Behavioral Ecology and Sociobiology

, Volume 54, Issue 5, pp 431–440 | Cite as

Influences of moonlight, ambient temperature, and food availability on the diurnal and nocturnal activity of owl monkeys (Aotus azarai)

  • Eduardo Fernandez-DuqueEmail author
Original Article


The study of activity rhythms, their potential zeitgebers and masking factors among free-ranging primates has received relatively little attention in the past. Most primates are diurnal, a few of them nocturnal, and even fewer are cathemeral. Owl monkeys (Aotus azarai azarai) regularly show diurnal, as well as nocturnal, activity in the Argentinean and Paraguayan Chaco. The goal of this study was to examine how changes in activity patterns in owl monkeys of Formosa, Argentina are related to daily, monthly, and seasonal changes in temperature, light and food availability . During 1 year, I collected activity data from five groups followed continuously from dawn to dusk, dusk to dawn or uninterruptedly during 24 or 36 h for approximately 1,500 h. I kept hourly and daily records of temperature and light conditions, and I gathered monthly information on the density, distribution and abundance of food resources available to the monkeys. I found that the area of study is highly seasonal, and characterized by significant fluctuations in rainfall, temperature, photoperiod, and food availability. Owl monkeys had on average 5 h of activity during the day and 4 h during the night. The amount of diurnal activity remained fairly constant through the year despite seasonal changes in exogenous factors. Owl monkeys did not show changes in their activity patterns that could be attributed to changes in food availability. Nocturnal activity increased as the amount of moonlight increased, whereas diurnal activity decreased following a full-moon night. Ambient temperature was a good predictor of activity only when the moon was full. These results argue convincingly for an interaction between ambient temperature and moonlight in determining the observed activity pattern. It is then highly advisable that any evaluation of diurnal activity in cathemeral animals be analyzed controlling for the possible effects of moonlight during the previous night.


Activity patterns Primates Cathemerality Aotus Monogamy 



This research was supported by grants to E.F.D. from the L.S.B Leakey Foundation, the Douroucouli Foundation, Dumond Conservancy for Primates and Tropical Forests, and the Argentinean National Council for Scientific and Technological Research (PIP 0051/98, CONICET). I want to thank each of the volunteers and students who made this research possible by spending long hours in the forest: Suzanne Bartholf, Luciano Chaneton, Santiago De Paoli, Kate Maurer, Patricio Ramirez-Llorens, Marcelo Rotundo, Ana Sallenave, Carrie Sloan, Charles Veitch, Emilio White, Gustavo Zurita, as well as all of the Earthwatch and University of California Research Expedition volunteers who collaborated during the preliminary stages of this work. Special thanks go to the managers of Estancia Guaycolec, Mr. Emilio Arauz and Mr. John Adams for their continuous support. I thank Debbie Curtis and Claudia R. Valeggia, for their useful comments on the manuscript. Special gratitude is due to Hans G. Erkert and Horacio de la Iglesia who contributed their vast experience on chronobiology to improve substantially the quality of the manuscript. E.F.D. wrote this manuscript while a Postdoctoral Millennium Fellow at the Center for Reproduction of Endangered Species (Zoological Society of San Diego) and an Assistant Researcher at the CECOAL (Corrientes, Argentina). This study was conducted with full compliance of the current laws of Argentina.


  1. Andrews JR, Birkinshaw CR (1998) A comparison between the daytime and night-time diet, activity and feeding height of the black lemur, Eulemur macaco (Primates: Lemuridae), in Lokobe Forest, Madagascar. Folia Primatol 69:175–182CrossRefGoogle Scholar
  2. Aquino R, Encarnación F (1986) Characteristics and use of sleeping sites in Aotus (Cebidae: Primates) in the Amazon Lowlands of Peru. Am J Primatol 11:319–331Google Scholar
  3. Arditi SI (1992) Variaciones Estacionales en la Actividad y Dieta de Aotus azarae y Alouatta caraya en Formosa, Argentina. Bol Primatol Latinoam 3:11–30Google Scholar
  4. Ashby KR (1972) Patterns of daily activity in mammals. Mammal Rev 1:171–185Google Scholar
  5. Bartness TJ, Albers EH (2000) Activity patterns and the biological clock in mammals. In: Halle S, Stenseth NC (eds) Activity patterns in small mammals. An ecological approach. Springer, Berlin Heidelberg New York, pp 23–47Google Scholar
  6. Brooks DM (1996) Some observations of primates in Paraguay. Neotrop Primates 4Google Scholar
  7. Brown AD, Zunino GE (1994) Hábitat, Densidad y Problemas de Conservación de los Primates en Argentina. Vida Silvest Neotrop 3:30–40Google Scholar
  8. Brown AD, Placci LG, Grau NR (1993) Ecología y Diversidad de las Selvas Subtropicales de la Argentina. In: Goin F, Goni R (eds) Elementos de Política Ambiental. Di Giovanni Grafica, La Plata, pp 215–222Google Scholar
  9. Colquhoun IC (1993) The socioecology of Eulemur macaco: a preliminary report. In: Kappeler PM, Ganzhorn JU (eds) Lemur social systems and their ecological basis. Plenum, New York, pp 11–23Google Scholar
  10. Curtis DJ (1997) Social structure and seasonal variation in the behaviour of Eulemur mongoz. Folia Primatol 70:79–96CrossRefGoogle Scholar
  11. Curtis DJ, Rasmussen MA (2002) Cathemerality in lemurs. Evol Anthropol 1 [Suppl]:83–86Google Scholar
  12. Curtis DJ, Zaramody A, Martin RD (1999) Cathemerality in the mongoose lemur, Eulemur mongoz. Am J Primatol 47:279–298CrossRefPubMedGoogle Scholar
  13. Daan S, Aschoff J (1982) Circadian contributions to survival. In: Aschoff J, Daan S, Groos G (eds) Vertebrate circadian systems. Structure and physiology. Springer, Berlin Heidelberg New York, pp 305–321Google Scholar
  14. Daly M, Behrends PR, Wilson MI (2000) Activity patterns of kangaroo rats. Granivores in a desert habitat. In: Halle S, Stenseth NC (eds) Activity patterns in small mammals. Springer, Berlin Heidelberg New York, pp 145–158Google Scholar
  15. Donati G, Lunardini A, Kappeler PM, Borgognini Tarli SM (2001) Nocturnal activity in the cathemeral red-fronted lemur (Eulemur fulvus rufus), with observations during a lunar eclipse. Am J Primatol 53:69–78CrossRefPubMedGoogle Scholar
  16. Engqvist A, Richard A (1991) Diet as a possible determinant of cathemeral activity patterns in primates. Folia Primatol 57:169–172PubMedGoogle Scholar
  17. Erkert HG (1974) Der einflub des mondlichtes auf die aktivitatsperiodik nachtaktiver saugetiere. Oecologia 14:269–287Google Scholar
  18. Erkert HG (1976) Lunarperiodic variation of the phase-angle difference in nocturnal animals under natural zeitgeber-conditions near the Equator. Int J Chronobiol 4:125–138PubMedGoogle Scholar
  19. Erkert HG (1989) Lighting requirements of nocturnal primates in captivity: a chronobiological approach. Zool Biol 8:179–191Google Scholar
  20. Erkert HG (1991) Influence of ambient temperature on circadian rhythms in Colombian owl monkeys, Aotus lemurinus griseimembra. In: Akivoshi E et al. (eds) Primatology today. Elsevier, Amsterdam, pp 435–438Google Scholar
  21. Erkert HG (2000) Bats. Flying nocturnal mammals. In: Halle S, Stenseth NC (eds) Activity patterns in small mammals. Springer, Berlin Heidelberg New York, pp 253–272Google Scholar
  22. Erkert HG, Grober J (1986) Direct modulation of activity and body temperature of owl monkeys (Aotus lemurinus griseimembra) by low light intensities. Folia Primatol 47:171–188PubMedGoogle Scholar
  23. Erkert HG, Thiemann-Jager A (1983) Dark switch in the entrainment of circadian activity rhythms in night monkeys, Aotus trivirgatus Humboldt. Comp Biochem Physiol 74A:307–310Google Scholar
  24. Fernandes MEB (1993) New field records of night monkeys, genus Aotus, in northern Brazil. Neotrop Primates 1:6–7Google Scholar
  25. Fernandez-Duque E, Bravo S (1997) Population genetics and conservation of owl monkeys (Aotus azarai) in Argentina: a promising field site. Neotrop Primates 5:48–50Google Scholar
  26. Fernandez-Duque E, Rotundo M, Sloan C (2001) Density and population structure of owl monkeys (Aotus azarai) in the Argentinean Chaco. Am J Primatol 53:99–108CrossRefPubMedGoogle Scholar
  27. Fernandez-Duque E, Rotundo M, Ramírez-Llorens P (2002) Environmental determinants of birth seasonality in owl monkeys (Aotus azarai) of the Argentinean Chaco. Int J Primatol 23:639–656CrossRefGoogle Scholar
  28. Ganzhorn JU, Wright PC (1994) Temporal patterns in primate leaf eating: the possible role of leaf chemistry. Folia Primatol 63:203–208PubMedGoogle Scholar
  29. García JE, Braza F (1987) Activity rhythms and use of space of a group of Aotus azarae in Bolivia during the rainy season. Primates 28:337–342Google Scholar
  30. Halle S (1995) Effect of extrinsic factors on activity of root voles, Microtus eoconomus. J Mammal 76:88–99Google Scholar
  31. Halle S (2000) Voles—small graminivores with polyphasic patterns. In: Halle S, Stenseth NC (eds) Activity patterns in small mammals. An ecological approach. Springer, Berlin Heidelberg New York, pp 191–215Google Scholar
  32. Halle S, Stenseth NC (1994) Microtine ultradian rhythm of activity: an evaluation of different hypotheses on the triggering mechanisms. Mammal Rev 24:17–39Google Scholar
  33. Halle S, Stenseth NC (2000) Activity patterns in small mammals. Springer, Berlin Heidelberg New YorkGoogle Scholar
  34. Le Maho Y, Goffart M, Rochas A, Felbabel H, Chatonnet J (1981) Thermoregulation in the only nocturnal simian: the night monkey Aotus trivirgatus. Am J Physiol 240:R156–165PubMedGoogle Scholar
  35. Mann GF (1956) Efecto del frío en mamíferos amazónicos. Invest Zool Chil III:155Google Scholar
  36. Marques MD, Waterhouse JM (1994) Masking and the evolution of circadian rhythmicity. Chronobiol Int 11:146–155PubMedGoogle Scholar
  37. Merritt JF, Vessey SH (2000) Shrews: small insectivores with polyphasic patterns. In: Halle S, Stenseth NC (eds) Activity patterns in small mammals. An ecological approach. Springer, Berlin Heidelberg New York, pp 235–252Google Scholar
  38. Morland HS (1993) Seasonal behavorial variation and its relationship to thermoregulation in ruffed lemurs. In: Kappeler PM, Ganzhorn JU (eds) Lemur social systems and their ecological basis. Plenum, New York, pp 193–203Google Scholar
  39. Morrison P, Simoes J (1962) Body temperatures in two Brazilian primate. Zoologia 24:167–178Google Scholar
  40. Mrosovsky N (1999) Masking: history, definitions, and measurement. Chronobiol Int 16:415–429PubMedGoogle Scholar
  41. Overdorff DJ (1996) Ecological correlates to activity and habitat use of two prosimian primates: Eulemur rubriventer and Eulemur fulvus rufus in Madagascar. Am J Primatol 40:327–342CrossRefGoogle Scholar
  42. Overdorff DJ, Rasmussen MA (1995) Determinants of nightime activity in "diurnal" lemurid primates. In: Alterman L (eds) Creatures of the dark: the nocturnal prosimians. Plenum, New York, pp 61–74Google Scholar
  43. Perrigo G (1987) Breeding and feeding strategies in deer mice and house mice when females are challenged to work for their food. Anim Behav 35:1298–1316Google Scholar
  44. Perrigo G (1990) Food, sex, time, and effort in a small mammal: energy allocation strategies for survival and reproduction. Behavior 114:191–205Google Scholar
  45. Rappold I, Erkert HG (1994) Re-entrainment, phase-response and range of entrainment of circadian rhythms in owl monkeys (Aotus lemurinus g.) of different age. Biol Rhythm Res 25:133–152Google Scholar
  46. Rauth-Widmann B, Thiemann-Jager A, Erkert HG (1991) Significance of nonparametric light effects in entrainment of circadian rhythms in owl monkeys (Aotus lemurinus griseimembra) by light-dark cycles. Chronobiol Int 8:251–266PubMedGoogle Scholar
  47. Rietvedl WJ, Minors DS, Waterhouse JM (1993) Circadian rhythms and masking: an overview. Chronobiol Int 10:306–312PubMedGoogle Scholar
  48. Rotundo M, Sloan C, Fernandez-Duque E (2000) Cambios Estacionales en el Ritmo de Actividad del Mono Mirikiná (Aotus azarai) en Formosa Argentina. In: Cabrera E, Mércolli C, Resquin R (eds) Manejo de Fauna Silvestre en Amazonía y Latinoamérica, Asunción, pp 413–417Google Scholar
  49. Schaik CP van, Kappeler PM (1993) Life history, activity period and lemur social systems. In: Kappeler PM, Ganzhorn JU (eds) Lemur social systems and their ecological basis. Plenum, New York, pp 241–260Google Scholar
  50. Schaik CP van, Kappeler PM (1996) The social systems of gregarious lemurs: lack of convergence with Anthropoids due to evolutionary disequilibrium? Ethology 102:915–941Google Scholar
  51. Smythe N (1997) The seasonal abundance of night-flying insects in a Neotropical forest. In: Leigh EGJ, Rand SA. Windsor DM (eds) The ecology of a tropical forest. Seasonal rhythms and long-term changes. Smithonian Institution Press, Washington, DC, pp 309–318Google Scholar
  52. Stallings JR, West L, Hahn W, Gamarra I (1989) Primates and their relation to habitat in the Paraguayan Chaco. In: Redford KH, Eisenberg JF (eds) Advances in neotropical mammalogy. Sandhill Crane, Gainesville, Fl, pp 425–442Google Scholar
  53. Tattersall I (1987) Cathemeral activity in primates: a definition. Folia Primatol 49:200–202Google Scholar
  54. Wallace RB, Painter LE, Taber AB (1998) Primate diversity, habitat preferences, and population density estimates in Noel Kempff Mercado National Park, Santa Cruz Department, Bolivia. Am J Primatol 46:197–211CrossRefPubMedGoogle Scholar
  55. Warren RD, Crompton RH (1997) A comparative study of the ranging behaviour, activity rhythms and sociality of Lepilemur edwardsi (Primates, Lepilemuridae) and Avahi occidentalis (Primates, Indriidae) at Ampijoroa, Madagascar. J Zool Lond 243:397–415Google Scholar
  56. Wauters LA (2000) Squirrels—medium-sized granivores in woodland habitats. In: Halle S, Stenseth NC (eds) Activity patterns in small mammals. Springer, Berlin Heidelberg New York, pp 131–144Google Scholar
  57. Wright PC (1978) Home range, activity patterns, and agonistic encounters of a group of night monkeys (Aotus trivirgatus) in Peru. Folia Primatol 29:43–55PubMedGoogle Scholar
  58. Wright PC (1985) The costs and benefits of nocturnality for Aotus trivirgatus (the night monkey). City University of New YorkGoogle Scholar
  59. Wright PC (1989) The nocturnal primate niche in the New World. J Hum Evol 18:635–658Google Scholar
  60. Wright PC (1999) Lemur traits and Madagascar ecology: coping with an island environment. Yearb Phys Anthropol 42:31–72CrossRefGoogle Scholar
  61. Zielinski WJ (2000) Weasels and martens. Carnivores in northern latitudes. In: Halle S, Stenseth NC (eds) Activity patterns in small mammals. Springer, Berlin Heidelberg New York, pp 95–118Google Scholar

Copyright information

© Springer-Verlag 2003

Authors and Affiliations

  1. 1.Center for Reproduction of Endangered SpeciesSan Diego ZooSan DiegoUSA

Personalised recommendations