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INTRODUCTION Exotic pets include numerous species belonging to different orders: carnivores, lagomorphs, rodent and many others. Among these, rodenta has a special place due to the high number of species. They represent a significant share of all pets because of their low body weight, gentle character and ease of maintenance, all these based on numerous information available regarding their necessities. All this led to an increasing share of these species as pets, raising the level of addressability with the practitioner in both health problems and counseling owners about reproduction. On the other hand, their usage as experimental model is well known, guinea pigs being chosen as subjects in many studies. However, anatomical data related to the morphology of the reproductive system is scarce in the literature compared to dogs and cats (Barone 2001), which are used as reference in most cases. This justifies the need of knowledge regarding the anatomy of different exotic species to satisfy the need for improvement in nurturing and medical care, especially surgery. Anatomical particularities of mammalian reproductive system are the result of ontogenetic development, which in males is primarily related to the development and migration of the Anatomical Particularities of Male Reproductive System of Guinea Pigs (Cavia porcellus) Florin STAN Department of Comparative Anatomy, Faculty of Veterinary Medicine, University of Agricultural Sciences and Veterinary Medicine, Cluj-Napoca, Romania *Corresponding author: [email protected] Bulletin UASVM Veterinary Medicine 72(2) / 2015, Print ISSN 1843-5270; Electronic ISSN 1843-5378 DOI:10.15835/buasvmcn-vm: 11410 Abstract Currently the pet area shares a great diversity by promoting many exotic species and increasingly expanding existing ones, particularly those of small size. To perpetuate these species a decisive role it has integrity and urogenital health. For this reason and in order to obtain more docile animals, influencing their sexual behavior, veterinarian interventions in order to sterilize, or other curative or preventive maneuvers are required. Knowing in detail the morphology of genitourinary apparatus is crucial for a correct surgical approach. The aim of this study is to achieve a detailed anatomical description of the components of male reproductive system in guinea pigs. Regional stratigraphic dissection was applied on 10 subjects. Macroscopically the components of male genitalia were examined. Wide opening of inguinal ring was present in all subjects. Ovoid testicle shows a well developed epididymus and a considerable amount of surrounding fat tissue. The glans penis is well represented, being present a small os penis within the dorsal surface of the entire length of glans. The seminal vesicles are the most developed sexual accessory glands, having a coiled pattern, blind ended, and stretching until the abdominal cavity. Prostate and coagulating glands are located at the base of seminal vesicles in close relationship. The prostate is composed of two lobes, dorsal and ventral lobe united by a transversal isthmus. Lobulated coagulating glands show pyramidal pattern being located caudal to the bladder. Bulbouretral glands were small, ovoid and lobulated. Both gonads and accessory sexual glands were well-developed in guinea pigs. Keywords: anatomy, guinea pig, male, reproductive system

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Page 1: Anatomical Particularities of Male Reproductive System of Guinea … · 2018-12-15 · The glans penis is well represented, ... size of the accessory sex glands with a length between

INTRODUCTIONExotic pets include numerous species

belonging to different orders: carnivores,lagomorphs, rodent and many others. Amongthese,rodentahasaspecialplaceduetothehighnumber of species. They represent a significantshareofallpetsbecauseoftheirlowbodyweight,gentle character and ease of maintenance, allthese based on numerous information availableregarding their necessities. All this led to anincreasing shareof these speciesaspets, raisingthe level of addressability with the practitionerin both health problems and counseling ownersabout reproduction. On the other hand, their

usage as experimental model is well known,guinea pigs being chosen as subjects in manystudies. However, anatomical data related to themorphologyofthereproductivesystemisscarceintheliteraturecomparedtodogsandcats(Barone2001),whichareusedasreferenceinmostcases.Thisjustifiestheneedofknowledgeregardingtheanatomyofdifferentexotic species to satisfy theneed for improvement in nurturing andmedicalcare,especiallysurgery.

Anatomical particularities of mammalianreproductivesystemaretheresultofontogeneticdevelopment, which in males is primarilyrelated to thedevelopment andmigrationof the

Anatomical Particularities of Male Reproductive System of Guinea Pigs (Cavia porcellus)

FlorinSTANDepartment of Comparative Anatomy, Faculty of Veterinary Medicine, University of Agricultural Sciences and Veterinary Medicine, Cluj-Napoca, Romania*Corresponding author: [email protected]

BulletinUASVMVeterinaryMedicine72(2)/2015,PrintISSN1843-5270;ElectronicISSN1843-5378DOI:10.15835/buasvmcn-vm:11410

AbstractCurrently the pet area shares a great diversity by promoting many exotic species and increasingly expanding existing

ones, particularly those of small size. To perpetuate these species a decisive role it has integrity and urogenital health. For this reason and in order to obtain more docile animals, influencing their sexual behavior, veterinarian interventions in order to sterilize, or other curative or preventive maneuvers are required. Knowing in detail the morphology of genitourinary apparatus is crucial for a correct surgical approach. The aim of this study is to achieve a detailed anatomical description of the components of male reproductive system in guinea pigs. Regional stratigraphic dissection was applied on 10 subjects. Macroscopically the components of male genitalia were examined.

Wide opening of inguinal ring was present in all subjects. Ovoid testicle shows a well developed epididymus and a considerable amount of surrounding fat tissue. The glans penis is well represented, being present a small os penis within the dorsal surface of the entire length of glans. The seminal vesicles are the most developed sexual accessory glands, having a coiled pattern, blind ended, and stretching until the abdominal cavity. Prostate and coagulating glands are located at the base of seminal vesicles in close relationship. The prostate is composed of two lobes, dorsal and ventral lobe united by a transversal isthmus. Lobulated coagulating glands show pyramidal pattern being located caudal to the bladder. Bulbouretral glands were small, ovoid and lobulated.

Both gonads and accessory sexual glands were well-developed in guinea pigs.

Keywords: anatomy, guinea pig, male, reproductive system

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testicles into the scrotum. In rabbit and rodentthe inguinal ring remains open through theanimal’slife(McCrackenet al.,2008;Quesenberryand Carpenter 2012). In these cases, testicledisplacement is physiological compared tomostmammalsinwhichaftermigrationtothescrotum,the inguinal ring closes. The morphology of thereproductive system contains accessory sexualglands alongside essential organs that producespermatozoa – the testicles. In rodents, thesecontainthefollowingformations:vesicularglands,coagulating glands, prostate and bulbo-uretralglands with small variations between species.Morphological development of accessory genitalglandsisinfluencedbymultiplefactors:hormonal,environmental, seasonal variations related toreproductive activity during mating season(Pelletier,2002;Nishinoet al.,2004).

The aim of the present study is to achievea detailed morphological description of themale reproductive system in guinea pigs (Cavia porcellus),thetopographyofessentialreproductiveorgansandaccessorysexglands.

MATERIALS AND METHODSAgroupof6maleguineapigswereused,with

weightsbetween380and650gramsfrombreedingfarms. The subjects were treated according toDirective 2010/63 /EU of the European Parliament and of the Council on the protection of animals used for scientific purposes and the InstitutionalBioethicsCommitteeofUniversityofAgriculturalScience and Veterinary Medicine approved thestudy. Euthanasia was performed by inhalingan overdose of Isoflurane (Baxter Health CareCorporation,USA).The subjectswerepositionedin dorsal decubitus performing the extension

and fastening of thoracic and pelvine members.Theabdominalcavitywasopenedbyperformingan incision along the white line until reachingthepubis. Thedigestiveorganswhichpresentedtopographical relations with components of thereproductive system were identified and thenremoved to achieve a clearer visualization. Afterin situ photographythegenitalapparatushasbeenremoved from the pelvic cavity, identifying eachcomponent. The terms were in agreement withNAV2012.

RESULTS AND DISCUSSION Testicles and sperm ducts (Testis, ducti

genitalis )Inexaminedsubjectsthetesticleswerelocated

intheperinealregion,onbothsidesoftheurethraopening.Theslightlyflatenedaspectoftesticularbursa (Bursae testis) was more visible due tobrowncoloringoftheskinintheprojectionregion(Fig.1).After incisionandsectioningof regionalskin, the testicles were well visualized becausetheirextraabdominallocation,beingenclosedinasignificantammountofadipoustissue.Incontactwith the ventral abdominal wall, between theventral musculature of the abdominal wall andthe skin, the ovoid testicles were dorso-lateralorientedwith a slight ventro-medial tilt (Fig. 1).Sectioning of the external layers has highlightedthe pink colored testicles, with a dorso-laterallylocatedepididimus(Epididymis).Theepididimuscomponents (head, body and tail) were easilyidentified due to their well development. Thehead of the epididymus (Caput epididymis), wasvery coiled and covered with adipous tissuebeing continued through the epididimus bodyventrallypositionedbydeferentducts.Thetailof

Fig. 1. Externalappearanceoftesticularbursawithurethralorifice(U)locatedcranialtotheanus(A)-leftandovalshapeoftesticles-right,inguineapigs

AnatomicalParticularitiesofMaleReproductiveSystemofGuineaPigs(Cavia porcellus)

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theepididymuswasveryobviousduetoexcesivecoiling being continued by the deferent duct(Ductus deferens) of1-2mmdiameter(Fig.2).Theductus deferens presented a relatively tortuousroute in the proximal segment, later to becomeapproximately 1.5-2.5mm in diameter. Whitish,thepairedvasdeferenswerewellvisualizeddueto outline clear, smooth and relatively straightpath(Fig.2).Beforeopeningtheurethra,theductsshowed a slight enlargement in size and a veryshort common route. Testes sizeswere between20-30mmlongand12-18mmcrosssection.

Accessory sex glands We identified the following accessory sex

glandsinallsubjects:seminalvesicles(Glandulae veziculares), coagulating glands, prostate glands(Glandula prostata) and bulbourethral glands (Glandula bulbourethralis).

The seminal vesicles showed a particularpatternbeingtubiform,cylindricalandvermiform,blind ended, well developed, having the largest

size of the accessory sex glands with a lengthbetween100-120mmand5-14mmlarge.Locateddorsal to the bladder and ventral to the uretersthe vesicular glands presented an upward pathsurpassing the pelvic cavity directing deep inthe abdominal cavity. The distal segments werepositionedonbothsidesofthedescendingcolon(Fig. 3). Each vesicular gland presented a broadand well vascularised ligament. The opening ofvesicularglandswasmademedianinuretra intoamediancleft(colliculus seminalis)togetherwiththeductusdeferensopening.

Caudal to the bladder in all subjects weidentified the pair coagulating glands, withpyramidalshape,lobulated,beingdisposedlaterodorsal near the seminal vesicles (Fig. 4). Also,theseglandsweredirectlyrelatedtotheprostategland,beingarrangedcranio-dorsaltothedorsallobeoftheprostate.

The prostate glandwas located immediatelycaudal to the bladder neck, caudomedial to thecoagulating glands and lateral to the seminal

Fig. 2.Ovalshapeoftesticlesandclearvisualizationofdeferensductsandepididymustail–leftandthepresenceofalargeamountoffatoncranialpoleoftesticlesandlargeinguinalrings–right.

Fig. 3.Thetubiformblindendedappearanceofvesicularglandslocateddorsaltothebladderanddeferensducts-leftandawelldevelopedligamentofeachvesiculargland–right.

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vesicles basically being surrounded between thespecifiedcomponents,initsturnsurroundingtheurethra(Fig.4).Largerdorsallobewasjoinedbyasmallisthmustotheventrallobe,smallerinsize.Prostateglandwithcoagulatingglandsappearedlike a common structure without presenting ajointcapsule(Fig.4).

Bulbourethral glands, small, have beenidentified on both sides of the urethra, on theischialarchsegmentoftheurethra,ventraltotherectumanddorsaltothepubicsymphysis(Fig.4).

Intheinitialsegment,thepeniswasattachedto the ischiatic arch by the ischio-cavernousmuscle while the distal segment was includedin the prepuce. Two portions of the penis wererecognized: the penian body and glans both ofthesamecalibrewithlengthsbetween45-85mmand 4-7mm circumference. The junction of thetwosegmentswaswellindividualized(Fig5).Thepeniswas“S”-shaped.Wealsoidentifiedapenianossituateddorsallyalongthepenianglans.Initsretractedpositionthepeniswassituatedventrally

to the pubic symfysis, between the latter andskin. Along all the penis glans until the uretralostiumweidentifiedprominenceslikesmallspursarrangedinparallel linessituateddorso-laterallyandventrally,with theones in thedorsal regionhavingadiscontinuousaspectopposedtotheonesintheventralregionwhichwerecontinuous.

Intheventralsideofthepenis,ventrallyfromthe extrapelvine urethra, in the caudal segmentof the penis, we identified the presence of anintormittentsacwhichopen ina transversalslit,caudally from the urethral ostium (meatus).Inside this formation two slightly curveddownwardskeratinaceousstyleswere identified.Theirinsertionwasatthecranialsegmentoftheintromittentsac.Inlivingsubjectsaslightpressureonthepenisbaseleadtoitsexternalization.

DISCUSSION The variety of information related to the

reproductivesystemofdomesticanimalsisalreadyrecognizedtakingintoaccountthecommercialor

Fig. 4. Theprostateglandtopographyandthecoagulatingglands–left.Theprostateandcoagulatingglandscomposeasinglestructurewithoutacommoncapsule–right.Thetopographyofbulbourethralglandscaudally

totheprostate–right.

Fig. 5. Theguineapigspenisanditsischiocavernousmuscleattachment–leftandtheSshapeofpenis–right.

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productive aspect. However, the morphologicaldescriptionsof thereproductivesystemofexoticspecies used as pets or as experimental modelsare relatively few. From all this, rodents andlagomorphs, especially mice, rats and rabbitsreceivemore attention because they are used invarious medical experiments (Vasquez and DelSol2002Suckovet al.,2005;KnoblahghandTrue,2011). Reproductive components are relativelysimilarinmostspeciesandincludeprincipalorgans-testes,spermaticductsandaccessorysexglands(Barone2001).Developmentofthesecomponentsisinfluencedbyvariousfactorssuchashormonecompositionandandrogenicstimulationbeingofthehighestimportance(Cepedaet al.,2006).Otherfactorsincludethecomponentsitself,namelythepresence or absence. In the latter scenario, theremaining organs take over the function of themissingone.Environmental factors, timeof yearandmatingseasonalsoinfluencethemorphologyand function of the reproductive apparatus(Gotteichet al.,1998;Nishinoet al.,2004;Breedet al.,2014).

Morphologyofmainorgansofthereproductivesystem in guinea pigs is common with that ofotherspecieslikecattle,sheep,swine,lagomorphsandevenhumans.The caudal-lateral orientationandaslightdorso-ventraltiltiscommoninmostrodents and lagomorphs (Barone 2001, Cooperet Schiller, 1975). Also, the extraabdominaltopographywiththepossibilityofintraabdominalmigration is present in rabbit as well. Duringfetal development the testicle descent throughtheinguinalchannelintothescrotalpoughtakesplaceintwomorphologicallydistinctphases,eachcontrolled hormonally by secretions from thetesticlesthemselves,withdirectimplicationuponthe gubernaculum testis. From the caudadl poleof the kidney, the testicles migrate through theinguinalchannelfollowingthelengtheningofthegubernaculumsandsuspensorligamentregressionconditioned by testosterone production (Hutsonet al., 2009, 2015).Thus, in some animals thedescentiscompletesincethefetalphase(cattle)oronlyapproachingbirth(horse)(Barone2001).Thetesticlesmigration through the lifemake guineapigsandrabbittohavefunctionalcryptorchidismThe extraabdominal loction of the testicles is ofgreat importance for sperm production becauseofthelowtemperaturenecessaryforthisprocess.The control for low temperature maintenance

is done by contraction of the dartoic layer andtesticularcordwhichbringcloserortakefurtherthetesticlesfromthebody.

The guinea pigs epididymis have commoncharacteristics with those of most mammals.Thepronouncedcoilingofheadandofthetailofthe epididymis is usually found in rat, hamster,chinchilla and in rabbit (Barone2001). The vastamountoffatcoveringtheheadoftheepididymisfoundinguineapigsandandotherrodentsisnotsowellrepresentedinrabbits.Duetothispatternthe need of surgical closure of the inguinal ring,in orchiectomy might be controversial. Someauthors claim that this amount of fat justmighthaveaprotectiveeffect.Inouropinion,topreventpostoperative herniation suturing is necessaryduetoconsiderablewidthoftheinguinalringandthe possibility of migration of fat from inguinalring. More over this fat is removed during theorchiectomy.Thus, this anatomical peculiarity oftesticles inguineapigshasdirect implications inorchiectomy.

Open or closed surgical approach is themostappropriatefortherodentsduetotheeasyanatomicalclosurebysuturingtheinguinalringswhich are much broader in guinea pigs than inrabbits. Abdominal laparoscopic approach isappropriate to juveniles or in rodents whosetesticles migrate extra-abdominally only inreproductive seasons such as sqiurel or prairiedog(Linetz2000).

Accessorysexglandsinguineapigsweretheseminal vesicles, coagulating glands,, prostateglands and bulbourethrale glands. In mammalsthepresenceofaccessorysexglandsisvariable,intermsof topography,number,sizeandespeciallyshape. The largest diversity is found in rodents,thefourcomponentsbeingpresentinrats(Rattus rattus) (Knoblahgh and True, 2011), chinchilla(Chinchilla lanigera)(Cepedaet al.,1999;Calamaret al.,2014)andspotedpaca(Agouti paca)(Borgeset al., 2014)while in rabbits are foundvesicularglands,well-developedprostateandrudimentarybulbourethrale glands which can be observedonly ventrally due to their small size (Barone2001).Incapybaraonlytheprostateandvesicularglands were reported (Ferandez et al., 2010).Regardlessofthepresenceorabsenceofsomeorotheraccessorysexglandstheirtopographyisthesameinallspecies–thefollowingareattachedtothe uretra in caudal direction: vesicular glands,

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coagulating glands, prostate and bulbourethralglands.

Ourresultsregardingthetubular,vermiformblindendedandslightlycoiledpattern,ofvesicularglandsaresimilartothosedescribedinchinchilla(Calamariet al.,2014).Thefactthattheseglandsare well represented is due to their function insecretionofseminalfluidaspartofthesperminarangeof50%,bothinguineapigsandchinchilla.Its production is important because in thesespecies after copulation, in the vaginal plug thecompositionproducedbythevesicularglandshasahighpercentage.Likeinrats(Sukovet al.,2005;Knoblahgh and True, 2011), vesicular glandsopeninginguineapigsarecommonwiththevasdeferensopeningcomparedwiththespotetpacawhich present separate openings of deferentsductsandseminalvesicles(Borgeset al.,2014).

The topography of the coagulating glanddescribed in this study, - located laterodorsal tothevesicularglandsandcraniodorsaltothedorsallobeof theprostate- issimilartothatdescribedin chinchillas (Cepeda et al.,2006) and gerbil(Pinheiro et al., 2003). In rats the coagulatingglands are located on the medial sides of thevesicularglands(KnoblahghandTrue,2011)beingreferredtoasanteriorprostaticlobes.Inrodentsthe similarity regarding the coagulating glandsisrelatedtotheircloseproximitytotheprostategland,eveniftheiropeningareatdifferentlevelsoftheurethra(Pinheiroet al.,2003;QuesenberryandCarpenter2012).Domesticspecieslikedog,horse,ram,goatandbull lackcoagulatingglands(Barone2001)

Inanimals,prostateglanddescriptionshowsthe presence of several lobes, compared tomanin which the prostate gland is a singular organ(Gray 1918). In chinchilla the presence of twolobes was described, the right and left, dorsallocatedtothejunctionoftheseminalvesicleswithurethra,unitedbyanisthmus(Cepedaet al.,2006;Calamari et al., 2014). These descriptions aresimilartoourresultsinguineapigs,inwhichtheprostateglandwascomposedoftwolobes:awelldeveloped dorsal lobe and a small ventral lobe.Neuhausetal.,2001madethesamedescriptioninguineapigsusingadifferentterminology:cranialand caudal lobe. In rats, according toKnoblahghandTrue,2011,theprostateglandhasfourlobes:anterior, dorsal, lateral and ventral, sometimesthedorsalandlaterallobesbeingidentifiedasthe

dorsolateral lobe.Thedorsal lobe surrounds theurethrawhile theventral lobe isarrangedbelowtheurethra and caudal to thebladderneck.Duetothesimilarstructureofthecoagulatingglandswith the prostate, these glands are sometimescalled the anterior lobe of the prostate, beingattachedto the lessercurvatureof the vesicularglands(KnoblahghandTrue,2011).

The ferret (Mustela putorius) shared thesame characteristic regarding the presence ofthe prostate gland as single organ, considerablyincreased in size (1.5/0.6cm), as in humans,surrounding the urethra (Jakobs and Podar,1986). Moreover, in ferret the prostate is theonlyaccessorysexgland.Themostcontroversialdescriptionsoftheprostateareinrabbits.Inthisspecies thr prostate is composed of three parts:proprostata, prostate and paraprostata (Holtsand Foote 2005; McCraken et al., 2008). Theproprostateisthesegmentlocatedcaudallyfromthevesicularglandsandcraniallytotheprostatewhile the prostate and paraprostate are locatedcranially to the bulbourethral glands. Theseglandular structures open at the intrapelvineurethra on both sides of the seminal culliculum(VasquezandDelSol2002;).

The bulbourethral glands in guinea pigs aresituated caudally to the prostate, dorsally to theurethraanddorsolaterallytotheischiocavernousmuscle.Thesametopographyhasbeendescribedin rats (Knoblahgh and True, 2011), chinchillas(Cepeda1999)andagouti(Menezeset al.,2010).Aparticularaspectoftheseglandsisthattheyarelocatedmorecaudallyontheurethra,notbeinginthecloseproximityoftheprostate,asisinhumans(Gray 1918; Barone 2001; Knoblahgh and True,2011). The lobulated, oval shape is common toratsandguineapigswhileinrabbitstheseglandsonlyhavethelattercharacteristic.

A particularity of the penis in guinea pigsrevealed by our study is the presence of theintromittentsac,situatedventrallytotheurethraandthetwokeratinoceousstyleswhoseinsertionsare cranially in thementioned structure. Duringthe erection the two keratinoceous styles areexternalized. This aspect has been previouslyreported in guinea pigs (Weir 1974; Cooperand Sdchiller 1995) and agouti (Molineau et al.,2006,2009).Alsothepresenceofthesmallspur-shapedformationsattheonthepenianglanswasdescribedinagouti(Molineauet al.,2005)spoted

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paca (Borges et al., 2014) and even cat (Barone2001). Even if the role of the proeminences onthe intermitent sac is not known (Cooper andSchiller1997)theirpresencealongsidethespur-shapedformationsanchorthepenianglandinthefemale vagina, contributing to the stimulationofspontaneousfemaleovulation.

Thepresenceof thepenianos iscommontoguineapigs,chinchillas,(Cepedaet al.,2006)andrats(KnoblahghandTrue,2011)butnottorabbitsin which, on the other hand has been observeda free extremity of the penis (Queensbery andCarpenter,2004).Alsothetopographyofrabbit’spenis is different from the one we observed inguineapigs,inwhichthepenisissituatedbetweenthe two testicles. This aspect can be consideredanadvantagewhile castrating rabbitsdue to thepossibility the prescrotal approach compared toguineapigsforwhichtwoincisionsarenecesary.

Acompletedescriptionincludinghistologicalresearch on the reproductive system in guineapigsisthesubjectofanotherongoingstudywhichwillbepublishedinthefuture.

CONCLUSIONThemorphology of the genital apparatus in

guineapigsshowsmanysimilaritieswith thatofrodents.

In guinea pigs the position of the testiclesin scrotal pouches without an obvious scrotum,their oval shape and overall conformation andtopographyiscommontothatofrats,chinchillas,rabbits,ferretsandotherrodets.

Theopenstateoftheinguinalcanalthroughoutall their lifespan, allows the intraabdominalmigrationofthetesticles,similartorabbits.

In guinea pigs the accessory genital glandsare: vesicular, coagulanting, prostate andbulbourethral.

The vesicular glands are well representedwith a vermiform aspect similar to chinchillas,extendingdeepintotheabdominalcavity.

Theprostatehastwolobes:awell-developeddorsaloneandasmallerventralone.

Presence of the intromitent sac is unique tohistricomorphs.

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