Morphological changes of silver and bighead carp in the Yangtze River over the past 50 years

YU Hong-Xia, TANG Wen-Qiao, LI Si-Fa

(Laboratory of Ichthyology, Shanghai Ocean University, Key Laboratory of Exploration and Utilization of Aquatic Genetic Resources, Ministry of Education, Shanghai 200090, China)

Morphological changes of silver and bighead carp in the Yangtze River over the past 50 years

YU Hong-Xia, TANG Wen-Qiao*, LI Si-Fa

(Laboratory of Ichthyology,Shanghai Ocean University,Key Laboratory of Exploration and Utilization of Aquatic Genetic Resources,Ministry of Education,Shanghai200090,China)

Multivariate analysis was adopted to analyze 30 morphometrical characteristics of 121 one-year-old juvenile silver carp (Hypophthalmichthys molitrix) and bighead carp (Aristichthys nobilis) bred during the 1950s (“the former population”) and 2008 (“the current population”) and collected from the middle reach of the Yangtze River. The average discriminant accuracies of the former and current silver and bighead carp population were 94.2% and 98.0%,respectively. Discriminant analysis also revealed that significant differences in morphology occurred between the former and current populations of both carp in overall characteristics. One-way analysis of variance indicated that between former and current populations, silver carp showed highly significant differences (P＜0.01) in twelve of their characteristics and significant differences (P＜0.05) in eight of their characteristics, while bighead carp showed highly significant differences (P＜0.01) in eight of their characteristics and significant differences (P＜0.05) in eight of their characteristics. Six head morphology variables of the current silver and bighead carp were significantly or highly significantly larger than the former populations; fourteen characteristics of silver carp and ten characteristics of bighead carp of the current populations, mainly reflecting truck and tail morphology, were significantly or very significantly smaller than the former populations. Our results indicate that silver and bighead carp have developed a larger head and smaller truck and tail during the last 50 years. Due to such morphological changes, it seems apparent that the heads of these fish species need to be considered in regards to human diets, particularly in relation to economic and nutritious value.

Silver carp; Bighead carp; 50 years breeding; Morphological change; Yangtze River

As early as the Tang Dynasty, silver carp(Hypophthalmichthys molitrix) and bighead carp(Aristichthys nobilis) have been the main type of fresh water fish cultivated in China. Together with grass carp(Ctenopharyngodon idellus) and black carp(Mylopharyngodon piceus), they are considered China’s major carp species. Following the successful breeding of these species during the late 1950s, cultivation of silver and bighead carp has been introduced to 80 countries and 68 regions around the world and they now have the highest aquaculture output in China and globally(Schofield et al, 2005). The Yangtze River, a high quality gene pool of the four major Chinese carp, has attracted significant scientific attention in regards to the biological characteristics of silver and bighead carp and its resource status (Survey Team of Spawning Grounds of Domestic Fishes in Yangtze River, 1982; Li et al, 1995; Liu et al,1992; Chen et al, 1995; Liu et al, 1997, 2004; Qiu et al,2002). In the last three decades, however, natural fishery resources have been seriously damaged as a result of excessive fishing, water pollution, and hydro project construction. Additionally, large groups of farmed fish have been released into the Yangtze River, which has disrupted this natural gene bank. To protect such fishery resources, it is important to track the genetic conditions of silver and bighead carp in the Yangtze River, as well as changes in their biological characteristics (Cao, 2008).

A number of intensive studies on the morphological and growth characteristics of silver and bighead carp have been conducted in China, which have identified the morphological standards for their original populations(Li et al, 1989, 1990, 1995; Liu et al, 1992; Sun et al,1992; Ding et al, 2003; Yu et al, 2009). As the oldest and simplest way to detect quantitative characteristics controlled by polygenes, morphometry not only reflects genetic conditions but also cultured capability. Based on a good understanding of the phenotypic changes of silver and bighead carp during their ontogenetic process (Yu et al, 2010), we measured the external morphological characteristics of one-year-old silver and bighead carp collected during the mid 20thcentury and early 21stcentury to reveal the morphological variation trends of these Yangtze River carp after 50 years of successful breeding. This was achieved through multivariate morphometrics to provide a basis to evaluate their genetic changes.

1 Materials and Methods

1.1 Materials

The former population was comprised of specimens collected during the 1950s by the Institute of Hydrobiology, Chinese Academy of Sciences and deposited in the Freshwater Fish Museum, which included 20 silver carp and 17 bighead carp. The current population was collected in 2008 from the National Laojianghe Primary Breeding Farm for the Four Domesticated Fishes (29°35′N, 113°00′E) in Jianli County, Hubei Province, which included 32 silver carp and 42 bighead carp. All specimens were undamaged and possessed a normal body shape. The specimens were preserved in 10% formalin solution. All fish for the two species were one year old, with age determined for the current specimens from scales below of dorsal fin and above the lateral line and for historical specimens based on similar size ranges to the current specimens(Tab. 1).

Tab. 1 Number and size of Hypophthalmichthys molitrix and Aristichthys nobilis

1.2 Morphometrical methods

Pictures were taken indoors. The lens was positioned perpendicular to the fish body at a distance four times as long as the length of fish body. The photos were then used as the measuring object. A total of 30 traditional characteristics and frame parameters were measured (Tab. 2). All data were obtained from the left side of the fish. Traditional characteristics measured included full body length, head length, proboscis length,eye orbit diameter, body depth, pectoral fin length,caudal peduncle length, caudal peduncle depth, and head depth. Ten anatomical coordinate points were selected as the measuring point for frame data (Fig. 1) (Bookstein et al, 1985; Li et al, 1990; Xie et al, 2003; Min et al, 2009)and a total of 21 frame data were built. All measurements were the distances between point to point, calculated from the pictures and measurement software and accurate to 0.01 mm.

Tab. 2 Morphometric characteristics taken on the specimen

Fig. 1 Schematic measurement for truss network

1.3 Data analysis

Meristic measurements vary greatly in magnitude values. To weigh in measurements of smaller absolute values, snout length and eye diameter were standardized to head length and the remaining measurements were standardized to total body length. All data were first tabulated with Microsoft Excel, and then analyzed with SPSS 11.0 (Yu et al, 2003).

Discriminant functions were established using the stepwise method, and samples were categorized based on the discriminant functions. Function accuracy was then tested (Li et al, 1998).

One-way analysis of variance was used to test differences between groups.

2 Results

2.1 Discriminant analysis of overall differences in characteristics

Discriminant formulas for the former and current populations were established according to the nine measurable characteristics and twenty-one frame numbers after standardization, respectively. To facilitate discrimination, we selected five parameters from the thirty normalizing morphological parameters and established useful discriminant formulas. The five parameters that best discriminate silver carp are X7, X9,X10, X12, and X13. The corresponding determinant formula is as follows:

For the former population:

The five parameters that best discriminate bighead carp areX2,X3,X8,X25, andX30. The corresponding discriminant formula is as follows:

For the former population:

The subscripts of the variables are the codes of characters.

The discriminant results are found in Tab. 3 and Tab.4, which show that discriminant accuracy of the former silver carp population was 95.0% and the discriminant accuracy of the current silver carp population was 93.8%;and the discriminant accuracy of the former bighead carp population was 95.0% and the discriminant accuracy ofthe current bighead carp population was 93.8%. The discriminant effects of both groups were very significant(P＜0.01). Such results indicate significant differences between the former and current populations of silver and bighead carp in their overall characteristics.

Tab. 3 Discriminant analysis of the two Hypophthalmichthys molitrix populations (based on five selected parameters)

Tab. 4 Discriminant analysis of the two Aristichthys nobilis populations (based on five selected parameters)

2.2 One-way analysis of variance of Specific Character Changes

To determine which characteristics experienced specific changes between the current and former populations, we conducted single-factor variance analysis of the 30 parameters used to discriminate the two population groups (Tab. 5 and Tab. 6). Results demonstrated that between former and current populations, silver carp showed highly significant differences (P＜0.01) in twelve characteristics and significant differences (P＜0.05) in eight characteristics.Among all characteristic parameters, six representing head morphology (head length, head back length, snout length, eye orbit diameter, tip of snout, and starting point of pectoral fins) became larger, while fourteen representing length and depth of trunks and tails become smaller.

Between former and current populations, bighead carp showed highly significant differences (P＜0.01) in eight and significant differences (P＜0.05) in eight of their characteristic parameters. Among all characteristicparameters, six representing head morphology (head length, head depth, head back length, snout length, tip of snout, and starting point of pectoral fins) and the starting point of pelvic fin became very significantly larger, while ten including eye orbit diameter, pectoral fin length, and length and depth of trunks and tails become smaller.

Tab. 5 Characteristics of high variance between the two Hypophthalmichthys molitrix populations

Tab. 6 Characteristics of high variance between the two Aristichthys nobilis populations

3 Discussion

The National Laojianghe Primary Breeding Farm is located in Jianli county of Hubei Province. The farm’s water body was formed naturally in 1901 as a remnant lake on the north in Jianli Section, Middle Reaches of the Yangtze River. In 1958, dams were constructed at the entrance and exit of the water way, forming a narrow horseshoe lake 22.5 km long, 1.1 km wide, and encompassing a 49.4 km of shoreline. Under normal conditions, when the water level is 27.5 m, the water surface area is 1840 km2, with the greatest water body depth of 19 m and average depth of 6 m. In 1991, the“Four Domesticated Fish Natural Germplam Resources Ecological Reserve of the Yangtze Water System” was established by the Ministry of Agriculture to protect these resources at the population level. Wild larva fish are collected from near the Yangtze River in May-June each year. The larvae are reared in the nursery pond until fish fry, when they were released into the lake without artificial feeding.

The largest silver or bighead carp living in the Yangtze River weigh up to 40 kg. The majority of silver carp become sexually mature at the age of three, while bighead carp become sexually mature at the age of four to five. Most parent fish breed in reaches possessing torrents and eddies, whilst young fish and already spawned parent fish tend to swim inhabit river bends and lakes for food and hibernation. During the process of growing from larva to adults, however, allometry occurs in some morphological characteristics (Osse et al, 1995)and overall features may change with individual ontogeny. According to our previous studies in the Yangtze River, significant allometry occurred in 73.3%of the morphological characteristics for silver carp between one and two years old and 56.7% for bighead carp between two and three years old. However, there was no significant allometry in the characteristic parameters of the same age group (Yu et al, 2010)

The specimens analyzed in this paper were all one-year old juveniles of similar body length, which allowed for natural differences arising from allometry to be eliminated. The average discriminant accuracies of former and current populations of silver and bighead carp were 94.2% and 98.0%, respectively, which indicates significant changes have taken place in the gross morphology of silver and bighead carp in the Yangtze River over the past 50 years. Single-factor analysis of variance indicated that between former and current populations, silver carp showed significant or very significant differences in 66.7% of their characteristics whereas bighead carp show significant or very significant differences in 53.3% of their characteristics. Among all characteristics, six related to the head morphology of silver and bighead carp became significantly or very significantly larger, while fourteen related to the trunks and tails of silver carp and ten of bighead carp became significantly or very significantly smaller. These results show that during the past 50 years,the heads of silver and bighead carp in the Yangtze River have tended to increase in size, while their trunks and tails have tended to decrease in size.

These morphological changes reflect the possible differences of silver and bighead carp in genetic factors and living environment before and after breeding over the last 50 years. Though the biological significance of such changes in fish populations and their heredity mechanisms remain unknown, such changes can be considered desirable. Previous studies have found that silver and bighead carp heads are not only rich in EPA,DHA, and EAA but also contain higher contents of fat,calcium, and phosphor than their muscles (Li et al, 2008).The economic and nutritious value of silver and bighead carp heads is, therefore, much greater than of their trunks.

Bookstein FL, Chernoff B, Elder RL, Humphries JM, Smith GR,Strauss RE. 1985. Morphometrics in Evolutionary Biology [M].Philadelphia: the Academy of Natural Science Special Publication.

Cao WX. 2008. Expert forum: The Yangtza Valley water ecological environment and sustainable economic development -Several issues on the protection of fish resources in Yangtze River Basin[J].Res Env Yangtza Valley, 17(2): 163-164. (in Chinese)

Chen DQ, Qiu SL, Huang MG, Liu SP. 1995. On the dynamic monitoring of fish resources in the Yangtze River [J].Res Env Yangtza Valley, 4(4): 303-307. (in Chinese)

Huysentruyt F, Devaere S. 2009. Early development and allometric growth in the armoured catfishCorydoras aeneus[J].Hydrobiologia, 627: 45-54.

John MC. 1990. Growth and relative size of calcified structures of fish[J].Trans Am Fish Soc, 119(4): 673-688.

John R, Post E, Parkinson A. 2001. Energy allocation strategy in young fish: Allometry and survival [J].Ecology, 82(4): 1040-1051.

Li HM, Liu DD, Ji H, Yu EM, Shan ST. 2008. Study on food price of the head of bighead carp[J].Food Nutr Chn, (6): 53-55. (in Chinese)

Li SF, Lu GQ, Zhou BY. 1995. Feasibility studies on genetic conservation of Chinese carp in swan oxbow of the Yangtze River[J].Res Env Yangtza Valley, 19(3): 193-202 . (in Chinese)

Li SF, Wu LZ, Wang Q, Qiu QR, Chen YL.1990. Genetical Characterization of Silver Carp, Bighead Carp and Grass Carp in Yangtze River, Pearl River and Heilongjiang River [M]. Shanghai:Shanghai Sci-Tech Publisher, 109-124. (in Chinese)

Li SF, Zhou BY, Lu GQ, Zhao JL. 1997. A study on the criteria and inspection of brooders of silver carp, bighead carp, grass carp and black carp originated from the Yangtze river [J].J Fish Chn, 21(2):143-151. (in Chinese)

Li SF, Zhou BY, Ni CK, Chen ZQ. 1989. Morphological variations of silver carp, bighead and grass carp from Changjiang, Zhujiang and Heilongjiang Rivers [J].Acta Zool Sin, 35(4): 390-398. (in Chinese)

Liu JK, Cao WX. 1992. Fish resources of the Yangtze River basin and the tactics for their conservation [J].Res Env Yangtza Valley, 1(1):17-23. (in Chinese)

Liu SP, Chen DQ, Duan XB, Qiu SL, Huang MG. 2004. Monitoring of the four famous Chinese carp resources in the middle and upper reaches of the Yangtze River [J].Res Env Yangtza Valley, 3(2):183-186. (in Chinese)

Liu SP, Chen DQ, Zhang JB, Qiu SL, Fan QX. 2002. Studies on the natural resources reservoir of the four major Chinese carp in Laojianghe oxbow[J].Acta Hydr Sin, 26(6): 628-634. (in Chinese)

Liu SP, Qiu SL, Chen DQ, Huang MG. 1997. Protection and rational utilization of the germplasm resources of the four major Chinese carp in the Yangtze River system [J].Res Env Yangtza Valley,6(2):128-130. (in Chinese)

Min R, Ye L,Chen XY, Yang JX. 2009. Morphometrics analysis ofSinocyclocheilus grahami(Cypriniformes: Cyprinidae) [J].Zool Res, 30(6): 707-712. (in Chinese)

Osse JWM, van den Boogaar JGM. 1995. Fish larvae, development,allometric growth, and the aquatic environment[C]// Pittman K,Batty RS, Verreth J(eds). Mass Rearing of Juvenile Fish. ICES Marine Science Symposium, 201:21-34. Bergen.

Qiu SL, Liu SP ,Huang MG, Chen DQ, Duan XW. 2002. Monitoring of spawning sites of four major Chinese carp in the middle section of Yangtze River[J].Acta Hydr Sin,26(6): 716-718. (in Chinese)

Schofield PJ, Williams JD, Nico LD. 2005. Foreign Nonindigenous Carp and Minnows (Cyprinidae) in the United States: A Guide to Their Identification, Distribution, and Biology[M]. USGS Scientific Investigations Report 2005-5041, Denver, US.

Shan XJ, Cao L, Huang W, Dou SZ. 2009. Feeding, morphological changes and allometric growth during starvation in miiuy croaker larvae[J].Env Biol Fish, 86: 121-130. (in Chinese)

Survey Team of Spawning Grounds of Domestic Fishes in Yangtze River. 1982. A survey on the spawning grounds of the “Four famous Chinese Carp” in the Yangtze River after dammed by the key water control project at Gezhouba [J].J Fish Chn, 6(4):287-304.

Xie ZG, Xie CX, Zhang E. 2003. Morphological variations among the Chinese species ofSinibrama(Pisces: Teleostei: Cyprinidae), with comments on their species validities[J].Zool Res, 24(5): 321-330.(in Chinese)

Yu HX, Tang WQ, Li SF. 2009. Growth character of silver carp at National Original Breeding Farm in Lake Laojianghe, middle reaches of the Yangtze River [J].Chn J Zool,44 (2): 21-27. (in Chinese)

Yu HX, Tang WQ, Li SF. 2010. Ontogenetic changes in meristic measurements of silver Carp and bighead Carp[J].Zool Res, 31(2):169-176.

Yu JY, He XH. 2003. SPSS Statistical Data Analysis and Application[M]. Beijing: Posts & Telecom Press, 251-310. (in Chinese)

Zhang YT, Fang KT. 1982. Introduction to Multivariate Statistical Analysis[M]. Beijing: Science Press, 393-401. (in Chinese)

50年来长江鲢、鳙形态特征的变迁

于红霞, 唐文乔*, 李思发

(上海海洋大学鱼类研究室，水产种质资源发掘与利用教育部重点实验室, 上海 201306)

采用多元分析方法, 对采自长江中游的上世纪中期(下称早期)和本世纪初(下称当前)的121尾1龄鲢、鳙的30项形态度量性状进行了分析。依据对判别贡献最大的5个参数所建立的判别公式, 对鲢、鳙早期和当前群体的平均判别准确率分别达94.2%和98.%, 显示鲢或鳙的当前与早期群体间在总体上存在着显著差异。单因素方差分析显示, 在早期和当前群体间, 鲢有12个特征差异极显著、8个差异显著, 鳙分别有8个特征差异极显著或显著。其中, 鲢和鳙的6个显著或极显著变大的特征参数集中在头部, 而14个鲢和10个鳙的显著或极显著变小的特征参数则主要集中在躯干部与尾部。研究表明, 最近 50年来长江鲢、鳙的头及头部特征有相对变大的趋势, 而躯干部与尾部的许多特征参数则有相对变小的趋势, 这些形态演变趋势符合人们喜食鱼头、追求高经济效益的期望。

鲢; 鳙; 人工繁殖50年前后; 形态变迁趋势; 中国长江

Q959.468; Q954.1

A

0254-5853(2010)06-0651-06

2010-06-04; 接受日期：2010-10-29

于红霞(1982—), 女, 硕士研究生; 研究方向：鱼类学; E-mail：yuhongxia2002@163.com

10.3724/SP.J.1141.2010. 06651

date: 2010-06-04; Accepted date: 2010-10-29

s: National Natural Science Foundation of China (30630051); Aquaculture E-Institute of Shanghai Universities(03E009); Shanghai

Leading Academic Discipline Project(S30701)

*Corresponding author (通讯作者), E-mail: wqtang@shou.edu.cn

We are grateful to the Freshwater Fish Museum for providing former specimens. We also want to thank Prof. Liu Huanzhang who helped on several aspects of the work.