Osteological Development of the Vertebral Column and Caudal Complex in Larval and Juvenile Blackhead Seabream, Acanthopagrus schlegelii (Perciformes, Sparidae) (Bleeker, 1854)

Jing Hu1,2, Yan Liu2,3, Gang Yu1,2, Changping Yang2,3, Binbin Shan2,3, Shengnan Liu2,4 and Dianrong Sun2,3,*

1South China Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, Sanya 572018, China

2Key Laboratory of South China Sea Fishery Resources Exploitation and Utilization, Ministry of Agriculture, Guangzhou, 510300, China

3Key Laboratory of Fishery Ecology and Environment, Guangdong, Guangzhou, 510300, China

4Tianjin Agriculture Unitersity, Tianjin 300000, China

Jing Hu and Yan Liu contributed equally to this study and share first authorship.

ABSTRACT

Osteological development of the vertebral column and caudal complex in blackhead seabream was described under extensive larval rearing conditions from 1DPH to 36DPH. The development of vertebral column originated from the occurrence of neural arch and hypural on 5DPH (SL2.4-3.4mmm, NL1.8-2.4mm), then skeletal ossification and Segmental bone formation occurred on 11DPH (SL3.6-4.0mm, NL2.6-2.8mm) and finished on 21DPH (SL9.6-11.6mm, NL7.4-8.6mm); Neural arch developed earlier than haemal arch, while haemal spine earlier than neural spine, consistent with the ossification; The development and ossification of neural arch and neural spine occurred in the backward order, while haemal arch and haemal spine from central tail to bothsides, Whatʼs more, all ossification occurred from proximal to outward; Along with the development of vertebral column, urostyle curved on 15-17DPH(SL4.0-5.0mm, NL2.9-3.4mm), then finished on 21DPH(SL4.6-5.2mm, NL3.4-3.8mm). During this progress, individuals present strong vitality of life and active action. This study explored the morphological characteristics of vertebral column and caudal skeletal ontogeny in larval A. schlegelii, which provides fundamental information for future artificial breeding and taxonomy of A. schlegelii and other relative species.

Article Information

Received 08 June 2018

Revised 22 July 2018

Accepted 01 August 2018

Available online 12 July 2019

Authors’ Contribution

JH, YL, GY and DS designed this study. JH, YL, CY, BS and SL conducted the field works and analyzed the samples. JH drafted this manuscript.

Key words

Acanthopagrus schlegelii, Vertebral column, Caudal complex, Skeletal development.

DOI: http://dx.doi.org/10.17582/journal.pjz/2019.51.5.1859.1867

* Corresponding author: [email protected]

0030-9923/2019/0005-1859 $ 9.00/0

Copyright 2019 Zoological Society of Pakistan

Introduction

The blackhead seabream Acanthopagrus schlegelii as a typical commercially valuable recreation and aquaculture fishery species is a marine teleost belonging to the perciform family Sparidae and widely distributed in the West Pacific Coasts from Japan, Korea to the East China Sea (Jean et al., 1996). For the delicious taste and high nutritional value, it has become a major marine-cultured species in China and other areas of Asia (Jean et al., 1998). Many researches are focus on the artificial breeding, diseases, nutriology and molecular biology of A. schlegelii, no report of early development of skeleton (Ho and Lin, 2005; Ho et al., 2007; Jeong et al., 2007; Ngandzali et al., 2011; Jin et al., 2017).

The skeletal system of fish is necessary to the survivor and growth of individuals, as it play an important in protecting internal organs, supporting the body and connecting muscle, also the source of motivation for feeding and avoiding the predators (Kohno et al., 1983, 1996; Dasilao and Yamaoka, 1998). Skeletal development is closely correlated with changes in swimming mode and also supports the anatomical and functional needs (Matsuoka, 1997; Koumoundouros and Sfakianakis, 2001; Cheng et al. 2018). In general, early skeletal development of A. schlegelii is the key to its motor function, avoiding predators and feeding success. Comprehensive knowledge of the osteological development of fish not only provides the means for understanding relationship of relative species and the fundamental data base for species identification, but it also encourages the understanding of functional development and determines the conditions compatible with animal welfare (Koumoundouros and Sfakianakis, 2001; Huang et al., 2014). The osteological development in early stage closely relate with survivor of fish, as skeletal deformity leaded by unfavorable surrounding and poor nutrition will induce mass mortality, even if several survive, lack of market competitiveness with inferior external morphology, result in low breeding efficiency automatically (Koumoundouros et al., 1997; Wittenrich et al., 2009; Boglione et al., 2013). So the key to the success of aquiculture is the understanding of osteological development of fish in early stage. Double-stained method (Dingerkus and Uhler, 1977) was used to investigate the osteological development of larval and juvenile A. schlegelii, include the development of the vertebral column and caudal complex, which provide a certain taxonomic basis and contribute to the understanding of the functional trends and biological requirements in each developmental stage of individuals. This study will provide the foundational scientific basis of skeletal development of the Sparidae, and establishes a theoretical foundation for efficient aquaculture.

 

Materials and methods

Larval and juvenile rearing

Fertilized eggs of blackhead seabream were obtained from spawning tank through natural fertilization in a commercial fish hatchery, tropical Aquaculture Research and Development Center, South China Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, Hainan Province, P.R. China, and the experiment was conducted in situ. Eggs were hatched in 500L fiberglass incubators at 27.5°C On 2 days post-hatch (DPH), larvae were reared into three 2500L tanks at a density of 60 fish·L-1. Each rearing tank was supplied with filtered seawater (5µm pores) with a daily water exchange rate of 200% of the tank volume. Daily photoperiod of 14 h light and 10 h dark with 2000 lux light intensity was maintained at the water surface. The water temperature, salinity, PH, and dissolved oxygen were maintained at 29.0±1.0°C, 33 ± 0.8 ppt, 7.8-8.1 and 6.5 ± 0.2 mg L-1, respectively. Total ammonia nitrogen < 0.1 mg L-1, and nitrite nitrogen < 0.05 mg L-1.

In the following feeding trials, the experimental condition was kept same as follows and any environmental modification was specified in each trial. One air stone was used in each bucket to maintain dissolved oxygen to near saturation. Fish were fed with rotifers (Brachionus rotundiformis) from 2 DPH to 9 DPH (SL 4.50±0.10mm)at a density of 10-20 rotifers mL-1. On 7 DPH, Artemia nauplii were introduced for co-feeding at 20-30nauplii mL-1 with B. rotundiformis deing contrast till 17DPH. Afterwards, B. rotundiformis were gradually replaced by Artemia salina from 18 DPH at 50-60 mL-1 Artemia salina with contrasting Artemia nauplii till the end of experiment. Live foods were enriched with the DHA protein Selco (INVE Aquaculture, Salt Lake City, UT, USA) for 12hours before feeding. To sure significant food and green surrounding, Nannocholoropsis sp. was induced during feeding of rotifer. Filters were cleaned to prevent outlet were choked up and siphon method was used to eliminate excrement, residue and dead organism daily.

Observations and measurements

A total of 20 samples were collected from rearing tankson1, 2, 3, 4, 5, 6, 7, 9, 11, 13, 15, 17, 19, 21 and 24 DPH respectively, and then anaesthetized with Aqui-S (AQUI-S New Zealand Ltd., Lower Hutt, New Zealand) at 40mgL-1. The individuals were observed under microscopic to eliminate individuals with abnormal osteological development and measure standard and notochord length of normal ones. Then followed the protocol as following: initially fixed in 10% neutral buffered formalin, and then stained with alcian blue and alizarin red followed by Taylor and Van Dyke (1985). After staining, samples were photographed under stereomicroscope (Olympus SZ40) equipped with a digital camera (Oneplus, 2001). A total of 400 larvae and juveniles were stained and photographed to identify the development of the vertebral column and caudal complex. The terminologies of the skeleton were adopted from Kihara et al. (2002) and Sfakuanakis et al. (2004) and classification of developmental stage followed Kendall et al. (1984).

 

Results

Vertebral column

Including the urostyle, the number section of the vertebra is 24, as the support components of vertebral column (Fig. 1). The vertebral column was formed by the vertebral centra, the neural and haemal arches and spines, the parapophyses and the ventral ribs. At hatching and in early ages of larval A. schlegelii, no metamerisms were observed (Fig. 1A-C). In this stage, the straight notochord was the only visible support structure that extended through the body at that period (1DPH, yolk-sac developmental stage, SL2.0-3.0mm, NL1.5-1.9mm, Fig. 1A). The first elements to be seen in the vertebral column are the neural and hypurals processes, which start to develop on 5-7 DPH (SL2.4-3.4mm, NL1.8-2.4mm). Their formation takes place via two developmental centers, front-end of notochord and middle part of caudal, respectively.

 

Each neural arch is composed of a pair of cartilage, located on both sides of the center of notochord back. The formation and ossification of neural arch both occurred backwards (Fig. 1B). On 9DPH (SL3.2-3.8mm, NL2.4-2.6mm, Fig. 1C), haemal arch was observed, and the process of formation occurred from the central part of caudal to anterior and posterior. Ossified parapophysis present through a budding process. At the same time, Ossified haemal spine occurred on the next few ventralis vertebra of vertebral body where parapophysis occurred. On 11DPH (SL3.6-4mm, NL2.6-2.8mm, Fig. 1D), inter-segmental vertebrae occurred, Ossified haemal spine and neural spine increased. Cartilaginous neural arch began to modified, and ossification of vertebral column processed in the same direction of neural arch. On 13DPH (SL4.2-5.0mm, NL3.0-3.4mm, Fig. 1E), the ossification process reach to the caudal end, and the three ossified parapophysis occurred at the time. The upward flexion of the urostyle significantly and the caudal rays started to ossify within the primordial fin, in the area adjacent to the cartilaginous hypurals. Till 17DPH (SL4.6-5.2mm, NL3.4-3.8mm, Fig. 1F), major vertebral body formed, except to the modified neural spine in the caudal region, the formation of other elements of vertebral column, as vertebral body, haemal spine and neural spine all are finished. The upward flexion of the urostyle process further to the angle of 30, and began to ossify in partial. On 21DPH (SL9.6-11.6mm, NL7.4-8.6mm, Fig. 1G), expect to the end of the urostyle, the ossification of vertebral column finished completely, the urostyle stop to curve anymore, all vertebral body formed in this stage. On 24 DPH (SL14.2-16.1mm, NL9.8-10.7mm, Fig. 1H), the ossification of vertebral body was finished and connect one by one, then the anterior and posterior apophyse occurred. The skeleton formed basically in this stage. During the development, neural arch developed and ossified earlier than haemal arch, while haemal spine earlier than neural spine, all ossification occurred from proximal to outward.

Caudal complex

The first four days after hatching, no development of caudal skeleton occurred, without caudal plates and fin rays, and the upwarp of urostyle also haven’t happened this time (Fig. 2A). About 5DPH (SL2.3-3.3mm, NL1.7-2.3mm, Fig. 2B), as the developmental origin of caudal skeleton, the occurrence of cartilaginous hypurals located (Hy1)on veutro of after-end of notochord consider as the first appearance of caudal skeleton. About 7 DPH (SL2.4-3.4mm, NL1.8-2.4mm, Fig. 2C), Hy2 occurred by the offside of Hy1, and parhypural (Phy) began to differentiate and emerge. On 9DPH (SL3.2-3.8mm, NL2.4-2.6mm, Fig. 2D), with the appearance of five fin rays, Hy3 occurred by the offside of Hy2, and the first epural appeared right above the Hy1 through a budding process. Phy elongated, and cartilaginous haemal spine occurred by the left side. On 11-13DPH (SL3.6-5.0mm, NL2.6-3.4-2.8mm, Fig. 2E, F), Hy4, Hy5 successively occurred rightward. Incompletely ossified neural spine (NS) occurred in the upper section of middle part caudal region (Fig. 2E). Hy1-Hy3, Expand Phy enlarged significantly with fuzzy edge between each other, and the tail began to divide into two parts with the Ur curve upward significantly (Fig. 2E). In this stage, ossification of notochord in the caudal region hasn’t observed, and the fin ray number increase to 10. Completely ossified fin rays attached to the terminal of four hypurals. On 15-17DPH (SL4.0-5.2mm, NL2.9-3.8mm, Fig. 2G), the 6th hypural (Hy6) was observed. The Hy1-Hy5, Hs, Ns and Ep enlarge further with clearer edge. The number of fin rays increased to 14 and the notochord ossified to the front-end of CA. On 21 DPH (SL9.6-11.6mm, NL7.4-8.6mm, Fig. 2H), the process continue to conduct to the CA and the Ur ossified partly with maximum bending Angle. The whole CA was expanded and original caudal fork was observed. The intersegmental caudal fin rays began to ossify as the rudiment of caudal skeleton formed. In this stage, 17 fin rays ossified partly and attach to the terminal of Ep, Hy and Phy. The ossification process of notochord extended to Hy6, and Hy1-Hy6, Ep, Hs, Ns enlarged further with clear edge, as Hs and sectional hypurals began to ossify also. On and after 24 DPH (SL14.2-16.2mm, NL9.8-10.7mm, Fig. 2I), no significant alteration was observed of the caudal complex formation, the differences only focus on the degree of ossification of Ur, caudal fin plate and fin rays.

 

Discussion

Adaptability and peculiarity of the vertebral column of blackhead seabream

With the development of technology of shaping and observing animal skeleton specimen, conventional anatomy, histology, scanning technique, x-ray fluoroscopy and staining were common used (Roo et al., 2010; Cobcroft and Battaglene, 2013). Depend on the perfection of relevant technology, the study of fish skeleton improved consequently. As the advantage of low coat, easy operation, effective result and high-quality preserved sample, staining became the most popular method for study of skeletal ontogeny as double-stained method used in this study.

 

The difference of fish skeletal ontogeny is closely related to the environment and its own physiological function (Kohno et al., 1996). For example, the skeleton of Japanese rice fish (Oryzias latipes) (Langille and Hall, 1987) has begun to develop before hatch for the demand of swimming and feeding in larval stage; the vertebral column and caudal complex of Senegalese sole (Solea senegalensis) begin to develop on 12-13 DPH to adapt to benthic life (Gavaia et al., 2002). The study of fish skeletal ontogeny is one of the effective ways to grasp the relationship between structures and function (Fukuhara, 1992), and the understanding of relationship between skeletal ontogeny and the breeding environment can guide the artificial culture work effectively (Boglione et al., 2001). The skeletal ontogeny of Osteichthyes has a polymorphic development, and the development of various genera is much of a muchness. The skeletal ontogeny of the O. latipes (Langille and Hall, 1987) and Inimicus japonicas (Imamura and Yabe, 1997) and Salmonidae fishes begin to develop before hatch. Unlike these, the skeletal ontogeny of the A. schlegelii developed after hatching, which similar to that of the Trachinotus ovatu (Ma et al., 2014) and most of the Sparidae fishes (Doi et al., 2004). Similar to most Osteichthyes, the development of vertebral column of the A. schlegelii begins at the development of the hypura and neural, which was first found at 5DPH (SL2.4-3.4mm, NL1.8-2.4mm), while the developmental starting point of T. ovatus (Ma et al., 2014), I. japonicas (Imamura and Yabe, 1997), Siniperca chuatsi (Kendall et al., 1984), Coilia nasus (Chen et al., 2011) and Seriola dumerili (Laggis et al., 2010) are 7-9DPH (SL3.49-4.0mm), 8DPH (TL5.7mm), 6.4 mmNL, 11.5 mmNL and 4.6 mmSL, respectively. So, through the comparison, the development of vertebral column of A. schlegelii presents certain superiority in timing, as provides a basis for supporting the body and the further development of the feeding apparatus, and proved the relevant conclusion of rapid development and strong adaptability. The ossification process of vertebral column and the formation of intersegmental vertebrae occurred on 13 DPH (SL3.6-4.0mm, NL2.6-2.8mm), while the same process of T. ovatus (Ma et al., 2014), S. chuatsi (Kendall et al., 1984) and S. dumerili (Laggis et al., 2010) occurred on 11DPH, 11.5mmNL and 4.8mmNL (notochord length). Thus, from the aspect of ossification of vertebral column, the superiority in early development of A. schlegelii was proved further. Neural arch developed earlier than haemal arch, while haemal spine earlier than neural spine, consistent with the ossification; The same as T. ovatus (Ma et al., 2014), the development and ossification of neural arch and neural spine occurred in the backward order, while haemal arch and haemal spine from central tail to bothsides, What’s more, all ossification occurred from proximal to outward. Different from S. chuatsi (Kendall et al., 1984) as the formation and ossification of haemal arch and haemal spine both occurred in the backward order, while the ossification of neural arch and neural spine of I. japonicas (Imamura and Yabe, 1997) occurred from central part to proximal and outward. The formation and ossification of C. nasus are both different from A. schlegelii, as the ossification of haemal arch and haemal spine occurred in the backward order, and the ossification of each neural arch, neural spine, haemal arch and haemal spine occurred from central part to proximal and outward, similar to the I. japonicas (Imamura and Yabe, 1997). The above comparison results indicate that the understanding of skeletal ontogeny possess some taxonomic significance, confirm the inference that, as a kind of inferior fish, the C. nasus maybe a transitional species in the evolutionary process to a certain extent by Chen et al. (2011). The completion of the ossification process of vertebral column in A. schlegelii occurred on 24DPH (SL9.6-11.6mm, NL7.4-8.6mm), a little slower than T. ovatus (Ma et al., 2014) (18DPH, SL9.12mm), presents the diversity and complexity of the vertebrae development of Osteichthyes. The occurrence of this phenomenon may be related to the breeding management or environmental factors in the later stage (Aragão et al., 2001; Ma et al., 2012; ZamboninoInfante et al., 1997), and the relevant research needs to be carried out further.

Adaptability and peculiarity of the caudal complex of blackhead seabream

As big family, perciformes occupies larger proportion of marine economy fish trade, while blackhead seabream, as a typical species of artificial breeding, enhancement and releasing, of which the research in recent years has become increasingly mature (Xue et al., 2008; Ngandzali et al., 2011; Shi et al., 2012). Caudal fin of perciformes is characterized by no more than 17 fin rays, in the research of A. schlegelii, the fin rays have reaching a maximum of 17 on 21DPH, indicating a strong adaptability (Kohno et al., 1996).

The caudal fin has the function of propulsion and steering. In view of its complex formation and development process, the strengthening of function must be closely coordinated with the spinal extremities to provide effective impetus (Ignacio et al., 2008). The development of the caudal of blackhead seabream is closely consistent with the development of the vertebral column. The development of the caudal fin is accompanied by the curvature of the notochord, and the upwarping of the urostile is defined as the sign of entering the juvenile stage (Takushima et al., 2003), and the A. schlegelii presents a strong vitality and activity in this stage. The upwarping of A.schlegelii began on 15-17DPH (SL4.0-5.0mm, NL2.9-3.4mm), accompanied by the ossification of vertebral column and the formation of Segmental bone. The ossification process of urostileis completed on 21DPH (SL4.6-5.2mm, NL3.4-3.8mm), and all vertebral bodies have formed and the vertebral column ossified completely except urostile at this time. A high consistency and synchronicity was presented between vertebral column and urostile, providing a guarantee for the improvement of the related functions such as feeding and avoiding the predators. Based on the observation of caudal complex development, microscopic observations were conducted of blackhead seabream’s internal organs. The results show that, functional gastric developed completely on 17-21DPH, as a marker of division of larval and juvenile (Stroband and Kroon, 1981), presents a high consistency with the result of skeletal ontogeny study. The caudal complex of A. schlegelii mainly consists of six different sizes of hypural, three epural and one uroneural. Including Sparidae species, studies on skeletal ontogeny of various marine fish have been carried out in large numbers (Sfakianakis et al., 2005; Park et al., 2016; Zheng et al., 2016), as the results show that there is a certain difference in structure and developmental timing of caudal complex between species. Such as T. ovatus (Zheng et al., 2016), Sparus aurata (Koumoundouros et al., 1997), Diplodus sargus (Koumoundouros and Sfakianakis, 2001), D. puntazzo (Sfakianakis et al., 2005), Epinephelus akaara (Park et al., 2016) and Dentex dentex (Koumoundouros et al., 2001), the caudal complex of which all consist of five hypural, three epural and one uroneural, all of them have one less hypural, as the foundation of motor ability and feeding power, and suggests a strong adaptability to some degree. Although the structure of hypural of blackhead seabream differs from many marine fishes, the developmental timing is consistent with other fish, all in the left and right way in the caudal. In this study, the first hypural occurred on 5DPH (SL2.3-3.3mm, NL1.7-2.3mm) and the last 15-17DPH (SL4.0-5.0mm, NL2.9-3.4mm). The first-feeding occurred in the yolk sac (1-2DPH, SL1.9-2.1 mm,NL1.3-1.8mm) of the blackhead seabream, which means that blackhead seabream is transitioned from endogenous nutrition to exogenous nutrition, and then goes through the transformation of larval to juvenile on15-17DPH. The study found that, both based on the development of vertebral column and caudal complex can showed an advantage of adaptability to the environment, and present that blackhead seabream is superior to many marine fishes. This advantage provides physiological needs for feeding conversion and feeding of larval-juvenile fish, and the necessary guarantee for its survival and growth.

Taxonomic significance of the skeletal ontogeny of blackhead seabream

The research on the development of skeletal ontogeny not only has the economic benefit of farming, but also has great revelation for the classification of fish. The skeletal ontogeny of fishes varies greatly between species (Zheng et al., 2016), and the morphological characteristics of the skeletal ontogeny are an important basis for studying the classification of fish systems. Yang and Li (2008) compared the Parargyrops edita and S. latus, obtained the results that some significant differences exist between this two species expect for some common characteristics of sparidae, can be used as a basis for the identification of interspecies. Wang (1989) studied a vast amount of information for Sparidae in China seas, and compared their skull morphology and tooth characteristics. The results suggest that Sparus, Rhabdosargus, Evynnis and Parargyrops have close kinship, while Pagrosomus, Argyrops and Dentex are closely related. While very different from the results obtained from Akazaki (1962). A large number of scholars (Akazaki, 1962; De et al., 2001; Carpenter and Johnson, 2002; Day, 2002; Orrell et al., 2002; Orrell and Carpenter, 2004; Chiba et al., 2009) have conducted a taxonomic study of the Sparidae in various ways, including molecular biology, and there are great differences. Especially the study on phylogenetic relationship between A. schlegelii and A. schlegelii czerskii, thereʼs no clear and exact conclusion yet, lack of research support in osteology. Many research in osteological development of Sparidae have conducted, mainly focus on the early development and artificial breeding (Koumoundouros et al., 1997, 1999, 2001; Sfakianakis et al., 2005). The research on the use of skeletal ontogeny in taxonomy is slightly weak, and the combination of the related classification techniques will be an effective way to master the classification of the Sparidae.

 

Conclusions

A comprehensive understanding of the skeletal development improve the breeding efficiency of larval and juvenile fish and provide some evidence for taxonomy.This study has explored the skeletal ontogeny in blackhead seabream. Results from the present study would be useful to understand functional morphology and larval aquaculture of marine teleosts, and would be helpful to the classification of the Sparidae.

 

Acknowledgments

This project was supported by the China-ASEAN Maritime Cooperation Found (China-Vietnam Cooperation in Fishery Stock Enhancement in the Tonkin Gulf).

 

Statement of conflict of interest

Authors have declared no conflict of interest.

 

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