Abstract
The taxonomy of Saimiri is controversial because morphological characteristics, traditionally used for identification, are insufficient to distinguish species and subspecies. Genetic studies of specimens become relevant for captive management, especially considering their frequently unknown geographical origin. We analyzed phenotypic and genetic parameters in Saimiri spp. in Argentinean zoological gardens and biological stations to provide a more accurate taxonomic identification. We studied 27 males and 19 females of Saimiri spp. The cytogenetic analysis in mitotic metaphases corroborated a modal number of 2N = 44, XX/XY, and FN = 75 for males and FN = 76 for females. G- and C-bands, fluorescence in situ hybridization (FISH) and the pelage coloration pattern of all the specimens corresponded to Saimiri boliviensis boliviensis. We characterized for the first time the sperm cell morphology and morphometry (mean ± SE): total length: 71.39 ± 5.40 μm; head length: 5.71 ± 0.81 μm; head width: 3.76 ± 0.70 μm; acrosome length: 3.70 ± 0.82 μm; midpiece length: 12.20 ± 2.22 μm. Researchers can use the characterization of the sperm morphology as another parameter for taxonomic identification that, together with cytogenetic and molecular ones, would allow a more precise identification of individual Saimiri boliviensis boliviensis.
Similar content being viewed by others
References
Abee, C. R. (2000). Squirrel monkey (Saimiri spp.). Research and resources. ILAR Journal, 41, 2–9.
Ascunce, M. S., Hasson, E. R., & Mudry, M. D. (2002). Description of the cytochrome oxidase subunit II gene in some genera of New World monkeys (Primates, Platyrrhini). Genetica, 114, 253–267. doi:10.1023/A:1016230421820.
Ascunce, M. S., Hasson, E. R., & Mudry, M. D. (2003). COII as a useful tool for phylogenetic studies in some genera of New World monkeys (Primates, Platyrrhini). Zoologica Scripta, 32, 397–406. doi:10.1046/j.1463-6409.2003.00123.x.
Ashley, M. V., & Vaughn, J. L. (1995). Owl monkeys (Aotus) are highly divergent in mitochondrial cytochrome c oxidase (COII) sequences. International Journal of Primatology, 16, 793–806. doi:10.1007/BF02735720.
Ayres, J. M. (1985). On a new species of squirrel monkey, genus Saimiri, from Brazilian Amazonia (Primates, Cebidae). Papeis Avulsos de Zoologia, 36, 147–164.
Boinski, S., & Cropp, S. J. (1999). Disparate data sets resolve squirrel monkey (Saimiri) taxonomy: Implications for behavioral ecology and biomedical usage. International Journal of Primatology, 20, 237–256. doi:10.1023/A:1020522519946.
Buckton, K., & Evans, H. (1973). Method for the Analysis of Human Chromosome Aberrations. Ginebra: WHO Publications.
Calamera, J. C. (1992). Introducción al estudio del espermatozoide. Buenos Aires, Argentina: Ediciones Hector Macchi.
Cetica, P. D., & Merani, M. S. (2004). El espermatozoide también tiene su historia. Ciencia Hoy, 14, 10–15.
Cetica, P. D., Solari, A. J., Merani, M. S., De Rosas, J. C., & Burgos, M. H. (1998). Evolutionary sperm morphology and morphometry in armadillos. Journal of Submicroscopic Cytology and Pathology, 30, 309–314.
Collins, A. C., & Dubach, J. M. (2000). Biogeographic and ecological forces responsible for speciation in Ateles. International Journal of Primatology, 21, 421–444. doi:10.1023/A:1005487802312.
Consigliere, S., Stanyon, R., Koehler, U., Arnold, N., & Wienberg, J. (1998). In-situ hybridization (FISH) maps chromosomal homologies between Alouatta belzebul (Platyrrhini, Cebidae) and other primates and reveals extensive interchromosomal rearrangements between howler monkeys genomes. American Journal of Primatology, 46, 119–133. doi:10.1002/(SICI)1098-2345(1998)46:2<119::AID-AJP2>3.0.CO;2-Z
Costello, R. K., Dickinson, C., Rosenberger, A. L., Boinski, S., & Szalay, F. S. (1993). Squirrel monkey (genus Saimiri) taxonomy: A multidisciplinary study of the biology of species. In W. H. Kimbel, & L. B. Martin (Eds.), Species, Species Concepts, and Primate Evolution. New York: Plenum Press.
de Oliveira, E. H. C., Neusser, M., Figueiredo, W. B., Nagamachi, C., Pieczarka, J. C., Sbalqueiro, I. J., Wienberg, J., & Mueller, S. (2002). The phylogeny of howler monkeys (Alouatta, Platyrrhini): Reconstruction by multicolor or cross-species chromosome painting. Chromosome Research, 10, 669–683. doi:10.1023/A:1021520529952.
Du Mond, F. V. (1967). Squirrel monkey reproduction: The “fatted” male phenomenon and seasonal spermatogenesis. Science, 158, 1067–1070. doi:10.1126/science.158.3804.1067.
Figueiredo, W. B., Carvalho-Filho, N. M., Schneider, H., & Sampaio, I. (1998). Mitochondrial DNA sequences and the taxonomic status of Alouatta seniculus populations in northeastern Amazonia. Neotropical Primates, 6, 73–77.
Fogle, T. (1990). Role of cytogenetics for breeding management of squirrel monkey colonies. Zoo Biology, 9, 373–383. doi:10.1002/zoo.1430090505.
Gallardo, M. H., Mondaca, F. C., Ojeda, R. A., Köhler, N., & Garrido, O. (2002). Morphological diversity in the sperms of caviomorph rodents. Mastozoología Neotropical, 9, 159–170.
García, M., Miró, R., Ponsá, M., & Egozcue, J. (1979). Chromosomal polymorphism and somatic segregation in Saimiri sciureus. Folia Primatologica, 31, 312–323. doi:10.1159/000155894.
García, M., Borrel, A., Mudry, M. D., Egozcue, J., & Ponsá, M. (1995). Prometaphase karyotype and restriction-enzyme banding in squirrel monkey, Saimiri boliviensis boliviensis (Primates: Platyrrhini). Journal of Mammalogy, 76, 497–503. doi:10.2307/1382358.
Gomendio, M., Cassinello, J., & Roldan, E. R. S. (2000). A comparative study of ejaculate traits in three endangered ungulates with different levels of inbreeding: fluctuating asymmetry as an indicator of reproductive and genetic stress. Proceedings of the Royal Society B: Biological Sciences, 267(1446), 875–882.
Groves, C. P. (2001). Primate Taxonomy p. 350. Washington and London: Smithsonian Institution Press.
Hedrick, P. W., & Kalinowski, S. T. (2000). Inbreeding depression in conservation biology. Annual Review of Ecology and Systematics, 31, 139–162. doi:10.1146/annurev.ecolsys.31.1.139.
Hershkovitz, P. (1984). Taxonomy of squirrel monkey genus Saimiri (Cebidae, Platyrrhini): A preliminary report with description of a hitherto unnamed form. American Journal of Primatology, 7, 155–210. doi:10.1002/ajp.1350070212.
Horovitz, I., Zardoya, R., & Meyer, A. (1998). Platyrrhine systematics: A simultaneous analysis of molecular and morphological data. American Journal of Physical Anthropology, 106, 261–281. doi:10.1002/(SICI)1096-8644(199807)106:3<261::AID-AJPA1>3.0.CO;2-Q
Howell, W. M., & Black, D. A. (1980). Controlled silver staining of nucleolus organizer regions with a colloidal protective developer: A 1-step method. Experientia, 36, 1014–1015. doi:10.1007/BF01953855.
Kumar, S., Tamura, K., Jakobsen, I. B., & Nei, M. (2001). Mega2: Molecular evolutionary genetics analysis software. Bioinformatics (Oxford, England), 17, 1244–1245. doi:10.1093/bioinformatics/17.12.1244.
Lavergne, A., Catzeflis, F., Lacote, S., Barnaud, A., Bordier, M., Mercereau-Puijalon, O., & Contamin, H. (2003). Genetic analysis of the Saimiri breeding colony of the Pasteur Institute (French Guiana): Development of a molecular typing method using a combination of nuclear and mitochondrial DNA markers. Journal of Medical Primatology, 32, 330–340. doi:10.1046/j.1600-0684.2003.00038.x.
Martinez, R. A., Torres, E., Nieves, M., Szapkievich, V., Rodríguez, S., Schinini, A., Ascurra, M., & Mudry, M. D. (2004). Genetic variability in two captive colonies of Cebus apella paraguayanus (Primates: Platyrrhini) from eastern Paraguay. Caryologia, 57, 332–336.
Meisner, A. D., Klaus, A. V., & O’Leary, M. A. (2005). Sperm head morphology in 36 species of Artiodactylans, Perissodactylans and Cetaceans (Mammalia). Journal of Morphology, 236, 179–202. doi:10.1002/jmor.10297.
Moore, C. M., Harris, C. P., & Abel, C. R. (1990). Distribution of chromosomal polymorphism in 3 subspecies of squirrel monkey (genus Saimiri). Cytogenetics and Cell Genetics, 53, 118–122. doi:10.1159/000132909.
Mudry de Pargament, M. D., Slavustky, I., & Brieux de Salum, S. (1982). Estudios citogenéticos en Saimiri sciureus de Bolivia. Mendeliana, 5, 81–90.
Mudry, M. D., Slavutsky, I., & Labal de Vinuesa, M. (1990). Chromosome comparisons among five species of Platyrrhini (Alouatta caraya, Aotus azarae, Callithrix jacchus, Cebus apella and Saimiri sciureus). Primates, 31, 415–420. doi:10.1007/BF02381112.
Mudry, M. D., Ponsa, M., Borrell, A., Gorostiaga, M., & García, M. (1995). La citogenética en la Taxonomía de los Platirrinos con especial enfasis en cébidos de Argentina y países limítrofes. Marmosiana, 1, 79–86.
Mudry, M. D., Rahn, M. I., & Solari, A. J. (2001). Meiosis and chromosome painting of sex chromosome systems in Ceboidea. American Journal of Primatology, 54, 65–78. doi:10.1002/ajp.1013.
Nieves, M., Steinberg, E. R., Ascunce, M. S., Oklander, L. I., & Mudry, M. D. (2003). Proyecto Primates: Caracterización Genética de Primates en cautiverio. Zool. Latin., 5, 3–6.
Nieves, M., Ascunce, M. S., Rahn, M. I., & Mudry, M. D. (2005). Phylogenetic relationships among some Ateles species: The use of chromosomic and molecular characters. Primates, 46, 155–164. doi:10.1007/s10329-004-0120-x.
Nieves, M., Mendez, G., Ortiz, A., Mühlmann, M., & Mudry, M. D. (2007). Karyological diagnosis of Cebus (Primates, Platyrrhini) in captivity: Detection of hybrids and Management Program Applications. Animal Reproduction Science, in press.
Roldán, E. R. S., Gomendio, M., & Vitullo, A. D. (1992). The evolution of eutherian spermatozoa and underlying selective forces: Female selection and sperm competition. Biological Reviews of the Cambridge Philosophical Society, 67, 551–593. doi:10.1111/j.1469-185X.1992.tb01193.x.
Rowe, N. (1996). The Pictorial Guide to the Living Primates p. 263. East Hampton, NY: Pogonias Press.
Ruvolo, M., Disotell, T. R., Allard, M. W., Brown, W. M., & Honeycutt, R. L. (1991). Resolution of the African hominoid trichotomy by use of a mitochondrial gene sequence. Proceedings of the National Academy of Sciences of the United States of America, 88, 1570–1574. doi:10.1073/pnas.88.4.1570.
Ryland, A. B., Schneider, H., Langguth, A., Mittermeier, R. A., Groves, C. P., & Rodrìguez-Luna, E. (2000). An assessment of the diversity of New World Primates. Neotropical Primates, 8, 61–93.
Schneider, H., Schneider, M. P. C., Sampaio, I., Harada, M. L., Stanhope, M., Czelusniak, J., & Goodman, M. (1993). Molecular phylogeny of the New World Monkeys (Platyrrhini, Primates). Molecular Phylogenetics and Evolution, 2, 225–242. doi:10.1006/mpev.1993.1022.
Schneider, H., Sampaio, I., Harada, M. L., Barroso, C. M. L., Schneider, M. P. C., Czelusniak, J., & Goodman, M. (1996). Molecular phylogeny of the New World Monkeys (Platyrrhini, Primates) based on two unlinked nuclear genes: IRBP intron1 and ɛ-globin sequences. American Journal of Physical Anthropology, 100, 153–179. doi:10.1002/(SICI)1096-8644(199606)100:2<153::AID-AJPA1>3.0.CO;2-Z
Schreiber, A., Wang, M., & Kaumanns, W. (1998). Captive breeding of squirrel monkeys, Saimiri sciureus and Saimiri boliviensis: The problem of hybrid groups. Zoo Biology, 17, 95–109.
Seabright, M. (1971). A rapid banding technique for human chromosomes. Lancet, ii, 971–972. doi:10.1016/S0140-6736(71)90287-X.
Steinberg, E. R., Nieves, M., & Mudry, M. D. (2007). Meiotic characterization and sex determination system of Neotropical Primates: Bolivian squirrel monkey Saimiri boliviensis (Primates: Cebidae). American Journal of Primatology, 69, 1–6. doi:10.1002/ajp.20430.
Sumner, A. T. (1972). A simple technique for demonstrating centromeric heterochromatin. Experimental Cell Research, 75, 304–305. doi:10.1016/0014-4827(72)90558-7.
Szapkievich, V., Martinez, R., & Mudry, M. D. (2002). New World monkeys in Argentinean zoos: Are they useful conservation iussues? Zoocriaderos, 8, 1–11.
Tardif, S., Bales, K., Williams, L., Ludlage Moeller, E., Abbott, D., Schultz-Darken, N., Mendoza, S., Mason, W., Bourgeois, S., & Ruiz, J. (2006). Preparing New World monkeys for laboratory research. ILAR Journal, 47, 307–315.
Thorington, R. W. (1985). The taxonomy and distribution of squirrel monkeys (Saimiri). In L. A. Rosenblum, & C. L. Coe (Eds.), Handbook of Squirrel Monkey Research (pp. 1–33). New York: Plenum Press.
Vandeberg, J. L., Willams-Blangero, S., Moore, C., Cheng, M., & Abee, C. (1990). Genetic relationships among three squirrel monkey types: Implications for taxonomy, biomedical research, and captive breeding. American Journal of Primatology, 22, 101–111. doi:10.1002/ajp.1350220204.
Walsh, P. S., Metzger, D. A., & Higuchi, R. (1991). Chelex® 100 as a medium for simple extraction of DNA for PCR-based typing from forensic material. BioTechnique, 10, 506–513.
Wildt, D. E. (1994). Endangered Species Spermatozoa: Diversity, Research and Conservation in Function of Somatic Cells in the Testis. New York: Springer-Verlag.
Acknowledgments
All research reported here complied with appropriate national and institutional guidelines for the legal acquisition and use of laboratory animals and authorized study of wild animals. The authors adhered to the Guide for Care and Use of Experimental Animals as promulgated by the Canadian Council of Animal Care. We thank the head of the institutions that made possible the genetic studies presented here, the veterinarians who collaborated in the sampling of all specimens, and the caretakers of the subjects. We especially thank C. Galliari (Botanical and Zoological Garden, La Plata, Argentina), G. Zunino (EBCo Breeding Center, Corrientes, Argentina); J. García (CEM Breeding Center, Chaco, Argentina), B. Carpinetti (ECAS Zoological and Breeding Center, La Plata, Argentina), M. Rivolta and M. Mas (Zoo Buenos Aires, Argentina), and G. Solís and A. Burna for their assistance in the management of the subjects, as well as M. Giordano (CITEFA), who provided valuable technical assistance with the ESEM. MDM PIP-CONICET 2450 and 5012, UBACyT X031 and X107, and ERS Sigma Xi 3040277 provided funding for this project.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Steinberg, E.R., Nieves, M., Ascunce, M.S. et al. Morphological and Genetic Characterization of Saimiri boliviensis . Int J Primatol 30, 29–41 (2009). https://doi.org/10.1007/s10764-008-9328-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10764-008-9328-8