Pesq. Vet. Bras. 36(10):1014-1020, outubro 2016 DOI: 10.1590/S0100-736X2016001000016
Morphology of the testes and epididymal ducts in the pampas cat Leopardus colocolo (Molina, 1782)1
Mahmoud Mehanna2 3, Adelina Ferreira3 2*
ABSTRACT.- , André L.S. Ferreira and MorphologyRegina C.R. Pazof the testes and epididymal ducts in the Pampas cat Leopardus colocolo (Molina, 1782). Pesquisa Veterinária Mehanna Brasileira M., Ferreira 36(10):1014-1020. A.L.S., Ferreira A. & Paz R.C.R. 2016. - Laboratório de Pesquisa em Animais de Zoológico, Faculdade de Agronomia,[email protected] Medicina Veterinária e Zootecnia, Universidade Fede ral deThe Mato pampas Grosso, cat Avenida Leopardus Fernando colocolo Corrêa (Molina, da Costa 1782) 2367, is a Bairrospecies Boa of Esperança,the Felidae Cuiabá, family, MT 78060-900, Brazil. E-mail: - mation,widely distributed the objective in ofSouth this America,study is to included describe on morphologically CITES Appendix the II testesand classified and epididymal as Near ductsThreatened of pampas on the cat. IUCN The Redanimal, List, coming with population from the Federal trend decreasing. University Basedof Mato on Grosso this infor Zoo, Brazil, had died after anesthesia procedure and the male reproductive system was dissec- ted to collect the testicles. The samples taken were fragmented and histologically exami- -
ned. From the microscopic analysis of the testes were identified: vaginal and tunica albu andginea, coated formed internally by dense by connectivespermatogenic tissue epithelium modeled consistingwith large ofamount Sertoli of cells, collagen surrounded fibers. byThe a tunica basement albuginea membrane fibrous in septa the presence emits into of the myoid body. cells. The seminiferousThe interstitial tubules tissue are between coiled the seminiferous tubules, is composed of loose connective tissue, blood and lymph vessels, - mnar epithelium with secretory cells of which stereocilia design, situated on a basement and Leydig cells in polyhedral shape. The epididymal ducts showed pseudostratified colu design stereocilia toward the lumen of the epididymal duct. membrane filled by myoid cells. This epithelium has principal and basal cells, the main cell Leopardus colocolo, histology, morphol- ogy, Felidae. INDEX TERMS: Testicles, epididymis, pampas cat, RESUMO.- [Morfologia dos testículos e ductos epididi- base nessas informações o objetivo deste estudo é carac- mários do gato-palheiro Leopardus colocolo (Molina, terizar morfologicamente os testículos e ductos epididi- 1782).] O gato-palheiro Leopardus colocolo (Molina, 1782) mários de L. colocolo é uma espécie da família Felidae, com ampla distribuição na América do Sul. Está incluido no Appendix II da CITES . O animal, oriundo do Zoológico da- - culinoUniversidade foi dissecado Federal para de coletaMato Grosso,dos testículos. Brasil, Asveio amostras a óbito lha da IUCN, apresentando população em decrescimo. Com retiradasapós procedimento foram fragmentadas anestésico e e o histologicamentesistema reprodutor exami mas- e classificada como Próxima da Extinção na Lista Verme 1 Received on October 2, 2015. pornadas. tecido A partir conjuntivo das análises denso modelado, microscópicas com grande dos testículos quanti- 2 foram identificados: a túnica vaginal e albugínea, formada Accepted for publication on May 30, 2016. Laboratório de Pesquisa em Animais de Zoológico (LPAZ), Faculdade sãodade enovelados de fibras de e colágeno.revestidos A internamentetúnica albugínea por emite epitélio septos es- de Agronomia, Medicina Veterinária e Zootecnia, Universidade Federal regina- fibrosos para o interior do órgão. Os túbulos seminíferos- [email protected] Mato Grosso (UFMT), Av. Fernando Corrêa da Costa 2367, Bairro Boa Esperança,3 Cuiabá, MT 78060-900, Brazil. *Corresponding author: lulas somáticas de Sertoli, envolvidos por uma membrana - basaltratificado com presença constituído de célulaspor células mioides. espermatogênicas O tecido intersticial, e cé Laboratório de Análises Morfológicas e Morfométricas, Instituto de - Biociências, UFMT, Av. Fernando Corrêa da Costa 2367, Bairro Boa Espe rança, Cuiabá, MT 78060-900, Brazil. entre os túbulos seminíferos, é constituído de tecido con 1014 Morphology of the testes and epididymal ducts in the Pampas cat Leopardus colocolo (Molina, 1782) 1015 juntivo do tipo frouxo com vasos sanguíneos e linfáticos, e - of Argentina, Bolivia and Brazil. In the IUCN (International - UnionPampas for Cat Conservation is listed as Vulnerable of Nature byand the Natural national Resources) Red Lists docélulas com decélulas Leydig secretoras em formato dos poliédrico. quais projetam Os ductos estereocílios, epididi situadosmários apresentaram sobre uma membrana epitélio cilíndrico basal repleta pseudoestratifica por células - cheriniRed List et ofal. Threatened2015). Species (2015) is listed by Near cujas células principais projetam estereocílios em direção ThreatenedThe pampas (ND) cat with is a populationsmall feline trend that looks decreasing similar (Lu to mióides. Este epitélio apresenta células principais e basais, the domestic cat, whose length of the head and body has an average of 52 cm, the tail is short, with 27 cm and wei- ao lúmen do ducto epididimário. Leopardus colocolo, histologia, morfologia, Felidae. TERMOS DE INDEXAÇÃO: Testículos, epidídimo, gato-palheiro, general color of the coat is predominantly light brown or ght ranges around 3.5 kg (Oliveira & Cassaro 2005). The INTRODUCTION grayish brown, with long dark hair in the dorsal region; triangular ears; dimmed present stripes on the sides of the Felines are top predators in the food chain and some authors body and the legs have transverse stripes, characteristic of the species (Nascimento 2010). species, since their disappearance would cause damage at This feline is nightly, terrestrial and solitary habits. It is define them as ecosystem health indicators calling them key all trophic levels of the food chain (Soulé 2000, Muller-Filho a carnivore, feeds mainly on small vertebrates like rodents, 2000). The cats are strict carnivores, representing the lar- gest predators of tropical forests, with great expression in and insects (Bagno et al. 2004). Gestation lasts about 80 the control of other vertebrates (Balarini 2008). daysground and birds the (Romopup’s number 1995), reptilesper litter (lizards is typically and snakes)two or - rance of key species can induce changes in ecosystem struc- Considering the perpetuation of a species, especially tureAccording and biodiversity to Miller loss, & Rabinowiz as these animals, (2002), regulatingthe disappea the wildthree cats, (Fajardo the reproductive & Pacheco 2011). system is possibly the most im- population of their prey and can affect the behavior of the same. Thus, although there is the conservation and mana- portant. The female role is to provide place for a concep- gement of populations of wild cats in free life, there is still tion, embryo development and release of a viable cub. But the need to maintain some species in captivity in order to the male has the responsibility to produce and transport reintroduce the pups born to the nature, aiming to prevent There are no data in the literature about pampas cat Many felid species exhibit polymorphism for melanism maleviable reproduction; sperm (Vidis 2014).however, the domestic cat can be used butthe extinctionthe relative of theseroles playedspecies by(Swanson genetic 1998).drift, natural se- as a model. Sexual maturity in domestic cats occurs betwe- lection, and interspecies hybridization remain uncertain. en eight and twelve months coinciding with the appearance Schneider et al. (2015) analyzing three wild cat species of sperm in the ejaculate. Males maintained in controlled showed points to unique evolutionary histories for each lighting do not exhibit seasonal reproductive behavior, and species, with a strong selective sweep in the pampas cat. animals kept in subtropical or tropical climate are fertile These results reveal an important role for natural selection. The Leopardus colocolo, popularly known by pampas Knowledge of the reproductive function of this specie cat, it’s kind of the Felidae family (currently divided into isand important sexually activebecause throughout there is great the year similarity (Paz 2013). between the - reproductive anatomy of the domestic cat (Felis catus) and nera and 40 species), with wide distribution in South Ame- most of the wild felines, so many studies can be performed rica,two subfamiliesextending from - Felinae the Ecuadorian and Pantherinae, Andes andto the has south 14 ge of using them as valuable biological model for physiology fe- line reproduction, especially for other endangered species and Central portions and southern Brazil (Cossios et al. (Wildt et al. 2007).Argentina, including Peru, Bolivia, Chile, Paraguay, Uruguay 2001). The regions where exist records of Leopardus colocolo In this sense, 1986, studiesGoodrowe related et al. to1989, the Pukazhenthigonads of males et al. include different habitats such as pastures and plains, den- se rain forests and mountains with poor vegetation in very morphological aspect, where exist few data in the literature high altitudes, as well as ecosystems such as southern gras- onof thisthe histologyspecies has of wildscientific cats testicles,relevance, and particularly in order to in com the- slands, riparian forests and savannas with a predominan- plement it is that purport to histological analysis and des- cription thereof to obtain information that might be useful in relation to reproduction of the species. ce of fields in Brazil, associated usually with open habitats- viduals/km²)(Garcia-Perea 1994).and localized throughout most of its range, MATERIALS AND METHODS andPampas appears cat to isbe generally declining rare in several or very parts rare (0.05-0.2of its extent indi of For this study, we use a male specimen pampas cat (Leopardus occurrence because of extensive loss or reduction in quali- colocolo, Molina 1782), who came from nature was a cub. The ani- mal was kept alone at UFMT Zoo, had ad libitum access to water and commercial dog food or meat was offered once daily. The cat habitatty of its ishabitat. widespread Predation and byis adogs, primary hunting concern. and roadIncluded kills died after anesthesia procedure for collection of biological mate- onare CITESadditional (Convention threats. Population on International decline Tradecaused in by Endan loss of- rial for epidemiological research, with 4 years of age and 3.5 kg gered Species of Wild Fauna and Flora) Appendix II. The body weight.
Pesq. Vet. Bras. 36(10):1014-1020, outubro 2016 Mahmoud Mehanna et al.
1016 In order to carry out the histological analysis, the male repro- more elongated shape and pyramidal cell with irregular ductive tract was dissected to collect the whole testis and the epi- contours and extending from the basement membrane to didymis, observing the arrangement of the organs. The samples the tubule lumen, and appear spherical to oval nucleus, nu- taken were fragmented into four parts, with distal and medial to cleolus with noticeably stained. the right and left testicles. Subsequently they were dehydrated in the seminiferous tubules, appear composed of loose con- RTS,alcohol where at 70% they andwere 95% cut to and a thickness embedded of in3µm glycol and methacrylatestained with The interstitial tissue, which fills the spaces between- type plastic resin, and brought to the microtome Leica RM2125 - nectivedifferent tissue sizes, presenting bright nuclei fibroblasts, and nucleoli blood evident and lymph (Fig.2B). ves criptionaqueous of1% structures. toluidine blue. And, finally, they were sent to photo sels,Analyzing and Leydig microscopically, cells appearing the in Leopardus polyhedral colocolo shape withepi- documentation, microscopic analysis in Leica DM750 and des didymal, it was found that is surrounded by a thick tunica RESULTS albuginea and dense modeled connective tissue, covered by the visceral layer of the tunica vaginalis. The epididymal The pampas cat male reproductive system is formed by the testes, epididymis, vas deferens, accessory glands, penis with secretory cells of which stereocilia design. This epi- and foreskin. theliumducts are is lined on a bydelicate a pseudostratified basement membrane columnar and epithelium integra- The testes are oval to rounded paired organs, loca- ted outside the abdominal cavity, in a skin fold called the structure. And, according to the cross sections of epididy- scrotum. These organs are responsible to the production malted byduct, myoid it was cells found (flat that cells they, with generally obvious have nucleus) a predomi in its- of sperm and secretion of male sex hormones, especially nantly ovoidais forms ducts (Fig.3A). testosterone. The coloration follows from white to yellow and is surrounded by a capsule called the tunica albuginea, consisting of dense connective tissue. Microscopically, the tunica albuginea examined in Le- opardus colocolo testis (Fig.1A) showed thick, formed by dense connective tissue modeled with great amount of the tunic). This is thickened on the dorsal which forms the mediastinumcollagen fibers, testis synthesized (axial range by fibroblastsof connective (cells tissue) found sen in- - partments called testicular lobes (Fig.1B). Beyond that, tes- ticularding fibrous arteries septa and intoveins the enter organ this by capsule, dividing demonstrating it into com a highly vascularized tissue. The tunica albuginea is cove- red by the visceral layer of the tunica vaginalis, consists of
The seminiferous tubules presented themselves as the mostconnective abundant tissue component with fibroblasts of the and pampas blood vessels.cat testicular parenchyma, performed tightly curled and coated strati- rise to sperm) and Sertoli cells, surrounded by a basement membranefied epithelium (Fig.2A). consists Adjacent of spermatogenic to the basement cells (whichmembrane, give - togonia cells round with rounded nuclei and one or more evidentthere is nucleolithe presence found of in flattened basal compartments myoid cells and of seminife sperma- rous tubules. with nuclei and evident nucleoli. Since the secondary sper- matocytesPrimary appear spermatocytes in sequence appear as smaller as larger cells round compared cells to primary spermatocytes, with nuclei and nucleoli barely visible, these, in turn, result in spermatids. Both sperma- tocytes result of spermatogonia divide and are located in adluminal compartment, where the germ cells are develo- ping (Fig.2B). with little stained nuclei (Fig.2B). After develop, spermati- ds appearThe spermatids darker, small present, , oval in and a first elongated. stage, as Both rounded are locacells- Fig.1. (A) ted in adluminal compartment, the latter with the presence obj.40x.Vaginal (B) and albuginea tunic, connective tissue (CT), of long tails projecting into the lumen of the seminiferous FibroblastsBlood vessel (arrows) (arrows) andcompartmentalizing Blood vessel (Vs). the Toluidine testis into blue, lo- tubule to differentiate into sperm. (Fig.2C). bules; SeminiferousTunica albugineatubules (Ts), (TA) Germinal and fibrous epithelium septum (Sp),(EG) The Sertoli cells are less frequent, distinguished by a
and the Lumen (L). Toluidine blue, obj.10x. Pesq. Vet. Bras. 36(10):1014-1020, outubro 2016 Morphology of the testes and epididymal ducts in the Pampas cat Leopardus colocolo (Molina, 1782) 1017
The cells of the epididymal duct epithelium are repre- sented by principal or columnar cells and basal cells. The principal cells are covered with long branched stereocilia with elongated nuclei and distinct nucleoli. The basal cells presenting rounded or oval, irregularly shaped nuclei and can be extended or elliptical and nucleoli are conspicuously peripheral (Fig.3B). The epididymal duct is surrounded by a tissue called peritubular stroma, which is composed of an arrangement
muscle cells, and is vascularized, located externally the ba- sementof collagen membrane fibers with of the fibroblasts, duct. fibrocytes and smooth Inside of the duct lumen it was found, sometimes, some material, probably represented by product of cell and sperm secretions. The lumen has, throughout its length, long stereocilia, which protrude from the principal cells present in the epithelium (Fig.3B). The end of the epididymal duct originates from the vas deferens, which ends in the urethra, which empties its con-
Fig.2. (A) Cross section of the pampas cat testis. Observe semi- - ca albuginea (TA) and interstitial tissue (arrows). Toluidine Fig.3. (A) Epididymal cut, observe epididymal ducts (De), con- blue,niferous obj.10x. tubules, (B) germinalSpermatogonia epithelium (E) primary (EG), Lume spermatocytes (L), tuni nective tissue (TC), tunica albuginea (TA) and tunica vaginalis (E1), spermatids (Es), Sertoli cells (S), interstitial tissue (TI) (C) Seminiferous obj.10x. (B) E - epithelium. Note spermatogonia (E) primary spermatocytes broblasts(TV), sperm (arrows), (Ep) and basal blood cell vessels (Cb), columnar (arrows). cells Toluidine (Cc), myoid blue, and Leydig cells (L). Toluidine blue, obj.40x. cells (Cm), stereociliapididymal (Ec) ducts and (De), sperm connective (Ep). Toluidine tissue (TC), blue, fi sperm (Ep). Toluidine blue, obj.40x. obj.40x (E1), spermatids (Es), Sertoli cells (S), Leydig cell (L) and
Pesq. Vet. Bras. 36(10):1014-1020, outubro 2016 1018 Mahmoud Mehanna et al.
tween one and eight years also have thick tunica albuginea and formed by moderately dense modeled connective tis- -
thesue. testicular These verified parenchyma. the presence of large amounts of colla genThe and seminiferous discrete elastic tubules fibers arewith formed thin septa by columnar emission intoepi- thelium, consisting of spermatogenic cells and Sertoli cells, surrounded by a basement membrane, separated by inters- - tions of spermatogenic cells of the epithelium development occurtitial tissue.within Accordinga seminiferous Bacha tubule, & Bacha in which (2003), these combina cellular stages occupy a portion of each tubule, and the total num- ber of different stages varies according to the species stu- died. The adult cats show the seminiferous tubules with large diameter, high germinal epithelium and small light - thelium of Leopardus colocolo showed a segment to which ittubular shall spermatogonia,(Silva et al. 2009). two In layers this sense, of spermatocytes the germinal (pri epi- mary and secondary) and numerous rounded spermatids. The germ cells, throughout the seminiferous epithelium are organized and supported by the Sertoli cell (Russell et
of FSH and testosterone in the spermatogenic process, in theal. 1990), support which and playsnutrition a fundamental in developing role germ in the cells mediation , in the compartmentalization of the seminiferous epithelium, in
secretion and phagocytosis of degenerating germ cells, andthe releasethe excess of spermatozoacytoplasm of spermatidsin the tubular in spermiogenesislumen, in fluid
The Sertoli cells are less frequent, distinguished by a more(Russell elongated & Griswold shape 1993, and Balarini pyramidal 2008). cell with irregular contours and extending from the basement membrane to the tubule lumen, and appear spherical to oval nucleus, nu- Fig.4. (A) Cross section of the vas deferens, observe smooth mus- cleolus with noticeably stained. - blood vessels (arrows). Toluidine blue, obj.10x. (B) Cross sec- ment consists of different components allocated between cle layers (ML), epithelium (Ept), connective tissue (TC) and the Accordingseminiferous Hooker tubules, (1970), among the which intertubular are connective compart tis- stereocilia (Ec), thick smooth muscle layers. Toluidine blue, obj.40x.tion of the vas deferens. Pseudostratified epithelium (Ept) and - tial cells, the main components of this compartment. These samesue, blood components and lymph were vessels, found inand both Leydig morphological cells or intersti study tents. The pampas cat has the vas deferens characterized of Leopardus colocolo as Leopardus tigrinus in a morpho- by a narrow lumen and a thick layer of smooth muscle. functional study by Balarini (2008). Its mucosa is rounded without longitudinal folds and has -
(Fig.4A,B). spacesIn cats, intertubulares; interstitial cellsThey and have Leydig polyhedral cells are shape more with abun lar- a pseudostratified columnar epithelium with stereocilia gedant spherical compared nucleus with andother evident species nucleolus; and substantially the cytoplasm fill the is DISCUSSION acidophilus and contains numerous granules and lipid dro- The testes are paired organs with rounded oval shape, sur- - rounded by a capsule called the tunica albuginea, consisting sent in the pampas cat, which appear in polyhedral shape, of dense modeled connective tissue. In Leopardus colocolo, butplets with (Banks different 1992), sizes, which round resembles and clear the nuclei Leydig and cells evident pre the tunica albuginea appeared thick and consists of dense - mestic cats showing varied dimensions with polyhedral sha- pe,nucleoli. vacuolated Silva etcytoplasm, al. (2009) clear describe nucleus, the nucleolus Leydig cells evident. in do modeled connective tissue with the presence of fibroblasts hisand study large of amount histology of ofcollagen domestic fibers. cats Thistesticles result (Felis is similar catus), cats (age from one day to one year), there are three types of theto the same observations standard of of appearance Diagone (2009), of the which tunica recounts albuginea, in Sanchez et al. (1993) report on a consisted study of 20 which is thick and consists of dense connective tissue rich - sedLeydig chromatin cells. Up and to a lipidmonth, droplets these arein the polyhedral cytoplasm, with the ovoid pe- According to Silva et al. - nucleus; two to five months, the nucleus contains conden in collagen fibers. (2009), domestic cats aged be ritubular with elongated nuclei, and five to six months are Pesq. Vet. Bras. 36(10):1014-1020, outubro 2016 Morphology of the testes and epididymal ducts in the Pampas cat Leopardus colocolo (Molina, 1782)
1019 polygonal and the nucleus is great arranged laterally to the of pampas cat, Oncifelis colocolo, in the Brazilian Cerrado. Mammalia cytoplasm. Data show that different from those found in Le- Balarini M.K. 2008. Morphofunctional Evaluation of Testis and Spermato- opardus colocolo, 68(1):75-79. shape in different sizes and with visibly stained nucleoli. Leopardus tigrinus Schreber, 1775) Adult. The epididymis where in mammals Leydig cells is considered appeared ain very polyhedral impor- genic Process Cat-to-Kill-Small ( Ap- tant segment in extra-testicular sperm via. The maturation Master’s Graduate in Veterinary Medicine, Viçosa, MG. Banks W.J. 1992. Male reproductive system, p.546-556. In: Ibid. (Ed.), and storage of sperm are its main functions. Furthermore, Cossios D., Beltrán Saavedra F.M., Bennett N., Bernal U., Fajardo M., plied Veterinary Histology. Manole, São Paulo. (Apud Diagone 2009) the epididymis provides a “biochemical environment” in Marino C., Napolitano R., which the sperm undergoes morphological and physiolo- Y., C. 2007. Manual gical changes, affecting its functional maturation passing Lucheriniof Methods M.J., for MerinoRelevamientos J., of High Andean Carnivores.Palacios Alianza R., Perovic Gato Ramirez L., Villalba S., Walker Y.C. & Sillero-Zubiri through several regions of the epididymal (Schimming et Andino, Buenos Aires. al. 2002), which can be evidenced by the presence of secre- testicles. Jabo- ting cells. Diagone K.V. 2009. Histology and morphometry of adult domestic cats Faculty of Agricultural and Veterinary Sciences, Unesp, Hoshino et al. (2002) showed, in a morphometric stu- Depart- dy of epididymal ducts of domestic cats, the same pattern ticabal, São Paulo. of cell structures of the Leopardus colocolo epididymal Fajardo U. & Pacheco V. 2011. Species CITES Peruvian Carnivores. epithelium ment of Mammalogy del Museo de Historia Natural, UNMSM, Dirección- . General de Diversidad Biologica, Ministerio del Ambiente, Lima. columnar epithelium, standing on a delicate basement ov, 1858) (Carnivora, Felidae), the systematic and biogeographic review. Garcia-Perea R. 1994. The pampas cat group (Genus Lynchailurus Severtz membrane andThe integratedepididymal by duct myoid showed cells. pseudostratified The epithelium biologyAmerican of theMuseum domestic Novitates cat with 3096:1-36. special reference to endocrinology, sperm and principal cells, different in L. colocolo, which presents Goodrowefunction andK.L., in-vitroHoward fertilization. J.G., Schmidt J. P.M.Reprod. & Wildt Fertility D.E. 1989. Reproductive theshowed principal different and basalcell populations, cells. And the which lumen are: had basal, long apicalstere- 39(Suppl.):73-90. ocilia projecting the principal cells. - In the domestic cat (Felis catus) the terminal part of the Hooker G.W. 1970. The intertubular tissue of the testis, p.483-550. In: Ibid. (Ed.), The Testis Development: anatomy and physiology. Vol.1(8). Aca epididymis continue in the vas deferens where the epithe- Malheiros E.B. 2002. demic Press, New York. - Morphometry of the seminiferous tubules and epididymal ducts of dogs Hoshinoand cats P., fromNakaghi neutering L.S.O., surgery. Pacheco M.R., Lui J.F. & Leopardus colocololial continues) whose to vasbe pseudostratified deferens showed with a thick small layer cell of stereo smoo- Biotemas 15(1):97-110. Leopardus colocolo thcilia muscle, (Diagone a rounded 2009), as mucosa well as thewithout pampas longitudinal cat ( folds Lucherini M., Eizirik E., De Oliveira T., Pereira J. & Wallace R. 2015. . The Downloaded IUCN Red on List April of Threatened Species: e.T15 of stereocilia. 309A50656743
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