~. Nigerian Veterinary JournalVol 35 (1) 942 - 947

ARTICLE

The Vertebral Formula of the AfricanSideneck Turtle (Pe/usios castaneus)

OLUKOLE, s.G.*\ OYEYEMI, M.0.2 AND OKE, B.O.'

'Depanment of Veterinary Anatomy, Faculty of Veterinary Medicine, University of Ibadan, Ibadan, Nigeria, 20epartment of VeterinarySurgery and Reproduction, Faculty of Veterinary Medicine, University of Ibadan, Ibadan, Nigeria. 'Corresponding Author: E-mail:deborolukole@yahoo.com,sg.olukole@mail.uLedu.ng, Phone number: +2348033574752

SUMMARYAn osteological analysis of the vertebralcolumn of the African sideneck turtle(Pelusios castaneus), was carried out withthe view of deriving its vertebral formulawhich could be useful in the comparativesystematic anatomy of sea and freshwaterturtles as well as in paleontological andarchaeological investigations. A total ofsixty five adult African sideneck turtlescomprising twenty five females and fortymales picked up at different times invarious river banks in Ibadan, Nigeria,were used for the study. The average bodyweight of the turtles used for the study was0.82 ±0.03kg. The curved carapace andplastron lengths of the turtles were 26-4±1.87cm and 19.3 ± 1.13cm, respectively.The turtle has eight cervical vertebrae ofwhich the first seven (craniocaudally) weremobile and the last fused with the ventralsurface of the carapace and articulatedcaudally with the first thoracic vertebra.The thoracic vertebrae were seven innumber, the last thoracic vertebraarticulated with the first sacral vertebra.Three sacral vertebrae were identified inthe animals while 15caudal vertebrae wereconstantly encountered in all the turtles.The vertebral column of the African side

neck turtle consists of 33 vertebrae andits formula can be expressed asC8T7S3Cd15. This formula, the first ofits kind in literature is therefore namedas the African sideneck turtle vertebralformula (of Olukole) and thereforeserves as baseline information on thevertebral column of the turtle.KEY WORD: Anatomy; Carapace;Freshwater Turtle; Skeletal System;Vertebral Column.

INTRODUCTIONAfrican sideneck turtles are relatively smallto medium sized freshwater turtles widelydistributed in Africa (Anderson, 1995;Broadley and Boycott, 2009). The Africansideneck turtle (Pelusios castaneus) is afreshwater turtle of the familyPelomedusidae, widely distributed in WestAfrica, occurring from Guinea and Senegalto northwestern Angola (Kirkpatrick,1995).Turtles of the genus Pelusios areoccasionally eaten by indigenous people,but their foul-smelling musk secretionsprobably serve to discourage more regularconsumption. They are also low in demandfor pet trade (Boycott and Bourquin,

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2000). In South-western Nigeria, the P.castaneus among other freshwater turtlesare also high in demand for severaltradomedical and fetish purposes.The skeletal system of turtles can bedivided into three: the skull, axial andappendicular skeletons. The axial skeletonof turtles is composed the carapace,vertebrae, ribs and the derivatives of theribs while the appendicular skeletonincludes the forelimbs (flippers in seaturtles), hind limbs and their supportingstructures (Wyneken, 2001). The vertebralcolumn of mammals had been described toconsist of morphologically differentiatedgroups of vertebrae: cervical, thoracic,lumbar, sacral, and caudal (Burke et aI.,1995; Levine et aI., 2007) while that ofturtles consists of the cervical, thoracic,sacral and caudal vertebrae (Sanchez-Villagra et aI., 2007). The entire thoracicand sacral vertebrae are usually fused to thecarapace of turtles while only the lastcervical vertebra fuses with the carapace(Wyneken, 2001).

Studies on the conservation, nutrition andhistory of migration of the genus Pelusioshad been documented (Broadley andBoycott, 2009). Recent research report onthe genus Pelusios had been on bloodparameters of the African sideneck turtle(Omonona et aI., 2011). Studies on thevertebral formula of mammals had beenwell reported by a number of authors(Aimi, 1994; Burke et aI., 1995;Hilderbrand and Goslow, 2001; Narita andKuratani, 2005). The skeletal system of seaturtles had been documented by Wyneken(2001). There is the paucity of researchreports on the basic anatomy of the skeletalsystem of the P. castaneus.

The search web literature showed thatthere is no information on the vertebralcolumn of the P. castaneus. There istherefore the need to investigate the basicanatomy of the vertebral column of the P.

castaneus. This study was thereforedesigned to investigate into the numberand structural arrangement of thevertebrae of the P. castaneus with the viewof deriving the vertebral formula of theturtle.

MATERIALS and METHODSA total of thirty adult P. castaneuscomprising fifteen females and fifteenmales picked up at different times invarious river banks in Ibadan, Nigeria,were used for the study. The animals werekept in artificial ponds and were stabilizedfor 72 hours prior to the investigationscarried out. They were fed with commercialfish pellets ad libitum. Standard bodyparameters were all determined using aDraper@ 115 mm vernier caliper andmetric tape. The body weight of the animalswas taken with the aid of a Microvar@weighing balance. The turtles wereanaesthetized using ketamine Hel at25mgjkg body weight intramuscularly atthe medial aspects of the thigh muscle andthen sacrificed by cervical decapitation.The preparation of skeletons of the animalswas obtained through hot watermaceration (Sommer and Anderson, 1974).The inner parts of the carapace and boneswere then washed with sodiumhypochloride and detergent to expose thevertebral column. The arrangement andnumber of the bones of the vertebralcolumn were investigated.

RESULTSThe average body weight of the turtles usedfor the study was 0.82 kg (0.580 -1.20 kg).The mean curved carapace and plastronlengths of the turtles were 26-4 ± 1.87Cm(20.3- 28.5 em) and 19.3 ± 1.13cm (17.8-21.2 em), respectively. There were 8cervical vertebrae of which the first seven(craniocaudally) were mobile (figure 1) andthe last fused with the inner surface of thecarapace and articulated caudally with thefirst thoracic vertebra (figure 2).

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Figure 1. Dorsolateral view of the cervical vertebrae ofthe African sideneck turtle (Pelusios castaneus) showingthe first seven (mobile) vertebrae. Cl-CT First to seventhcervical vertebrae.

In each of the turtles observed, there wasthe fusion of the dorsal vertebrae (the lastcervical, the entire thoracic and the sacralvertebrae) with the ventral surface of thecarapace. The ribs with the dermal bonesform the pleurals while the neural boneslied ventral to the thoracic vertebrae. The

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Figure 2:The ventral view of the carapace of the Africansideneck turtle (Pelusios castaneus) showing the dorsalvertebrae and their relations. C8: Eighth cervical vertebra(fused to the carapace); Tito T7: First to seventh thoracicvertebra; 81 to 83: First to third sacral vertebra; PLB:Pelvic bone (fused to the carapace and relates mediallywith the lateral processes of the sacral vertebrae).

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Figure 3. The dorsal view of the caudal vertebrae of theAfrican sideneck turtle (Pelusios castaneus). Cdi to Cdrg:First to fifteenth caudal vertebra.

thoracic vertebrae were 7 in number andthe last thoracic vertebra articulated withthe first sacral vertebra (figure 2). Thethoracic vertebrae decrease in lengthdistally with their width decreasingcranially. Each of the thoracic vertebrae iscomposed of a separate dorsal arch andventral vertebral body. The ventral bodyarticulates bilaterally with a pair of ribs. Inall the turtles studied, the rib heads werealigned with the junctions of

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Figure 4. The ventral view of the carapace of theAfrican sideneck turtle (Pelusios castaneus)showing the anatomical relations of thecomponents of the vertebral column in the animal.Ci and C8: First and eighth cervical vertebraerespectively; T1 and TS: First and fifth thoracicvertebrae respectively; SV: Sacral vertebrae; CdV:Caudal veltebrae.

adjacent vertebral bodies.There were 3 sacral vertebrae which jointlyform attachment for the hip bones laterallyon both sides of the median plane of theanimals (figure 2). In all the turtles studied,the lateral processes of the sacral vertebraewere not fused with the carapace. Theselateral processes were observed to formarticulations with the ilium. A veryprominent feature on each of the sacralvertebrae was the dorsal sacral foramenthat accommodates vessels supplying thesacrum and the articulating hip joint. Atotal of 15 caudal vertebrae wereconsistently observed in all the animalsregardless of size and sex (figure 3).However, the caudal vertebrae of thefemale were shorter than those of the malesand decreased in size more distally thanthose of the males. In addition, the caudalvertebrae of the males had more extensive

dorsal and lateral processes than those ofthe females. Hence, the vertebral column ofthe African sideneck turtle consists of 33vertebrae and its formula can be expressedas C8T7S3Cd15 (figure 4). This formula,being the first of its kind in literature istherefore named as the P. castaneusvertebral formula (ofOlukole).

DISCUSSIONThe knowledge of the arrangement andnumber of the bones of the vertebralcolumn of the P. castaneus is important inthe understanding of the normal gait of theanimal and the types of motion permittedalong the spine. Vertebral columnbiomechanics had been used to explainnormal gait and pathologic stress on thespine of domestic animals (Levine et al.,2007). The number and arrangement of thecervical vertebrate of the P. castaneus aresimilar to that reported in the sea andfreshwater turtles and the fusion observedbetween the last cervical vertebra and thecarapace is typical of all turtles (Walker,1973; Wyneken, 2001). This fusion could berelated to the stability of the neck and spinethereby preventing the over-extension ofthe neck during motion. The vertebralarches of the successive cervical vertebraehave articulating processes with slidingjoints that allow limited dorsal-ventralbending of the neck, but little twisting(Wyneken, 2001). However, the number ofcervical vertebrae being constantly eight inturtles differentiates them from mammalswhere the number is constantly seven andhas been almost fixed by certainmammalian specific developmentalconstraints (Zangerl et al., 1988). Thenumber of mammalian cervical vertebraehas been reported to be constant at seven,irrespective of the neck length of differentspecies (Narita and Kuratani, 2005).

The arrangement and articulationsbetween the ribs and thoracic vertebral inthe African sideneck turtle is similar to

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those of the Green turtle described byWyneken (2001). Nevertheless, thenumber of thoracic vertebrae in the Greenturtle and many sea turtles had beenreported as ten unlike those of the P.castaneus being seven. This finding is notin conformity with the report of Wyneken,2001 on the possession of ten thoracicvertebrae by sea turtles. The P. castaneus,like all turtles lack the lumbar vertebraefound in mammals (Wyneken, 2001;Sanchez-Villagra et al., 2007, 2009). Thepresence of the lumbar vertebrae inmammals may be responsible for the abilityof mammals to twist their (trunk) unliketurtles whose twisting of the entire body ismainly by the neck. The number andarrangement of the sacral bones of the P.castaneus are similar to those reported inother turtles. Two to three sacral vertebraehad been reported by Wyneken (2001) inmost sea turtles. Also, the number andmorphological dispositions of the caudalvertebrae in the turtles studied are inconformity to previous report by Wyneken(2001) that turtles have 12 or more caudalvertebrae and that there exist a sexualdimorphism in the morphology of thecaudal vertebrae in turtles. Male turtlesusually have longer tail than their femalecounterparts, nevertheless, the study hadshown that this longer length does notmean that the caudal vertebrae are more inthe male than in the female; rather, they arelonger.The P. castaneus vertebral formula (ofOlukole) derived by this study providesnecessary information which could be ofassistance in forensic anthropologicalstudies as well as serving as a baseline dataneeded in the comparative osteology of seaand freshwater turtles; especially those ofthe family Pelomedusidae.

ACKNOWLEDGEMENTSThis work was supported by University ofIbadan Senate Research Grants(SRG/FVM/2010/4A and

SRG/FVM/2010/1B). The authors wouldlike to appreciate the efforts of OladapoAgbato, Beatrice Okusanya and TomiwaKekere in the preparation of the turtleshells used for this work.

REFERENCESAIMI, M. (1994). Numerical variation of

vertebrae in Japanese macaques,Macaca fuscata. AnthropologicalScience 102 (SUppl):1-10.

ANDERSON, N.B. (1995). Life Historynotes: Pelusios sinuatus:reproduction. African Herp News23:49·

BOYCOTT, R.C. and BOURQUIN, O.(2000). The Southern AfricanTortoise Book: A guide to SouthernAfrican Tortoise, Terrapins andTurtles. 0 Bourquin, Hilton,KwaZulu-Natal, South Africa, 228.

BROADLEY, D.G. and BOYCOTT, R.C.(2009). Pelusios sinuatus (Smith1838) -Serrated Hinged Terrapin.Conservation Biology of FreshwaterTurtles and Tortoises, ChelonianResearch Monographs 5: 036.1-036.5·

BURKE, A.C., NELSON, C.E., MORGAN,B.A. and TABIN, C. (1995). Hoxgenes and the evolution ofvertebrate axial morphology.Chelonian Development121:333-346.

HILDEBRAND, M. and GOSLOW, J.G.E.(2001). Analysis of vertebratestructure. New York: John Wileyand Sons, Inc.

KIRKPATRICK, D. T. (1995). "An Essay onTaxonomy and the Genus Pelusios."Available at:http.Z/www.unc.edu/ =dtkirkpa/stuff/pel.html. Accessed: 22February 2013. Originallypublished in Reptile & AmphibianMagazine, March/April, pp. 32-40.

LEVINE, J.M., LEVINE, G.J., HOFFMAN,A.G., MEZ, J. and BRATTON, G.R.

946

Olukole et al ISSN 0331 • 3026

(2007). Comparative Anatomy ofthe Horse,Ox, and Dog:TheVertebral Column andPeripheral Nerves. CompediumEquine, September/October, 279-292.

NARITA, Y. and KURATANI, S. (2005).Evolution of the VertebralFormulae in Mammals: Aperspective on developmentalconstraints. Journal ofExperimental Zoology,304B:91-106.

OMONONA A.O., OLUKOLE, S.G. andKUSHE, F.A. (2011). Haematologyand serum biochemical parametersin free ranging African sideneckturtle (Pelusios sinuatus) in Ibadan,Nigeria. Acta Herpetologica 6 (2), p.267-274.

SANCHEZ-VILLAGRA, M.R.,MITGUTSCH, C., NAGASHIMA,H. and KURATANI, S. (2007).Autopodial development in the seaturtles Chelonia mydas and Carettacaretta. Zoological Science,24:257-263.

SANCHEZ-VILLAGRA, M.R, MULLER,H., SHEIL, C.A., SCHEYER, T.M.,NAGASHIMA, H. and KURATANI,S. (2009). Skeletal Development inthe Chinese Soft-Shelled TurtlePelodiscus sinensis (Testudines:Trionychidae). Journal ofMorphology, 270:1381-1399.

SOMMER, H. G. and ANDERSON, S.(1974). "Cleaning skeletons withdermestid beetles - tworefinements in the method",Curator. 17, (4), 290-298.

WALKER, W.F.,JR (1973). The locomotorapparatus of testudines, in Biologyof the Reptilia, Gans, C. andParsons, T.S., Eds., AcademicPress, New York.

WYNEKEN,J. (2001). The Anatomy of SeaTurtles. U.S. Department ofCommerce NOAA Technical

Memorandum NMFS-SEFSC 470,1-172.

ZANGERL, R, HENDRICKSON, L.P. andHENDRICKSON, J.R. (1988). Aredescription of the Australianflatback sea turtles, Natatordepressus. Bishop Museum Bull.Zool., 1,1-69, 1988.

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