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Morphologic analysis of sperm from two neotropical primate species: comparisons between the squirrel monkeys Saimiri collinsi and Saimiri vanzolinii

Published online by Cambridge University Press:  16 January 2017

Wlaisa V. Sampaio
Affiliation:
Laboratory of Wild Animal Biology and Medicine, Faculty of Veterinary Medicine, Federal University of Pará, Castanhal, Pará, Brazil. Institute of Sustainable Development Mamirauá, Tefé, Amazonas, Brazil.
Karol G. Oliveira
Affiliation:
Laboratory of Wild Animal Biology and Medicine, Faculty of Veterinary Medicine, Federal University of Pará, Castanhal, Pará, Brazil. National Primate Center, Ananindeua, Pará, Brazil.
Danuza L. Leão
Affiliation:
National Primate Center, Ananindeua, Pará, Brazil.
Maria C. Caldas-Bussiere
Affiliation:
Laboratory of Animal Reproduction and Breeding, State University of Norte Fluminense ‘Darcy Ribeiro,’ Campos dos Goytacazes, Rio de Janeiro, Brazil.
Helder L. Queiroz
Affiliation:
Institute of Sustainable Development Mamirauá, Tefé, Amazonas, Brazil.
Fernanda P. Paim
Affiliation:
Institute of Sustainable Development Mamirauá, Tefé, Amazonas, Brazil.
Regiane R. Santos*
Affiliation:
Faculty of Veterinary Medicine, Federal University of Pará, Laboratory of Wild Animal Biology and Medicine, BR 316 Km 61, CEP 68740–970, Castanhal, Pará, Brazil.
Sheyla F.S. Domingues
Affiliation:
Laboratory of Wild Animal Biology and Medicine, Faculty of Veterinary Medicine, Federal University of Pará, Castanhal, Pará, Brazil.
*
All correspondence to: Regiane R Santos. Faculty of Veterinary Medicine, Federal University of Pará, Laboratory of Wild Animal Biology and Medicine, BR 316 Km 61, CEP 68740–970, Castanhal, Pará, Brazil. Tel.: +55 91 33114707. E-mail: R.Rodriguesdossantos@pq.cnpq.br

Summary

Sperm morphometry can be applied to identify different animal groups and species and to evaluate sperm quality. Furthermore, knowledge on species-specific differences will help to enhance biological information, as well as to develop efficient reproductive technologies. The aims in the present study were to describe sperm morphometry from the recently characterized species S. collinsi and S. vanzolinii, to verify if the morphometric sperm patterns are similar or different between both species, and to determine if the sperm morphometry is affected by the levels of sperm defects using the S. collinsi as a model. Semen was collected from S. collinsi (n = 10) and S. vanzolinii (n = 2) monkeys, and sperm was submitted to morphological analysis. From the 10 samples from S. collinsi, five presented sperm of poor quality and two subgroups were formed for this species, i.e. high and poor quality sperm. Data on sperm motility and vigour were analysed, as well morphometric parameters on sperm head and tail. It was observed the normal morphometry was correlated with high quality sperm. Poor quality sperm presented smaller and 7% more ellipticity in their head, when compared with high quality sperm. Sperm from S. vanzolinii presented larger head than those from S. collinsi, but tail lengths were similar. Sperm morphometry can be used as a complementary tool to predict sperm motility and vigour for the S. collinsi species, and S. collinsi appear as a suitable model for S. vanzolinii.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2017 

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References

Andrabi, S.M.H. & Maxwell, W.M.C. (2007). A review on reproductive biotechnologies for conservation of endangered mammalian species. Anim. Reprod. Sci. 99, 223–43.CrossRefGoogle ScholarPubMed
Beletti, M.E., Costa, L.F. & Guardieiro, M.M. (2002). Morphometric features and chromatin condensation abnormalities evaluated by toluidine blue staining in bull spermatozoa. Braz. J. Morphol. Sci. 22, 8590.Google Scholar
Bennett, J. P. (1967). Semen collection in the squirrel monkey. J Reprod. Fertil. 13, 353–5.CrossRefGoogle ScholarPubMed
Bloom, E. (1973). The ultrastructure of some characteristic sperm defects and a proposal for a new classification of the bull spermogram. Nord. Vet. 25, 8391.Google Scholar
Cummins, J. M. & Woodall, P. F. (1985). On mammalian sperm dimensions. J. Reprod. Fertil. 75, 153–75.CrossRefGoogle ScholarPubMed
Dong, Q., Rodenburg, S.E., Huang, C. & VandeVoort, C.A. (2008). Cryopreservation of rhesus monkey (Macaca mulatta) epididymal spermatozoa before and after refrigerated storage. J. Androl. 29, 283–92.CrossRefGoogle ScholarPubMed
Gage, M.J. (1998). Mammalian sperm morphometry. Proc. Roy. Soc. Lond. B: J. Bio. Sci. 265, 97103.Google Scholar
Gage, M.J.G. & Freckleton, R.P. (2003). Relative testis size and sperm morphometry across mammals: no evidence for an association between sperm competition and sperm length. Proc. R. Soc. Lond. B. 270, 625–32.CrossRefGoogle ScholarPubMed
García, D.A., Montiel, J.L.C., Pérez, O.H., Pichardo, E.M., Reza, F.A.C. & García, R.A. (2003). Estudio comparativo de los testículos, epidídimos,glândulas sexuales accesorias y espermatozoides em tres especiesde lagomorfos (Romerolagos diazi, Lepus californicus y Oryctolagus cuniculus). Acta. Zool. Mex. 88, 257–69.Google Scholar
Gomendio, M. & Roldan, E.R.S. (1991). Sperm competition influences sperm size in mammals. Proc. R. Soc. Lond. B: Biol. Sci. 243, 181185.Google ScholarPubMed
Gomendio, M. & Roldan, E.R.S. (1993). Coevolution between male ejaculates and female reproductive biology in eutherian mammals. Proc. R. Soc. Lond. B: Biol. Sci. 252, 712.Google Scholar
Gomendio, M. & Roldan, E.R.S. (2008). Implications of diversity in sperm size and function for sperm competition and fertility. Int. J. Dev. Biol. 52, 439.Google Scholar
Gould, K.G. & Martin, D.E. (1978). Comparative morphology of primate spermatozoa using scanning electron microscopy. II. Families Cercopithecidae, Lorisidae, Lemuridae . J. Hum. Evol. 7, 637–42.CrossRefGoogle Scholar
Humphries, S., Evans, J.P. & Simmons, L.W. (2008). Sperm competition: linking form to function. BMC Evol. Biol. 8, 319.CrossRefGoogle ScholarPubMed
IUCN, 2016. IUCN Red List of Threatened Species, Version 2011.2. Diponible in: https://doi.org/10.2305/IUCN.UK.2008.RLTS.T19839A9023022.en Downloaded on 03 May 2016.Google Scholar
Izar, P., Stone, A., Carnegie, S. & Nakai, E.S. (2009). Sexual selection, female choice and mating systems. In South American Primates: Comparative Perspectives in the Study of Behavior, Ecology and Conservation (Garber, P.A., Estrada, A., Bicca-Marques, J.C., Heymann, E.W. & Strier, K.B. eds). Series Developments in Primatology: Progress and Prospects. University of Chicago. Springer. New York, pp. 175–89.Google Scholar
Laverde, H.J., Medina, V.M. & Casallas, C.P.E. (2001). Contribución al conocimiento de las características semifinales del mono ardilla Saimiri sciureus. Universidade de los Lianos-Escuela de Medicina Veterinaria y Zootecnia Villaavivencio- Colômbia, 2001.Google Scholar
Lynch Alfaro, J.W.L., Boubli, J.P., Paim, F.P., Ribas, C.C., Silva, M.N.F., Messias, M.R., Rohe, F., Merces, M.P., Silva Junior, J.S., Silva, C.R., Pinho, G.M., Koshkarian, G., Nguyen, M.T., Harada, M.L., Rabelo, R.M., Queiroz, H.L., Alfaro, M.E. & Farias, I.P. (2015). Biogeography of squirrel monkeys (genus Saimiri): South-central Amazon origin and rapid pan-Amazonian diversification of a lowland primate. Mol. Phylogenet. Evol. 82, 436–54.Google Scholar
Maree, L., Du Plessis, S.S., Menkveld, R. & Van der Horst, G. (2010). Morphometric dimensions of the human sperm head depend on the staining method used. Hum. Reprod. 25, 1369–82.CrossRefGoogle ScholarPubMed
Martí, J.I., Aparicio, I.M. & García-Herreros, M. (2011). Sperm morphometric subpopulations are differentially distributed in rams with different maturity age in cryopreserved ejaculates. Theriogenology 76, 97109.Google Scholar
Martin, D.E., Gould, K.G. & Warner, H. (1975). Comparative morphology of primate spermatozoa using scanning electron microscopy. I. Families Hominidae, Pongidae, Cercopithecidae and Cebidae . J. Hum. Evol. 4, 287–92.Google Scholar
Mercês, M.P., Alfaro, J.W.L., Ferreira, W.A., Harada, M.L. & Júnior, J.S.S. (2015). Morphology and mitochondrial phylogenetics reveal that the Amazon River separates two eastern squirrel monkey species: Saimiri sciureus and S. collinsi . Mol. Phylogenet. Evol. 82, 426–35.CrossRefGoogle ScholarPubMed
Micklem, K. & Sanderson, J. (2001). Digital imaging in pathology. Curr. Diagn. Pathol. 7, 131–40.CrossRefGoogle Scholar
Moore, H.D.M., Hartman, T.D. & Holt, W.V. (1984). The structure and epididymal maturation of the spermatozoon of the common marmoset (Callithrix jacchus). J. Anat. 138, 227–35.Google Scholar
Nakazato, C., Yoshizawa, M., Isobe, K., Kusakabe, K.T., Kuraishi, T., Hattori, S., Matsumoto, H., Fukui, E., Kuwahata, A., Ochi, M., Kiso, Y. & Kai, C. (2015). Morphological characterization of spermatozoa of the night monkey. J. Mamm. Ova. Res. 32, 3740.Google Scholar
Oliveira, K.G., Leão, D.L., Almeida, D.V.C., Santos, R.R. & Domingues, S.F.S. (2015). Seminal characteristics and cryopreservation of sperm from the squirrel monkey, Saimiri collinsi. Theriogenology 84, 743–9.CrossRefGoogle ScholarPubMed
Oliveira, K.G., Santos, R.R., Leão, D.L., Brito, A.B., Lima, J.S., Sampaio, W.V. & Domingues, S.F.S. (2016a). Cooling and freezing of sperm from captive, free-living and endangered squirrel monkey species. Cryobiology 72, 283–9.Google Scholar
Oliveira, K.G., Santos, R.R., Leão, D.L., Queiroz, H.L., Paim, F.P., Vianez-Júnior, J.L. S.G. & Domingues, S.F.S. (2016b). Testicular biometry and semen characteristics in captive and wild squirrel monkey species (Saimiri sp.). Theriogenology 86, 879–87.Google Scholar
Paglia, A.P., da Fonseca, G.A., Rylands, A.B., Herrmann, G., Aguiar, L.M.S., Chiarello, A.G., Leite, Y.L.R., Costa, L.P., Siciliano, S., Kierulff, M.C.M., Mendes, S.L., Tavares, V. da C., Mittermeier, R.A. & Patton, J.L. (2012). Annotated checklist of Brazilian mammals. Occasion. Papers Conserv. Biol. 6, 176.Google Scholar
Paim, F.P. & Rabelo, R. (2015). Methods for capturing wild squirrel monkeys in a floodplain forest: a comparison of two techniques and two species. Neotrop. Primates. 22, 711.CrossRefGoogle Scholar
Paim, F.P., Valsecchi, J., Harada, M.L. & Queiroz, H.L. (2013). Diversity, geographic distribution and conservation of squirrel monkeys, Saimiri (Primates, Cebidae), in the flood plain forests of Central Amazon. Int. J. Primatol. 34, 1055–76.Google Scholar
Phetudomsinsuk, K., Sirinarumitr, K., Laikul, A. & Pinyopummin, A. (2008). Morphology and head morphometric characters of sperm in Thai native crossbred stallions. Acta Vet. Scand. 50, 41.Google Scholar
Rylands, A.B., Mittermeier, R.A. & Silva, J.S. (2012). Neotropical primates: taxonomy and recently described species and subspecies. Int. Zoo Yearbook. 46, 1124.CrossRefGoogle Scholar
Saacke, R.G. (2008). Sperm morphology: Its relevance to compensable and uncompensable traits in semen. Theriogenology. 70, 473–78.Google Scholar
Sailer, B.L., Lorna, K.J. & Donald, P.E. (1996). Bull sperm head morphometry related to abnormal chromatin structure and fertility. Cytometry. 24, 167–73.3.0.CO;2-G>CrossRefGoogle ScholarPubMed
Simmons, L.W. & Fitzpatrick, J.L. (2012). Sperm wars and the evolution of male fertility. Reproduction. 144, 519–34.Google Scholar
Smith, B.H. (1989). Dental development as a measure of life history in primates. Evolution 43, 683–8.Google Scholar
Sousa, P.C., Santos, E.A.A., Bezerra, J.A.B., Lima, G.L., Castelo, T.S., Fontenele-Neto, J.D. & Silva, A.R. (2013). Morphology, morphometry and ultrastructure of captive six-banded armadillo (Euphractus sexcinctus) sperm. Anim. Reprod. Sci. 140, 279–85.CrossRefGoogle ScholarPubMed
Steinberg, E.R., Nieves, M., Ascunce, M.S., Palermo, A.M. & Mudry, M.D. (2009). Morphological and genetic characterization of Saimiri boliviensis . Int. J. Primatol. 30, 2941.Google Scholar
Swanson, W.F., Valle, R.R., Carvalho, F.M., Arakaki, P.R., Rodas-Martínez, A.Z., Muniz, J.A.P.C. & García-Herreros, M. (2016). Sperm morphology assessment in captive neotropical primates. Reprod. Dom. Anim. 51, 623–7.Google Scholar
Tourmente, M., Gomendio, M. & Roldan, E.R. (2011). Sperm competition and the evolution of sperm design in mammals. BMC Evol. Biol. 11, 12.Google Scholar
Valle, R.D.R., Nayudu, P.L., Leal, C.L.V. & Garcia-Herreros, M. (2012). Sperm head morphometry in ejaculates of adult marmosets (Callithrix jacchus): a model for studying sperm subpopulations and among-donor variations. Theriogenology, 78, 1152–65.Google Scholar
Valle, R.R., Arakaki, P.R., Carvalho, F.M., Muniz, J.A.P.C., Leal, C.L.V. & García-Herreros, M. (2013a). Identification of sperm head subpopulations with defined pleiomorphic characteristics in ejaculates of captive Goeldi's monkeys (Callimico goeldii). Anim. Reprod. Sci. 137, 93102.Google Scholar
Valle, R.R., Carvalho, F.M., Muniz, J.A.P.C., Leal, C.L.V. & García-Herreros, M. (2013b). Differential distribution of sperm subpopulations and incidence of pleiomorphisms in ejaculates of captive howling monkeys (Alouatta caraya). Naturwissenschaften. 100, 923–33.Google Scholar
Yániz, J.L., Soler, C. & Santolaria, P. (2015). Computer assisted sperm morphometry in mammals: a review. Anim. Reprod. Sci. 156, 112.CrossRefGoogle ScholarPubMed