Double-faced monster in the bottlenosed dolphin (Tursiops truncatus) found in the Mediterranean sea

doi: 10.1136/vr.154.10.306

2004 154: 306-308

Veterinary Record

W. Dabin, C. Cesarini, I. Clemenceau, et al.

Mediterranean sea

) found in the

Tursiops truncatus

dolphin (

Double-faced monster in the bottlenosed

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andMadbouly 1981, Buttiker and Zumpt 1982) concern-ing myiasis did not record W nuba larvae as causative agents.

Although this study recorded few cases of traumatic myiasis, itidentifiedthe important causativeflyspeciesand indicated their geographical and seasonal distribution in

Saudi Arabia.Itseems certainthatmore screwwormmyiasis occurred butwas not reported, owingtothe failure of vet-erinarians tosubmitsamples andthe lackofawareness onthe partof animalownersof the needtobringtheir livestockfor

treatment. Further intensivestudiesareneededtoprovide

moredetailed dataonthegeographical distribution and the

pest statusof the Old WorldscrewwormflyinSaudi Arabia. Successful control should be basedontheidentification of infestedareasandcomplete involvement ofownersand vet-erinarians in a wellorganised campaign of prevention and

treatment.

ACKNOWLEDGEMENTS

The authors thank Dr M. Hall of the Natural History

Museum,London, for his help intheidentification ofsome

fly species and for revising the manuscript, and Dr P. Spradbery ofCSIRO,Australia, for hisinterest.

References

AL-IZZI,M. A.J.,AL-TAWEEL,A. A.&JASSIUM,F. A.(1999)Epidemiology

and rearing of Old World screwworm, Chrysomya bezziana Villeneuve (Diptera; Calliphoridae) in Iraq. Iraq Journal of Agriculture 4, 153-160

ANSARI,M. A.&OERTLEY,R. E.(1982) Nasal myiasis duetoBezzi'sblowfly

(screwworm):casereport.Saudi MedicalJournal3,275-278

BANAJA,A. A. &MADBOULY,M. H.(1981)Fieldandlaboratoryobservations

onthreeDipterous larvae causing myiasis in livestock in thewesternregion

of Saudi Arabia. BulletinoftheFacultyof Science, KingAbdulazizUniversity,

Jeddah 5,77-80

BUTTIKER,W. &ZUMPT,F.(1982) Myiasis in domestic animals.Faunaof

Saudi Arabia 4,520-524

EL-AZAZY,0.M.E.(I1992)Observationsonthe New Worldscrewwormflyin

Libyaand risk of itsentranceintoEgypt.VeterinaryParasitology42, 303-310

EL-AZAZY,0.M. E.(1993)Old Worldscrewwormfly (Chrysomya bezziana)

intheGulf. Veterinary Record 132,256

EL-KHOLANY,K. A. &OMER, S.F.A.(1999)Someparasitologicalstudieson Chrysomyabezzianaas amaincauseofsheep myiasisinSaudi Arabia.Journal

ofthe EgyptVeterinaryMedical Association 59,1695-1708

KERSTEN,R.C., SHOUKREY,N. M. &TABBAYA,K. F.(1986)Orbital

myia-sis.Ophthalmology93,1228-1232

LINDQUIST,D.A.,ABUSOWA,M. &HALL,M.J.R.(1992)TheNewWorld

screwwormflyinLibya:areviewof its introduction and eradication. Medical andVeterinaryEntomology6,2-8

NAVIDPOUR, S., HOGHOOGHI-RAD, N.,GOODARZI,H. &POOLADGAR,

A. R.(1996)Outbreak ofChrysomyabezziana in Khoozestanprovince,Iran.

VeterinaryRecord 139,217

RAMADAN,R.0.&EL-BIHARI,S.(1980)Dermalmyiasisinfarm animals

in Hofufareawithspecialreferencetotheclinical pictureandsurgical

management.Proceedingsofthe SaudiBiological Society4,305-315

SPRADBERY, J.P.(1991)AManual for theDiagnosisof the ScrewwormFly. Canberra,CSIRO

SPRADBERY, J.P.(1992)Studiesontheprepupalandpuparialstagesof the Old World screwworm fly, Chrysomya bezziana Villeneuve (Diptera:

Calliphoridae).CSIRO Division ofEntomologyTechnicalReport, Number

49.Canberra,CSIRO.pp 1-24

SPRADBERY, J. P., KHANFAR,K. A. &HARPHAM,D.(1992) Myiasisinthe Sultanate ofOman.VeterinaryRecord 131,76-77

TERNOVOY,V.I.(1978)Astudyof thediapauseinWohlfahrtia magnifica

(Diptera, Sarcophagidae). Entomological Review (Entomologicheskoye

Obozreniye)57,328-332

VERVES,Y. G. (1986) Family Sarcophagidae. In CatalogueofPalaearctic

Diptera.Calliphoridae-Sarcophagidae.Vol12.EdsA.Soos,L.Popp.Budapest,

AkademiaiKiado. pp58-193

Double-faced

monster

in

the bottlenosed

dolphin

(Tursiops

truncatus)

found

in

the

Mediterranean

sea

W.

DABIN,

C.

CESARINI, 1. CLEMENCEAU,

F.

DHERMAIN,

T.

JAUNIAUX,

0.

VAN

CANNEYT,

V.

RIDOUX

TERATOLOGYisthestudyof abnormal

development.

In par-ticular,itisthe

study

of thecauses,mechanisms and

manifes-tations of abnormal

development,

whether

genetically,

gestationally,

or

postnatally induced,

andis

expressed

as

mor-tality,

malformation,

growth

retardationorfunctional

aber-rations (Wilson 1986). Abnormal

development

produces

monsterswhicharedefinedas afetusor neonatewith such pronounced developmentalanomaliesastobegrotesqueand

usuallynon-viable.

Analysis

of thesecases can

provide

more

informationon

embryological

processesduetoeither

genetic

orchromosomal

factors,

and theeffect of

mutagenetic

factors

operatingafter

fertilisation,

or

infectious,

chemicalor

physi-cal factorsoperating

during

embryogenesis

andfetal

develop-ment(BriardandLe Merrer1989,

Shepard

and others

2000).

Thisknowledgeisimportantinhuman andveterinary

medi-cine(Brentand others2000),canbe relatedto

possible

envi-ronmentalcauseslikecontaminants

(Bjerkedal

1989,Inouve

1989,Yasuda 1994)andcan

provide

useful

insight

into

phylo-genetic

relationships

(Slaipka 1994).

Manytypes of

terato-logical specimens have been found among mammals

including man.

Comparatively,

such records in cetaceans

remainscarce.This shortcommunicationdescribesa caseof

a double-facedmonsterinabottlenosed

dolphin (Tursiops

truncatus)found strandedontheFrench Mediterraneancoast.

Thespecimenwascollectedon June 24, 2001,at Borgo

beach,

Corsica,inthewesternMediterraneanSea. Itwas a

partially decomposed

female bottlenosed

dolphin

calf,

119cm

in

length,

weighing

22

kg

withan80cm

lone, single

umbili-calcord still attached. Thesemeasurements werecloseto

stan-dard valuesfor newborn bottlenosed

dolphin calves,

whose

lengthsatbirthare

approximately

0-9to 1-3m

(Mead

and

Potter1990)and

suggested

thatthespecimenhad

completed

itsfetal

development

and

probably

diedat

delivery.

Thiswas

confirmed

by

examinationofthe

lungs,

whichshowedthat

the animal hadneverbreathed.The

teratological

natureofthe specimenwas

externally

revealed

by

the presenceoftwo vis-iblebeaks.

Thecarcasewas

kept

frozen for furtherexamination.The animalwas

x-rayed

andapostmortemexaminationwas

car-riedout attheUniversityofLuminy,

Marseille,

on

July

2.The

malformation

mostly

affectedtheface ofthe animalandto a

lesserextentthe braincase

(Figs

1,

2).

Theskullwas

abnor-mally

wideand hada

single occipital

hole. Therewas a

sin-gle

braincasewithtwotympanic

bullae,

buttwo

beaks,

two

blow

holes,

twoeyeslocated

laterally

andtwoothersinserted betweenthetwobeaks. Therewasa

single hyoid

apparatus, butthetonguewas

bifid,

eachpart

corresponding

to oneof

thetwobeaks.Teeth formation in the upper and lower

jaws

wasnormal for such ayoung

animal,

with

well-developed

teeth

barely erupting

from thegum.Therestof theexternal

structureslocated furtherbackward showed nodifference fromanormal

dolphin

calf in either

shape

orsize.For

exam-ple,therewere apairof

flippers,

a

normal-shaped

tail fluke

VeterinaryRecord(2004)

154,306-308

W.Dabin, 0.VanCanneyt,

Centrede Recherchesur

les MammiferesMarins,

PortdesMinimes,17000 LaRochelle,France C.Cesarini, Groupd'Etudesdes CetacesdeMediterranee,

Amococcola,20230Santa

LuciaMorioni,France I.Clemenceau,

DirectionRegionalede l'Environnement de

Corse,Chemind'Agliani, Montesoro,20600Bastia,

France

F.Dhermain,DVM,

Groupd'Etudes des CetacesdeMediterranee, 13Boulevard duRedon, 13009Marseille,France T.Jauniaux,DVM, DepartmentofPathology, FacultyofVeterinary Medicine,Universityof Liege,4000Liege, Belgium V.Ridoux, Laboratoire deBiologieet EnvironnementMarins, EA3168,Universityof LaRochelle,17042 LaRochelle,France

The

Veterinary

Record,

March6,2004

306

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FIG 1:Radiograph of the headshowingthetwo

completebeaks and the

teeth,as well asthe single,abnormallywide braincase with two

auditory bullae

(denser

areas).Bar=2cm

and dorsal fin and an umbilical cord attached to the FIG

2:

Frontal view of the head of the dolphin during abdomen.Viscera inthe thoracic and abdominal cavities dissection showing the locations of two blow holes(arrows)

werenodifferenttotheconformationobservedatthesame and twoeyes(arrowheads) stageofdevelopmentin anormaldolphincalf. Thestateof

decompositionprecludedanyfurtherinvestigation andthe

possible initialcausesof the malformation couldnotbedeter- formed

normally

with oneofeach of the

following

bones: minedfrom examination of thecarcase.

supraoccipital, exoccipital,

basioccipital

aswellas apairof Theskullwaskeptmaceratedinfreshwaterandgradually squamosalandapairof

auditory

bullae.In

between,

a transi-cleaned by handinordertopreservebonesutures(Fig 3)and tionalzonewasvisibleinwhich the

parietal

and

interparietal

toallow thedescriptionandmeasurementsof featureson cra- boneswere

only partially

duplicated.

Two

interparietals

were

nial bones(Table 1), asproposedbyRommel (1990) and

clearlyvisible

intheaxisof eachrostrumand the

parietals

were Perrin(1975)fordelphinidskulls. The skull divisionwas com- represented

by

three bones.Twoboneswerelocated

laterally

plete forward from thefrontalbones,locateddorsally,and the andseemedtobe

shaped

normally;

the

third,

probably

result-vomers, locatedventrally. The backofthe brain casewas ing fromthefusion oftwoother

parietals

(fused parietals),

was locatedbetweentheduplicateinterparietal bones.Intermsof relativedimensions, the supraoccipital andthe basioccipital

FIG 3:Dorsal view of the skullshowingthat thefacial bonesareduplicated.frnFrontal,fusedparietals,fpFused

parietals, int-parInterparietals,parParietals, socSupraoccipital.Bar=2cm

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werebroader than normal, and the outer bones of each beak (left and right premaxillary, maxillary and frontal bones of the left andright rostra, respectively) were notably more elongated thanthe corresponding inner ones (Table 1).

This short communication describes the second case of a duplicateanteriorand thefirst knowncaseofadouble-faced

monster inodontocetes. The classification of monster in this

caseis anatlodymus, that is, a duplicate face with only one atlas. The other case ofaduplicate anterior was reported by Kamiya andothers (1981) who described the first known case ofdicephalyinodontocetes. They described a malformed embryo ofastriped dolphin (Stenella coeruleoalba), found in Japanin 1981, whichwasaduplicate anteriorcharacterised by the presence oftwodistinct heads, not merely two 'faces'

as inthe present specimen (diproscopy). It had duplicate cer-vical vertebraeand four eyes (tetraophthalmy), and was clas-sifiedas aderodymusmonster.

Othercasesof monstrosityin cetaceans arescarce,but

sev-eral realdoublemonsters(two individuals moreorless com-pletelyfused) have been described previously.A case of a double monster in a bottlenosed dolphin with fusion of the thoracic and abdominal cavities was described by Droogleever Fortuyn andRomer (1920)intheNetherlands.

Kawamura (1969) describedsiamesetwinsinthe sei whale (Balaenopteraborealis). Thetwins weretwomalefetuses that measured114and137cm inlength. Thiscasewasconsidered

atypicalexample of complete fusion of thoracic and abdom-inalcavitiesfrom the throatto apointjust posteriortothe

naval,withoneumbilical cordonly,inline with the definition ofamonophalus monster.ZemskyandBudylenko (1970) reportedaseeminglyidenticalcaseoftwinfemalehumpback

whale(Megaptera noveanglia) fetuses with bodylengthsof

124and120 cm. Astripeddolphin doublemonsterwasalso observedbyKawamuraandKashita(1971)-acaseoftwin embryos,withbody lengths16-8and 17-2 cm,fused anteri-orlytotheflippers alongarostrocaudalaxis, likeasycephalus monster.

Finally,afewcasesof individuals withone ormore

anom-alies have also beenreported.Kamiya andMiyazaki(1974)

described the early developmentalstage ofa 9 mm long stripeddolphin embryo showingmultipleseverecongenital

malformations.Perrinand others(1989) reviewed the col-lection ofdolphin embryosheldatthe Southwest Fisheries

Centerof theusNationalOceanographicandAtmospheric

Administrationin LaJolla, California,and described fivecases

of monstrous dolphins of unspecified species, reporting

severecaudalregression(geneticatrophy), megalencephaly (duetocerebrospinalfluidexpansion), omphalocele (diges-tive tractdevelopinginthe umbilicalcord,externallytothe abdominalcavity),cleft mandible andhypoplasiaof maxilla andmonozygote twins.

All ofthesecases arerelativelyunusual and theirrelative prevalencecanhardly be discussedin termsofpossiblecauses, eithergeneticorenvironmental.However,itisinformativeto

compare them withtheprevalence ofmonstrosityamong other mammals.Teratologicalspecimens havelongbeen doc-umentedinadiversityofmammals,mostlydomesticspecies andman, andcasesof double-facedordouble-headed mon-sters arewellknowninthe orderArtiodactyla,theclosest

rel-atives to cetaceansamong terrestrialmammalfauna.

ACKNOWLEDGEMENTS

The authors wouldliketothank M. A.Buttafoco for his field

assistanceandF.Passeleguewhokindly provided

accommo-dationfor the postmortemexamination.Theauthorsarealso

grateful to F. Moutou and D. Robineau for providing refer-encesandconstructive comments.Specialthanksaredueto G. Doremusforhishelpinthepreparation of the skull.

References

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Teratology 12,18

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guidelinesandexpertise recognition. Teratology61,469

BRIARD,M.L. & LEMERRER, M.(1989) Malformationscong6nitales.In

Traite deMedicine. Eds P.Godeau, S. Herson,J. C. Piette. Paris, Flammarion. pp1515-1517

DROOGLEEVER FORTUYN,A.B.&ROMER, J. (1920) Enschede gevonden dubblemonstrum. InHandelingenvanhet XVIIdeNederlandschNatuuren

Geneeskundig Congres. Haarlem, The Netherlands. p229

INOWVE,M.(1989) Teratology of heavymetals:mercuryand other

contam-inants. Teratology40,652-653

KAMIYA, T. &MIYAZAKI, N. (1974) Amalformed embryo ofStenella

coeruleoalba.ScientificReports of the Whales Research Institute, Tokyo

26,259-263

KAMIYA,T., MIYAZAKI, N.&SHIRAGA,S.(1981) Firstcaseofdicephalyin

odontoceti. Scientific Reports of the Whales ResearchInstitute, Tokyo 33,

127-129

KAWAMURA, A.(1969) Siamese twin in the seiwhaleBalaenoptera borealis Lesson. Nature 221,490-491

KAWAMURA,A.&KASHITA,K.(1971)Araredoublemonsterof dolphin. ScientificReports of the Whales Research Institute, Tokyo 23,139-140

MEAD,J.G.&POTTER, C.W.(1990) Naturalhistory ofbottlenose dolphins along the central Atlanticcoastof theUnited States.InThe Bottlenose Dolphin.Eds S.Leatherwood, R.R.Reeves. SanDiego,AcademicPress. pp 165-195

PERRIN,W. F.(1975) Variation ofspotted and spinner porpoise (genus Stenella) in theeasternPacific and Hawaii. Bulletin of the Scripps Institution ofOceanography 21,6-12

PERRIN,E. V.D.,BENIRSCHKE,K.&PERRIN, W.F.(1989) Monstrous dol-phins-malformations in marine mammals.Teratology 39,51

ROMMEL, S.(1990)Osteologyof thebottlenosedolphin.InThe Bottlenose Dolphin. Eds S.Leatherwood,R. R.Reeves. SanDiego, Academic Press.

pp 29-49

SHEPARD,T.H.,BARR, M., BRENT, R. L., HENDRIKX, A.,KOCHAR,D., OACKLEY, G. & SCOTT,W.J.(2000) History of theTeratologySociety. Teratology 62,301-316

SLAIPKA,J.(1994) Malformationas anontogeneticaldeviation anda phylo-genetical reminiscence.Teratology 50, 27

WILSON, J. G. (1986) Definition of the Teratology. The International Dictionary of Medicine andBiology

YASUDA,M.(1994)EnvironmentalpollutionandreproductioninJapan.

Teratology50,21

ZEMSKY, V.A.&BUDYLENKO, G.A.(1970) Siamese twins of humpback whale. Atlant NIRO 24,225-230

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