, Volume 55, Issue 3, pp 393–401 | Cite as

Effect of photoperiod on characteristics of semen obtained by electroejaculation in stump-tailed macaques (Macaca arctoides)

  • Mónica Dafne García Granados
  • Leonor Estela Hernández LópezEmail author
  • Alejandro Córdoba Aguilar
  • Ana Lilia Cerda Molina
  • Olivia Pérez-Ramírez
  • Ricardo Mondragón-Ceballos
Original Article


Some environmental variables determining seasonal reproduction in mammals are temperature, humidity, food availability, and photoperiod. Among these, photoperiod is considered the main regulator of primates’ seasonal reproduction, thus the latitudinal distribution of primate populations is a key factor determining the appearance of seasonal reproduction. The present work presents supporting discrete seasonality in male stump-tailed macaques (Macaca arctoides). We investigated whether semen quality and testosterone covaried with Mexico City’s photoperiod and relative humidity by analyzing variations in the portions that form the ejaculate: the seminal liquid, the seminal coagulum, and the copulatory plug. Five male adult stump-tailed macaques were electroejaculated once a month, obtaining three semen samples per male, from August 2011 to July 2012 (except for December 2011) (n = 165). Our results showed that stump-tailed macaque sperm counts were significantly different between the portions of the ejaculate. The seminal coagulum contained the significantly largest number of spermatozoids, followed by the copulatory plug and the seminal fluid. Photoperiod and relative humidity had major influence on the sperm count in the seminal coagulum and the testosterone concentrations. Testosterone reached its highest values around the time when days and nights lasted the same hours, decreasing when days either grew longer or became shorter. Concerning relative humidity, sperm counts in the seminal coagulum were highly variable on dry days, but decreased as the relative humidity increased. We conclude that stump-tailed macaques have a discrete seasonality, occurring in spring and fall when macaques’ reproductive condition and readiness for postcopulatory intrasexual competition increase.


Macaca arctoides Photoperiod Relative humidity Seasonal reproduction 



This research project was supported by the Instituto Nacional de Psiquiatría Ramón de la Fuente Muñiz. We thank Javier Borráz León and Gema Estudillo for their valuable help with laboratory work. We thank Mrs. Sally Packard for correcting the English version of the manuscript. Concerning experimentation ethics, the Bioethics Committee of the Instituto Nacional de Psiquiatría Ramón de la Fuente Muñiz approved the experimental protocol and animal handling. We also followed the Mexican Official Norm of Technique Specifications for the Production, Care, and Use of Laboratory Animals (NOM-062-ZOO 1999), and the Policy Statement on Use of Primates for Biomedical Purposes, as adopted by the World Health Organization (WHO) and the Ecosystem Conservation Group (ECG).


  1. Altmann J (1974) Observational study of behaviour: sampling methods. Behaviour 49:227–267PubMedCrossRefGoogle Scholar
  2. Anderson DP, Nordheim EV, Boesch C (2006) Environmental factors influencing the seasonality of estrus in chimpanzees. Primates 47:43–50PubMedCrossRefGoogle Scholar
  3. Bauman JE, Kolodny RC, Webster SK (1982) Vaginal organic acids and hormonal changes. Fertil Steril 38:572–579PubMedGoogle Scholar
  4. Bertrand M (1969) The behavioral repertoire of the stumptail macaque: a descriptive and comparative study. Karger, BaselGoogle Scholar
  5. Boskey ER, Cone RA, Whaley KJ, Moench TR (2001) Origins of vaginal acidity: high D/L lactate ratio is consistent with bacteria being the primary source. Hum Reprod 16:1809–1813PubMedCrossRefGoogle Scholar
  6. Boskey ER, Telsch KM, Whaley KJ, Moench TR, Cone RA (1999) Acid production by vaginal flora in vitro is consistent with the rate and extent of vaginal acidification. Infect Immun 67:5170–5175PubMedCentralPubMedGoogle Scholar
  7. Bronson FH (1988) Seasonal regulation of reproduction in mammals. In: Knobil E, Neill JD (eds) The physiology of reproduction. Raven, New York, pp 1831–1873Google Scholar
  8. Cerda-Molina AL, Hernández-López L, Chavira-Ramírez R, Cárdenas M, Mondragón-Ceballos R (2009) Seasonality of LH, testosterone and sperm parameters in spider monkey males (Ateles geoffroyi). Am J Primatol 71:427–431PubMedCrossRefGoogle Scholar
  9. Cerda-Molina AL, Hernández-López L, Páez-Ponce LD, Rojas-Maya S, Mondragón-Ceballos R (2006) Seasonal variations of fecal progesterone and 17β-estradiol in captive female black-handed spider monkeys (Ateles geoffroyi). Theriogenology 66:1985–1993PubMedCrossRefGoogle Scholar
  10. Clewe TH (1969) Observations on reproduction of squirrel monkeys in captivity. J Reprod Fertil 6:151–156Google Scholar
  11. de Waal FBM (1989) Peacemaking among primates. Harvard University Press, CambridgeGoogle Scholar
  12. Devine CM (1977) Copulatory plug restricted mating opportunities and reproductive competition among male garter snakes. Nature 267:245–246CrossRefGoogle Scholar
  13. Di Bitetti MS, Janson CH (2000) When will the stork arrive? Patterns of birth seasonality in Neotropical primates. Am J Primatol 50:109–130PubMedCrossRefGoogle Scholar
  14. Dixson AF, Anderson MJ (2002) Sexual selection, seminal coagulation and copulatory plug formation in primates. Folia Primatol 73:63–69PubMedCrossRefGoogle Scholar
  15. Dixson AF, Anderson MJ (2004) Sexual behavior, reproductive physiology and sperm competition in male mammals. Physiol Behav 83:361–371PubMedCrossRefGoogle Scholar
  16. Donald A, Dewsbury A (1988) A test of the role of copulatory plugs in sperm competition in deer mice (Peromyscus maniculatus). J Mammal 69:854–857CrossRefGoogle Scholar
  17. Dorus S, Evans PD, Wyckoff GJ, Choi SS, Lahn BT (2004) Rate of molecular evolution of the seminal protein gene SEMG2 correlates with levels of female promiscuity. Nat Genet 36:1326–1329PubMedCrossRefGoogle Scholar
  18. Estrada A, Estrada R (1976) Birth and breeding cyclicity in an outdoor living stumptail macaque (Macaca arctoides) group. Primates 17:225–231CrossRefGoogle Scholar
  19. Gammell MP, de Vries H, Jennings DJ, Carlin CM, Hayden TJ (2003) David’s score: a more appropriate dominance ranking method than Clutton-Brock et al’.s index. Anim Behav 66:601–605CrossRefGoogle Scholar
  20. Harvey NC, Rhine RJ (1983) Some reproductive parameters of stumptailed macaques (Macaca arctoides). Primates 24:530–536CrossRefGoogle Scholar
  21. Hastings MH, Roberts AC, Herbert J (1985) Neurotoxic lesions of the anterior hypothalamus disrupt the photoperiodic but not the circadian system of the Syrian hamster. Neuroendocrinol 40:316–324CrossRefGoogle Scholar
  22. Hernández-López L, Cerezo-Parra G, Cerda-Molina AL, Pérez-Bolaños SC, Díaz-Sánchez V, Mondragón-Ceballos R (2002) Sperm quality differences between the rainy and dry seasons in captive black-handed spider monkeys (Ateles geoffroyi). Am J Primatol 57:35–41PubMedCrossRefGoogle Scholar
  23. Hoffmann K, Illnerová H, Vaněček J (1981) Effect of photoperiod and of one minute light at night-time on the pineal rhythm on N-acetyl transferase activity in the Djungarian hamster Phodopus sungorus. Biol Reprod 24:551–556PubMedCrossRefGoogle Scholar
  24. Hrdy SB (1979) Infanticide among animals: a review, classification, and examination of the implications for the reproductive strategies of females. Ethol Sociobiol 1:13–40CrossRefGoogle Scholar
  25. Kanagawa H, Hafez ESE, Nawar MM, Jaszczak S (1972) Patterns of sexual behavior and anatomy of copulatory organs in macaques. Z Tierpsychol 31:449–460PubMedCrossRefGoogle Scholar
  26. Koening A, Borrie C, Chalise MK, Winkler P (1997) Ecology, nutrition, and the timing of reproductive events in an Asian primate, the Hanuman langur (Presbytis entellus). J Zool 243:215–235CrossRefGoogle Scholar
  27. Lancaster JB, Lee RB (1965) The annual reproductive cycle in monkeys and apes. In: DeVore I (ed) Primate behavior: field study of monkeys and apes. Academic, New York, pp 486–513Google Scholar
  28. Lindburg DG (1971) The rhesus monkey in north India: an ecological and behavioral study. In: Rosenblum LA (ed) Primate behavior: developments in field and laboratory research. Academic, New York, pp 1–106CrossRefGoogle Scholar
  29. Lindburg DG (1987) Seasonality of reproduction in primates. In: Erwin J, Mitchell G (eds) Comparative Primate Biology. Alan R. Liss, New York, pp 167–218Google Scholar
  30. MacDonald GJ (1971) Reproductive patterns in three species of macaques. Fertil Steril 22:373–377PubMedGoogle Scholar
  31. Milette JJ, Turek FW (1986) Circadian and photoperiodic effects of brief light pulses in male Djungarian hamsters. Biol Reprod 35:327–335PubMedCrossRefGoogle Scholar
  32. Miller GF (1998) How mate choice shaped human nature: a review of sexual selection and human evolution. In: Crawford C, Krebs D (eds) Handbook of evolutionary psychology: Ideas, issues and applications. Lawrence Erlbaum, New Jersey, pp 87–129Google Scholar
  33. Papka R, Williams S (1998) Vagina. In: Knobil E, Neill JD (eds) Encyclopedia of reproduction. Academic, San Diego, pp 961–968Google Scholar
  34. Parga JA (2003) Plug displacement evidences sperm competition in Lemur catta. Int J Primatol 24:889–899CrossRefGoogle Scholar
  35. Rahaman H, Parthasarathy MD (1969) Studies on the social behavior of bonnet monkeys. Primates 10:149–162CrossRefGoogle Scholar
  36. Roonwal ML, Mohonot SM (1977) Primates of South Asia: ecology, sociobiology and behavior. Harvard University Press, CambridgeCrossRefGoogle Scholar
  37. Slob AK, Ooms MP, Vreeburg JTM (1979) Annual changes in serum testosterone in laboratory housed male stumptail macaques (M. arctoides). Biol Reprod 20:981–984PubMedCrossRefGoogle Scholar
  38. Small M (1993) Female choices: sexual behavior of female primates. Cornell University Press, New YorkGoogle Scholar
  39. Solanki GS, Zothansiama (2012) Male homosexual behavior among different age groups in captive stump-tailed macaque (Macaca arctoides): socio-sexual or sexually motivated? Int Multidiscip Res J 2:22–27Google Scholar
  40. Suarez SS, Pacey AA (2006) Sperm transport in the female reproductive tract. Hum Reprod 12:23–37CrossRefGoogle Scholar
  41. Wicklings EL, Nieschlag E (1980) Seasonality in endocrine and exocrine testicular function of the adult rhesus monkey (Macaca mulatta) maintained in a controlled laboratory environment. Int J Androl 3:87–104CrossRefGoogle Scholar

Copyright information

© Japan Monkey Centre and Springer Japan 2014

Authors and Affiliations

  • Mónica Dafne García Granados
    • 1
  • Leonor Estela Hernández López
    • 1
    Email author
  • Alejandro Córdoba Aguilar
    • 2
  • Ana Lilia Cerda Molina
    • 1
  • Olivia Pérez-Ramírez
    • 1
  • Ricardo Mondragón-Ceballos
    • 1
  1. 1.Departamento de EtologíaInstituto Nacional de Psiquiatría, “Ramón de la Fuente Muñiz”Mexico, D.F.Mexico
  2. 2.Departamento de Ecología Evolutiva, Instituto de EcologíaUniversidad Nacional Autónoma de MéxicoMexico, D.F.Mexico

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