habitat use by blueback herring (Alosa aestivalis) using otolith microchemical methods. Canadian Journal of Fisheries and Aquatic Sciences, 72(7): 1073–1086. doi: 10.1139/cjfas-2014-0206

Xu Zhi, Ma Jing, Wang Hao, et al. 2018. River discharge and saltwater intrusion level study of Yangtze River Estuary, China. Water, 10(6): 683. doi: 10.3390/w10060683

Xu Gangchun, Nie Zhijuan, Zhang Chengxiang, et al. 2012. Histological studies on testis development of Coilia nasus under artificial farming conditions. Journal of Huazhong Agricultural University (in Chinese), 31(2): 247–252

Yang Jiangshuai, Arai T, Liu Hongbo, et al. 2006. Reconstructing habitat use of Coilia mystus and Coilia ectenes of the Yangtze River Estuary, and of Coilia ectenes of Taihu Lake, based on otolith strontium and calcium. Journal of Fish Biology, 69(4): 1120–1135. doi: 10.1111/j.1095-8649.2006.01186.x

Yuan Chuanmi. 1987. Spawning migration of Coilia nasus. Bulletin of Biology (in Chinese), 22(12): 1–4

Yuan Chuanmi. 1988. The resources and population composition and causes of Coilia nasus in the middle and lower reaches of the Yangtze River. Journal of Zoology (in Chinese), 23(3): 15–18

Yuan Chuanmi, Lin Jinbang, Qin Anling, et al. 1976. On the classification history and status quo of genus Coilia in China. Journal of Nanjing University: Natural Sciences Edition (in Chinese), (2): 1–12

Zhu Dongliang. 1992. Observations and studies on embryonic development and natural reproduction of Coilia nasus in Yangtze River Estuary. Fisheries Science & Technology Information (in Chinese), 19(2): 49–51

施引文献

资源附件(0)

访问统计

点击查看大图

图(6) / 表(1)

计量

文章访问数: 292
HTML全文浏览量: 111
PDF下载量: 13
被引次数: 0

doi: 10.1007/s13131-022-2135-9

计量

出版历程

Otolith microchemical evidence revealing multiple spawning site origination of the anadromous tapertail anchovy (Coilia nasus) in the Changjiang (Yangtze) River Estuary

Corresponding author: jiany@ffrc.cn

计量

出版历程

目录