Research Article
Some Osteological Studies of Coptodon zillii (Gervais 1848) and Oreochromis aureus (Steindachner 1864) Collected Shatt al-Arab River, Basrah, Iraq 
,
Fawziah Sh. Habbeb2 
,
Mustafa A. Al-Mukhtar2 2 Department of marine vertebrates, Marine Science Centre, University of Basrah, Basrah, Iraq
Author Correspondence author
International Journal of Marine Science, 2018, Vol. 8, No. 4 doi: 10.5376/ijms.2018.08.0004
Received: 04 Dec., 2017 Accepted: 29 Dec., 2017 Published: 12 Jan., 2018
Jawad L.A., Habbeb F.S., and Al-MukhtarM.A., 2018, Some osteological studies of Coptodon zillii (Gervais 1848) and Oreochromis aureus (Steindachner 1864) collected Shatt al-Arab River, Basrah, Iraq, International Journal of Marine Science, 8(4): 26-32 (doi:10.5376/ijms.2018.08.0004)
This paper presents the results of a comparative study of the vertebral column regionalization of Coptodon zillii and Oreochromis aureus of the fish family Cichlidae. Osteological features that may prove valuable for taxonomic indications are defined, and on the basis of the material handled, their use to separate the two cichlid species. The morphological characteristics of the vertebral column of C. zillii and O. aureus allowed the separation of this bony structure into five morphologically distinct regions and the features of their specified vertebral shape. This regionalization is more complex than the classical division in truncal and caudal parts only. The vertebral length and height express a morphotype that may be linked with the cichlid mode of swimming.
Background
Fish identification is an important aspect that several studies depend on knowing the correct taxonomic status of the fish species. In the process of identification of fish specimens, several methods and techniques are usually used including the classic morphometric and meristic characters, osteology, and the recent molecular genetic aspects (Costa-Pier, 2003; Barriga-Sosa et al., 2004; Doherty and McCarthy, 2004).
Species wise, the fish family Cichlidae is considered among the richest teleosts families species. Members of this family are distributed in South and Central America, Madagascar, Africa, The Middle East, India and Sri Lanka (Kocher, 2004; Salzburger and Meyer, 2004). The taxonomy of the cichlid species encounters arguments as the systematics have been intensely studied (Chakrabarty, 2010; Dunz, 2012).
In both East and West Africa, most cichlid species are belong to the tribes Oreochromini and Coptodonini. The taxonomic validity of those species remains to be assessed as many species are still being described extent (Dunz and Schliewen, 2010a; 2010b; Dunz, 2012). Outside their original localities, the diversity of the African cichlid showed to be reduced (Teugels and Thys van den Audenaerde, 2003), but on the other hand signs of strains evolved to a new species were evident in the area where tilapia species have been transplanted (McAndrew, 2000; Costa-Pierce, 2003; Volff, 2005). Such new species need to be genetically checked in addition to the classical morphological traits.
The number and shape of the vertebrae are among the osteological characters that can be used to set apart the closely related species and at the same time resolve the taxonomic status of the species (Jawad and Al-Hassani, 2014 a; 2014 b; Jawad et al., 2014; Jawad, 2015).
Regionalization in the vertebral column of fish species can shows reasonable spectrum of variation (Ward and Brainerd, 2007). Classically known, the actinopterygian fishes have two well recognized regions in their vertebral column, the abdominal region and the caudal region (Grande and Bemis, 1998). Vertebrae have shown variation in their shape within each of the two regions (Ford, 1937; Pietsch, 1978; Grande and Bemis, 1998; Bemis and Forey, 2001; Ward and Brainerd, 2007). In several fish species (Jawad and Al-Hassani, 2014a; 2014b; Jawad et al., 2014; Jawad, 2015), anteriorly located vertebrae can be seen joined into the skull through ontogeny. Among such vertebrae are the Weberian apparatus of Ostariphysi and vertebrae that support abdominal ribs (Jawad, 2015). Two types of vertebrae were usually present in the caudal region of the vertebral column, vertebrae with haemal spines, and ural vertebrae with hypural. The sections in the vertebral column will rule the locomotory functions of the fish and expressed uniqueness of the vertebral column of the fish species by this regional pattern of vertebral structure (Laerm, 1976; Lindsey, 1978; Weihs, 1989; Ramzu et al., 1992). The vertebral column structure goes through several types of biological stresses that delivered by local and specific morphological peculiarities (Kubo and Asano, 1987; 1990; Desse et al., 1989).
The aim of the present work is to: (1) describe the morphology of the skeleton of the caudal fin; (2) to evaluate the implementation of these osteological characters to diagnose the two cichlid species examined; (3) to create a reference database containing of added osteological characters to those already in use in the systematics of the two species involved in this work. Such characters may create a more robust taxonomic system that can facilitate the separation of C. zillii and O. aureus studied.
1 Materials and Methods
In the present work, fresh specimens of both C. zillii and O. aureus were used to obtain the vertebral column in order to do the analyses. Specimens (726 individuals, 363 individuals for each species respectively) were examined shortly after landing while still fresh. Fishes of C. zillii ranging in total length (TL) from 50 to 130 mm and samples of O. aureus with TL range 100 to 120 mm were collected from the Shatt al-Arab River, Basrah, Iraq in the period December 2015 to January 2016. The method of James (2008) in preparing the vertebral column was followed in the present study. In this method, boiled water was used to remove the flesh off the bone, and running water was used to brush the bones after boiling. The vertebrae were measured using a digital 1/100 caliper (Ted Pella, Inc., Redding, USA). The dry vertebrae were stored in the ichthyological collection of the Marine Science Centre, University of Basrah, Iraq.
Two measurements of the vertebral centrum were chosen (Figure 1). The first is vertebral length (VL), the distance along the left mid-ventral line, and the second is vertebral height (VH), the maximum vertical distance of the anterior side of the vertebra.
|
Figure 1 Vertebral column of Coptodon zillii showing different regions |
.png)
To assist future comparisons with other samples, each vertebral measurement was converted into a vertebral index Vi (Ramzu and Meunier, 1999):
Vi = P/SL (1)
where P is the vertebral parameter (VL and VH) and SL the standard length. Profiles of the vertebral column were drawn by plotting VL and against the ordinal number of the vertebrae for the species. The thoracic vertebrae represent those vertebrae that having separated haemal arches. The caudal region was denoted as the region with vertebrae having their haemal arches fused. ANOVA test was used to decide whether the measurements of vertebrae found in the different regions of the vertebral column of C. zillii and O. aureus were significantly different from each other.
2 Results
The study of the vertebral measurements has revealed the presence of 5 regions (Post-cranial region, middle region, anterior caudal region, posterior caudal region, and ural region) in C. zillii and O. aureus (Figure 1; Figure 2; Figure 3; Figure 4).
|
Figure 2 Vertebral column of Oreochromis aureus showing different regions |
.png)
|
Figure 3 Vertebral profiles of Coptodon zillii. Vertebral length, dark line; vertebral height, gray line |
.png)
|
Figure 4 Vertebral profiles of Oreochromis aureus. Vertebral length, dark line; vertebral height, gray line |
.png)
2.1 Vertebral column regionalization
2.1.1 Post-cranial region
In the two cichlids species studied, the anteriormost four vertebrae (V1–V5) appear different from the remaining precaudal vertebrae due to their position immediately behind the skull. The centra of these vertebrae are shortened anteroposteriorly and dorsoventrally in relation to the centra of the other abdominal vertebrae. The centra form sites for articulation for neural arches and parapophyses. The neural arch of the 1st vertebra in C. zillii is longer that in the remaining four post-cranial vertebrae. In O. aureus, the neural arches of all four post-cranial vertebrae were similar in length.
The VL and VH parameters of the vertebrae in this region showed a maximum and minimum values at V5 for both C. zillii and O. aureus (Figure3; Figure 4; Table 1; Table 2).
|
Table 1 Mean values (mm) of length (VL) and height (VH) for the successive vertebrae of the vertebral column of Coptodon zillii (ONV, ordinal number of vertebrae; SD = standard deviation)
|
.png)
|
Table 2 Mean values (mm) of length (VL) and height (VH) for the successive vertebrae of the vertebral column of Oreochromis aureus (ONV, ordinal number of vertebrae; SD=standard deviation) |
.png)
In both C. zillii and O. aureus, the length and height of the vertebrae (VL and VH) of the post-cranial regions have shown an increase trend in their values.
2.1.2 Middle region
This region is composed of 10 vertebrae (V6-V15) for both C. zillii and O. aureus (Figure 1; Figure 2; Figure 3; Figure 4). In this region the profiles of VL was at its minimum value at V6 for both C. zillii and O. aureus. The maximum value of this parameter was at V15 in the case of C. zillii and V17 in the case of O. aureus. Similar trend of variation is observed in the profile of the VH parameters for the two species examined.
Both VL and VH have shown several types of trends in the 2 species studied, which showed sharp and slight increase or decrease in the values of these two parameters. In C. zillii, the values fluctuated between the increase and decrease, but in O. aureus, the values showed an increasing trend.
2.1.3 Anterior caudal region
There are 4 vertebrae in this region (V16-V19) in both C. zillii and O. aureus. In the profile of VL for both species examined, the minimum value at V16, while the maximum value was observed at V19 and V18 for C. zillii and O. aureus respectively.
The minimum and the maximum values as shown in the VH profile for both species were at V16 and V19 respectively.
In both species studied, the main trend of variation in the values of the two parameters VL and VH was the progressive decrease.
2.1.4 Posterior caudal region
There are 4 vertebrae in this region (V20-V23) in both C. zillii and O. aureus. In the profiles of VL and VH for both species examined, the minimum value at V20, while the maximum value was observed at V23 for C. zillii and O. aureus.
In both species studied, the main trend of variation in the values of the two parameters VL and VH was the progressive decrease.
2.1.5 Ural region
The number of vertebrae in this region was 4 (V24-27) in case of C. zillii and 5 (V24-V28) in case of O. aureus. In the profiles of VL and VH for both species examined, the minimum value at V24, while the maximum value was observed at V27 for C. zillii and V28 for O. aureus.
In both species studied, the main trend of variation in the values of the two parameters VL and VH was the sharp decrease.
3 Discussion
In the present study osteological traits are assessed and described to add more characters to those previously used to identify the two cichlid species C. zillii and O. aureus (Pouyaud and Agnèse, 1995; Dunz and Schliewen, 2013). Osteological characters are continued proving to be appropriate for fish systematics (Day, 2002; Tyler et al., 2003). The osteological examinations mentioned here showed the usefulness of the osteological features found in C. zillii and O. aureus. It is likely to recognize two groups of osteological characters: (1) exclusive characters that clearly describe a species; and (2) characters that are allotted by both species.
The analysis of the variation of the two vertebral measurements (VL and VH) of the two cichlid species studied has showed that the structure of their vertebral column is more complex than a simple division into two areas, precaudal and caudal (Table 3). This biometric study suggests the division of the vertebral column into five regions these are: (1) postcranial region, (2) middle region, (3) anterior caudal region, (4) posterior caudal region and (5) ural region. The grouping according to the number of regions of the vertebral column could be an overlapped characters between the two species. Further studies on the sections of the vertebral column in the members of the two species are prerequisite to reveal whether such grouping of vertebrae is among the characteristic features of the species of these genera.
.png) Table 3 Summary of the variation in the values of vertebral length (VL) and vertebral height (VH) in the 5 regions of the vertebral column of Coptodon zillii and Oreochromis aureus |
In both species examined, the post-cranial region is distinguished in having an increase in the two vertebral parameters chosen in this work, while the ural region was categorized by a distinct decrease in the values of the vertebral parameters. In the remaining regions located between the 1st and the last regions are characterised in having different kinds fluctuations in the values of VL and VH for C. zillii, but a study increase in O. aureus.
This first postcranial vertebra is aimed to articulate with the posterior region of the skull, forming, with the next vertebra, a link between the two main elements of the axial skeleton (Videler, 1993). In C. zillii and O. aureus, the 6–15 vertebrae posterior to the 5 postcranial vertebrae could be considered transitional vertebrae because they show a dramatic fluctuation in the values of VL and VH in C. zillii and significant increase in the case of O. aureus (Ramzu and Meunier, 1999). The transitional vertebrae both species are the same. Such similarity might indicate a similarity in the general structure of the vertebral column that adapt to feeding habits (Oso et al., 2006) or reproductive-tactic-specific variation (Bruton and Gophen, 1992; Ota and Kohda, 2006; Fitzpatrick et al., 2007) used by those different cichlid species.
The middle region comprise the boundary between the precaudal and caudal regions that corresponds to the haemal arch closing. It is therefore comprised of truncal vertebrae and forms a morphological component. In this region and in C. zillii, a fluctuation in the values of VL and VH was observed, but in the case of O. aureus, a steady increase was noticed until a maximum value before decreasing gradually. The vertebrae 24–27 and 24–28 mark the start of the ural region in C. zillii and O. aureus respectively. They belong to the tail and they characterised by a decrease in the two vertebral parameters examined. The ural vertebra is distinctive in having the haemal arches and spines have different thickness, but it has hypural plates that support the lepidotrichia of the caudal fin. In the two cichlid species studied, the hypural bones appeared united in two hypural plates, dorsal and ventral. These plates appeared to be transparent and not fully ossified.
The maximum length of the vertebra VL has been observed at V15 in both C. zillii and O. aureus, which may be due to the structural reaction of these vertebrae to the local presence of maximal mechanical restraints. This characteristic may provide an evidence for the similarity in swimming function that the two cichlid species are use in their daily life (Holden, 1992).
In C. zillii, the minimum value of the mean vertebral length is positioned at V25, while it is at V27 in O. aureus. Such differences may considered a good taxonomic criterion to set a part the two species studied.
The specific parametrical variation of the vertebrae in the ural region might express the major role played by the caudal vertebrae in the motor process of swimming. The caudal skeleton responds to the alternate contractions of the intrinsic muscles on the lateral sides of this region; thus, a torsion of the caudal peduncle is created, when the muscles slightly increase or decrease the surface area of the caudal fin at different phases of one beat (Bainbridge, 1963), thereby creating a support on water.
The position of the 1st caudal vertebra is at V15 and V17 for C. zillii and O. aureus respectively, which is considered good taxonomic criterion to separate the two species of cichlid studied.
The morphometric analysis of the vertebral column has revealed no significant difference in the variation of the vertebral length and height studied taken on each vertebra of C. zillii and O. aureus. Therefore, the specification of one vertebra along the vertebral column would be adequate if it was based on only one of these two parameters (Desse et al., 1989). This result backs that of Kacem et al. (1998) on the morphology of the skeleton of Salmo salar.
The sections in the vertebral column of the two cichlid species in question could be developed through the difference in length of vertebrae in different regions of the vertebral column, which in turn is due to different mechanisms that regulate the growth of the vertebrae in each region (Fjelldal et al., 2005).
The morphometric characters such as body proportions and meristic counts that usually used in the identification and separating fish species might in several occasions show an overlap especially in the case of the closely related species. Such overlap might hinders the differences between those species. With the new set of osteological characters used in the present study, the feasibility to set apart the species is high. Therefore, this group of characters need to obtain for any fish species that need to be compared.
The two cichlids species studied, C. zillii and O. aureus are recognized as nests diggers, and the closely related species Sarotherodon galilaeus is identified as cleaning an area for nest by removing of large items, but not by digging. It will of interest if this study is applied for S. galilaeus to unveil the relationship between cleaning and diffing behaviour and the structure of the vertebral column if there are any.
Authors’ contributions
All authors have contributed equally toward the publication of this paper.
Acknowledgments
We would like to thank Marine Science Centre, University of Basrah for giving us the opportunity to use the scientific facilities available.
Bainbridge R., 1963, Caudal fin and body movement in the propulsion of some fish, Journal of Experimental Biology, 40:23–56
Barriga-sosa I.D.L.A., Badillo-Jiménez M.L., Ibáñez-Aguirre A.L., and Arredondo Figueroa J.L., 2004, Variability of tilapias introduced in Mexico: morphometric, meristic and genetic characters, Journal of Applied Ichthyology, 20: 7-14
https://doi.org/10.1111/j.1439-0426.2004.00445.x
Bemis W.E., and Forey P.L., 2001, Occipital structure and the posterior limits of the skull in actinopterygians. In: Ahlberg P, editor. Major events in vertebrate evolution, London: Taylor and Francis, pp.350–369
Bruton M.N., and Gophen M., 1992, The effect of environmental factors on the nesting and courtship behaviour of Tilapia zillii in Lake Kinneret (Israel), Hydrobiologia, 239: 171-178
https://doi.org/10.1007/BF00007674
Chakrabarty P., 2010, The transitioning state of systematic ichthyology, Copeia 3: 513–514
https://doi.org/10.1643/OT-10-087a
Costa-Pierce B.A., 2003, Rapid evolution of an established feral tilapia (Oreochromis spp.): the need to incorporate invasion science into regulatory structures. In Marine Bioinvasions: Patterns, Processes and Perspectives,Springer Netherlands, pp.71-84
Day J.J., 2002, Phylogenetic relationships of the Sparidae (Teleostei: Percoidei) and implications for convergent trophic evolution, Biological Journal of the Linnaean Society, 67: 269–301
https://doi.org/10.1111/j.1095-8312.2002.tb02088.x
Desse J., Desse-Bersrt N., and Rochteau M., 1989, Les profils rachidiens globaux. Reconstitution de lataille des poisons et appréciation du nombre minimal d’individus à partir des pieces rachidiennes, Review of Paléobiology, 8:89–94
Doherty D., and McCarthy T.K., 2004, May. Morphometric and meristic characteristics analyses of two western Irish populations of Arctic Char, Salvelinus alpinus (L.), In Biology and Environment: proceedings of the Royal Irish Academy,Royal Irish Academy, pp.75-85
https://doi.org/10.3318/BIOE.2004.104.1.75
Dunz A., 2012, Revision of the substrate brooding “Tilapia” (Tilapia Smith, 1840 and related taxa), (Teleostei: Perciformes: Cichlidae). Dissertation zur Erlangung des Doktorgrades, Maximilians-Universität, München, Germany
Dunz A.R., and Schliewen U.K., 2010a, Description of a new species of Tilapia Smith (Teleostei: Cichlidae) from Ghana, Zootaxa, 2548: 1–21
Dunz A.R., and Schliewen U.K., 2010b, Description of a Tilapia (Coptodon) species flock of Lake Ejagham (Cameroon), including a redescription of Tilapiadeckerti Thys van den Audenaerde, 1967, Spixiana, 33: 251–280
Dunz A.R., and Schliewen U.K., 2013, Molecular phylogeny and revised classification of the haplotilapiine cichlid fishes formerly referred to as “Tilapia”, Molecular Phylogenetics and Evolution, 68: 64-80
https://doi.org/10.1016/j.ympev.2013.03.015
Fitzpatrick J.L., Desjardins J.K., Milligan N., Montgomerie R., and Balshine S., 2007, Reproductive-tactic-specific variation in sperm swimming speeds in a shell-brooding cichlid, Biology of Reproduction, 77: 280-284
https://doi.org/10.1095/biolreprod.106.059550
Fjelldal P.G., Nordgarden U., Berg A., Grotmol S., Totland G.K., Wargelius A., and Hansen T., 2005, Vertebrae of the trunk and tail display different growth rates in response to photoperiod in Atlantic salmon, Salmo salar L., post-smolts, Aquaculture, 250: 516–524
https://doi.org/10.1016/j.aquaculture.2005.04.056
Ford E., 1937, Vertebral variation in teleostean fishes, Journal of the Marine Biological Association of the United Kingdom, 22:1–60
https://doi.org/10.1017/S0025315400011863
Grande L., and Bemis W.E., 1998, A comprehensive phylogenetic study of amiid fishes (Amiidae) based on comparative skeletal anatomy. An empirical search for interconnected patterns of natural history, Journal of Vertebrate Palaeontology, 18:1–696
https://doi.org/10.1080/02724634.1998.10011114
Holden M.N., 1992, A life-history approach to the early ontogeny of the Mozambique tilapia Oreochromis mossambicus (Pisces, Cichlidae), African Zoology, 27: 173-191
James P.S.B.R., 2008, Osteo-taxonomic distinction of fishes of the family Leiognathidae, Indian Journal of Fisheries, 55:305–310
Jawad L.A., and Al-Hassani L., 2014a, Morphological aspects of the vertebral column of the Indian mackerel Rastrelliger kanagurta (Osteichthyes: Scomberidae) collected from the Sea of Oman, Thalassia Salentina, 36: 3-12
Jawad L.A., and Al-Hassani L., 2014b, Morphological Study of the Vertebral Column of the Ponyfish Leiognathus equulus (Family: Leiognathidae) Collected from the Sea of Oman, International Journal of Marine Science, 4: 1-6
Jawad L.A., 2015, Study of the vertebral column of the onion trevally, Carangoides caeruleopinnatus (Teleostei: Carangidae) collected from the Sea of Oman, Italian Journal of Zoology, I: 1–7
https://doi.org/10.1080/11250003.2014.1000983
Jawad L.A., Al-Hassani L., and Al-Kindi A., 2014, Vertebral column morphology of the Bengal snapper, Lutjanus bengalensis (Bloch, 1790), from the Oman Sea, Cahiers de Biologie Marine, 55: 491-497
Kacem A., Meunier F.J., and Bagliniere J.L., 1998, A quantitative study of morphological changes in the skeleton of Salmo salar during its anadromous migration, Journal of Fish Biology, 53:1096–1109
https://doi.org/10.1111/j.1095-8649.1998.tb00466.x
Kocher T.D., 2004, Adaptive evolution and explosive speciation: the cichlid fish model, Nature Reviews Genetics, 5: 288–298
https://doi.org/10.1038/nrg1316
Kubo Y., and Asano H., 1987, Growth type of vertebral centra and the hard tissue observed by microradiography of the rainbow trout,Nippon Suisan Gakkaishi, 53:1367–1372
https://doi.org/10.2331/suisan.56.1021
Kubo Y., and Asano H., 1990, Relative growth pattern and hard tissue of vertebral centra by microradiography of Bluefin tuna, bigeye tuna and skipjack, Nippon Suisan Gakkaishi, 56:1021–1027
Laerm J., 1976, The development, function, and design of amphicoelous vertebrae in teleost fishes, Zoological Journal of the Linnean Society, 58:237–254
Lindsey C.C., 1978, Form, function and locomotory habits in fish. In: Hoar W S, Randall DJ, editors, Fish physiology, New York: Academic Press, pp.1–100
https://doi.org/10.1016/S1546-5098(08)60163-6
McAndrew B.J., 2000, Evolution, phylogenetic relationships and biogeography, Fish and Fisheries Series, 25: 1-32
https://doi.org/10.1007/978-94-011-4008-9_1
Oso J.A., Ayodele I.A., and Fagbuaro O., 2006, Food and feeding habits of Oreochromis niloticus (L.) and Sarotherodon galilaeus (L.) in a tropical reservoir, World Journal of Zoology, 1: 118-121
Ota K, and Kohda M.,2006, Description of alternative male reproductive tactics in a shell-brooding cichlid, Telmatochromis vittatus, in Lake Tanganyika, J Ethol., 24:9–15
https://doi.org/10.1007/s10164-005-0154-6
Pietsch T.W., 1978, Evolutionary Relationships of the Sea Moths (Teleostei: Pegasidae) with a Classification of Gasterosteiform Families, Copeia, 3:517–529
https://doi.org/10.2307/1443620
Pouyaud L., and Agnèse J.F., 1995, Phylogenetic relationships between 21 species of three tilapiine genera Tilapia, Sarotherodon and Oreochromis using allozyme data, Journal of Fish Biology, 47: 26-38
https://doi.org/10.1111/j.1095-8649.1995.tb01870.x
Ramzu M., and Meunier F.J., 1999, Descripteurs morphologiques de la zonation de la colonne vertébrale chez la truite are-en-ciel Oncorhynchus mykiss (Walbaum, 1792) (Teleostei, Salmonidae), Annals des Sciences Naturalles, 3:87–97
https://doi.org/10.1016/S0003-4339(00)86973-7
Ramzu M., Meunier F.J., and Schovaer D., 1992, Morphological and histological characteristics of the vertebral axis zonation in the trout (Salmo trutta L.) (Teleostei, Salmonidae): possible functional implications, Oceanis, 18:85–91
Salzburger W., and Meyer A., 2004, The species flocks of East African cichlid fishes: recent advances in molecular phylogenetics and population genetics, Naturwissenschaften, 91: 277–290
https://doi.org/10.1007/s00114-004-0528-6
Teugels G.G., and Thys van den Audenaerde D.F.E., 2003, Cichlidae. In: Paugy, D., Teugels, G.G, Leveque, C. (Eds.), The fresh and brackish water fishes of West Africa Volume 2. Coll. faune et flore tropicales 40. Institut de recherché de développement, Paris, France, Muséum national d'histoire naturelle, Paris, France and Musée royal de l'Afrique Central, Tervuren, Belgium, pp.521–600
Tyler J.C., O’Tool B., and Winterbottom R., 2003, Phylogeny of the genera and families of zeiform fishes, with comments on their relationships with tetraodontiforms and caproids, Smithsonian Contributionto Zoology, 618: 1–110
https://doi.org/10.5479/si.00810282.618
Videler J.J., 1993, Fish swimming. London: Chapman and Hall,pp.260
https://doi.org/10.1007/978-94-011-1580-3
Volff J.N., 2005, Genome evolution and biodiversity in teleost fish, Heredity, 94: 280-294
https://doi.org/10.1038/sj.hdy.6800635
Ward A.B., and Brainerd E.L., 2007, Evolution of axial patterning in elongate fishes, Biological Journal of the Linnean Society, 90: 97–116
https://doi.org/10.1111/j.1095-8312.2007.00714.x
Weihs D., 1989, Design features and mechanics of axial locomotion in fish, American Zoologist, 24:107–120
https://doi.org/10.1093/icb/29.1.151
. PDF(418KB)
. FPDF(win)
. HTML
. Online fPDF
Associated material
. Readers' comments
Other articles by authors
. Laith A. Jawad
. Fawziah Sh. Habbeb
. Mustafa A. Al-Mukhtar
Related articles
. Vertebral column
. Vertebrae
. Ural vertebrae
. Morphology
Tools
. Email to a friend
. Post a comment