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Ultrastructure of the Reproductive System of the Black Swamp Snake (Seminatrix Pygaea)

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Ultrastructure of the Reproductive System of the Black Swamp Snake (Seminatrix Pygaea) Butler University Digital Commons @ Butler University Scholarship and Professional Work - LAS College of Liberal Arts & Sciences 2002 Ultrastructure of the reproductive system of the black swamp snake (Seminatrix pygaea). Part III. The sexual segment of the male kidney. David M. Sever Follow this and additional works at: https://digitalcommons.butler.edu/facsch_papers Part of the Biology Commons Recommended Citation Sever, D. M., R. Stevens, T. J. Ryan, and W. C. Hamlett. 2002. Ultrastructure of the reproductive system of the black swamp snake (Seminatrix pygaea). Part III. The sexual segment of the male kidney. Journal of Morphology 252:238-254. Available from: digitalcommons.butler.edu/facsch_papers/530/ This Article is brought to you for free and open access by the College of Liberal Arts & Sciences at Digital Commons @ Butler University. It has been accepted for inclusion in Scholarship and Professional Work - LAS by an authorized administrator of Digital Commons @ Butler University. For more information, please contact [email protected]. JOURNALOFMORPHOLOGY252:238–254(2002) UltrastructureoftheReproductiveSystemoftheBlack SwampSnake(Seminatrixpygaea).III.SexualSegment oftheMaleKidney DavidM.Sever,1*RebeccaA.Stevens,1 TravisJ.Ryan,2,3 andWilliamC.Hamlett4 1DepartmentofBiology,SaintMary’sCollege,NotreDame,Indiana 2SavannahRiverEcologyLaboratory,Aiken,SouthCarolina 3DivisionofBiologicalSciences,UniversityofMissouri,Columbia,Missouri 4IndianaUniversitySchoolofMedicine,SouthBendCenterforMedicalEducation,NotreDame,Indiana ABSTRACTInmaturemalesnakesandlizards,adistal spermatogeniccycleandmatingactivity.Weshowthat portionofthenephronishypertrophiedinrelationtoits synthesisofsecretoryproductisinitiatedwiththeonsetof appearanceinfemalesandimmaturemales.Thissexual spermatogenicactivityinthespringandculminateswith segmentofthemalekidneyapparentlyprovidesseminal completionofspermiationinthefall.Secretionofthe fluidthatismixedwithspermandreleasedintothefe- product,however,occursinaprematingperiodinMarch malecloacaduringcopulation.Inthisarticle,weprovide whenthetestesareinactive.Secretionduringthispre- thefirststudyattheultrastructurallevelofseasonal matingperiodisprobablynecessarytoprovidetimefor variationinthesexualsegmentofthekidneyofasqua- thepassageoftheproductsdowntheureterinorderto mate,thenatricinesnakeSeminatrixpygaea.Previous mixwithspermduringmatinglaterinspring.J.Morphol. workershaveindicatedthatthesexualsegmentissecre- 252:238–254,2002. ©2002Wiley-Liss,Inc. toryonlywhenthetestesarespermatogenicallyactive. ThesexualsegmentofthekidneyinS.pygaeadoesnotgo KEYWORDS:Reptilia;Squamata;Serpentes;Semina- throughanextendedperiodofinactivitybutdoesshowa trix;kidney;sexualsegment;histology;ultrastructure; cycleofsynthesisandsecretionthatcanberelatedtothe reproduction Thefirsthistologicaldescriptionofasquamate reptilesthepresenceofasexualsegmentcanbe nephronwasmadeontheEuropeannatricinesnake consideredasynapomorphyatleastfortheSqua- NatrixnatrixbyGampert(1866).Henotedthata mataandprobablyfortheLepidosauria. portionofthedistalsegment(the“Harncanalchen”) Withinsquamates,however,somevariationoc- wasespeciallythickenedandheprovidedthefirst cursintheextentofthesexualsegment.Inmost accurateillustrationofasnakenephron(Fig.1). snakesthesexualsegmentjustinvolvesthetermi- SubsequentreportsbyHeidenhain(1874),alsoonN. nalportionofthedistalconvolutedtubule(called natrix,andbyTribondeau(1902),onColuberviridi- thepre-terminalsegmentbyFox,1952).Inmany flavus,describedtheenlargeddistalsegmentofthe lizardsandsomesnakes,thesexualsegmentmay nephron.RegaudandPolicard(1903),however, includetheterminalsegment,postterminalseg- werethefirsttonotethatthissegmentwassexually dimorphic,beinghypertrophiedonlyinmales(but seeDelConte,1972).Theynamedthisregionthe “segmentsexuel.” Contractgrantsponsor:U.S.DepartmentofEnergytotheUniver- RegaudandPolicard(1903)alsodemonstrated sityofGeorgiaResearchFoundation;Contractgrantnumber:DE- thatthesexualsegmentwaspresentinavarietyof FCO9-96SR18546. malesnakesandlizardsbutwasabsentinturtles. Laterworkconcludedthatthesexualsegmentis CurrentaddressforT.J.Ryan:DepartmentofBiology,ButlerUni- alsoabsentincrocodilians(Fox,1952)butispresent versity,Indianapolis,IN. inamphisbaenids(BonsandSaintGirons,1963; *Correspondenceto:DavidM.Sever,DepartmentofBiology,Saint SaintGirons,1972);aportionofthenephronof Mary’sCollege,NotreDame,IN46556. Sphenodon(Rhynchocephalia)mostlikelydifferen- E-mail:[email protected] tiatesseasonallyintoasexualsegment(Gabeand †ThisarticleisaUSGovernmentworkand,assuch,isinthepublic SaintGirons,1964).ThereptiliancladeLepidosau- domainintheUnitedStatesofAmerica. riaistraditionallycomposedoftheSquamata PublishedonlinexxMonth2002in (snakes,lizards,andamphisbaenids)andRhyn- WileyInterScience(www.interscience.wiley.com) chocephalia(cf.,Poughetal.,1998).Thus,among DOI:10.1002/jmor.1102 ©2002WILEY-LISS,INC. KIDNEY SEXUAL SEGMENT 239 Fig. 1. Male snake nephrons as originally depicted by Gampert (1866), copied by Regaud and Policard (1903), and redrawn here by T.J. Ryan. Terminology follows Bishop (1959). The “inter- mediate segment,” a short portion between proximal and distal segments that is difficult to distinguish externally, is not labeled. ment, collecting ducts, and/or portions of the ureter tions may sustain and activate sperm (Bishop, 1959; (Fox, 1965; Saint Girons, 1972). Cuellar, 1966), provide courtship pheromones (Vol- Fox (1977) provides a comprehensive review of the søe, 1944), form copulatory plugs (Devine, 1975), literature and no major morphological studies have and/or have other purposes generally associated been done since that time. The function of the sexual with seminal fluid (Prasad and Reddy, 1972). The segment is still not clearly understood, but its secre- only other source of seminal fluids in squamates is 240 D.M. SEVER ET AL. the epididymis (Depeiges and Dufaure, 1980). Max- TABLE 1. Specimens utilized and diameters of 10 sexual imal development of the sexual segment is related to segment tubules per individual increased androgen levels (Bishop, 1959; Misra et Sexual segment al., 1965; Pandha and Thapliyal, 1964; Prasad and 1 2 3 Sanyal, 1969; Krohmer, 1986). Thus, seasonal vari- Date sacrificed SVL Prep Range Mean SE ation occurs, with the height of development gener- 31 March 28.1 Par 0.15–0.21 0.17 0.005 ally associated with the mating season. Snakes, 26.2 JB4 0.15–0.20 0.18 0.005 however, do not show as marked seasonal changes 23.2 TEM 0.13–0.18 0.15 0.005 16 May 26.1 Par 0.12–0.20 0.15 0.007 in the sexual segment as lizards (Fox, 1977). 27.9 JB4 0.15–0.18 0.17 0.004 To our knowledge, only three ultrastructural stud- 31.2 TEM 0.11–0.15 0.13 0.004 ies have previously been done on the sexual segment 9 June 25.6 Par 0.12–0.15 0.13 0.003 of squamates. Furieri and Lanzavecchia (1959) were 23.8 JB4 0.08–0.11 0.09 0.004 concerned only with the effects of castration on the 26.8 TEM 0.11–0.12 0.11 0.002 30 July 28.0 Par 0.12–0.15 0.13 0.003 ergastoplasm of the sexual segment of the lacertid 23.8 JB4 0.08–0.11 0.09 0.004 lizard, Lacerta sicula. Del Conte and Tamyo (1973) 26.8 TEM 0.11–0.12 0.11 0.002 compared the sexual segment of males of the teiid 8 October 28.0 Par 0.13–0.17 0.14 0.004 lizard, Cnemidophorus lemniscatus, to a homologous 25.5 JB4 0.12–0.18 0.15 0.007 area that undergoes some differentiation in females. 29.0 TEM 0.12–0.16 0.14 0.007 They stated that this species has continuous sexual 1SVL ϭ snout–vent length in cm. activity, but used only three specimens of each sex. 2Preparation in paraffin, JB–4 glycol methacrylate, or in epoxy In both L. sicula and C. lemniscatus, the sexual resin for TEM. 3Sexual segment measurements are in mm. segment involves the collecting ducts. The only prior ultrastructural study on a snake is by Kuhnel and Krisch (1974) on Natrix natrix. All of Kuhnel and cago, IL). This procedure was approved by the Ani- Krisch’s specimens were sacrificed in one month mal Care and Use Committee of Saint Mary’s Col- (November), and they did not describe the reproduc- lege. After death, snout–vent length (SVL) was tive condition of their specimens. In this article, we measured from the tip of the snout to the posterior provide the first study at the ultrastructural level of end of the cloacal orifice. The reproductive tracts seasonal variation in the sexual segment of the kid- and kidneys were removed and prepared for light ney of a snake and we relate this to our observations microscopy (LM) and transmission electron micros- on the spermatogenic cycle. copy (TEM). Carcasses of all specimens were pre- served in neutral buffered formalin (NBF) and are MATERIALS AND METHODS housed in the research collections at Saint Mary’s College. The squamate used for this study is the black For LM examination, tissues were initially fixed swamp snake, Seminatrix pygaea (Cope). This small in NBF, rinsed in water, dehydrated in ethanol, (20–40 cm snout–vent length as adults), highly cleared in toluene, and embedded in paraffin or gly- aquatic snake is limited to the southern Atlantic col methacrylate (JB-4 Plus; Electron Microscopy coastal plain of the United States (Dorcas et al., Sciences, Port Washington, PA) plastic resin. Paraf- 1998). This species is the subject of other studies fin sections (10 ␮m) were cut with a rotary mic- concerning its reproductive cycle (Seigel et al., 1995) rotome and affixed to albuminized slides. Alternate and the ultrastructure of the reproductive system paraffin slides from each specimen were stained (Sever and Ryan, 1999; Sever et al., 2000). with hematoxylin-eosin
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