bs_bs_banner 80 NEW WORLD PRIMATES: IN SITU AND EX SITU CONSERVATION Int. Zoo Yb. (2012) 46: 80–94 DOI:10.1111/j.1748-1090.2011.00156.x Owl monkeys Aotus spp in the wild and in captivity E. FERNANDEZ-DUQUE Department of Anthropology, University of Pennsylvania, 3260 South Street, Philadelphia, Pennsylvania 19104, USA, and Centro de Ecología Aplicada del Litoral, Ruta Prov.5-km 2,5, Provincia de Corrientes, Argentina E-mail: [email protected] Owl monkeys Aotus spp have the potential to be a great field research with both intellectual and prac- model to accomplish a thorough integration of zoo tical benefits. In fact, given their nocturnality, and field research. Their most salient features are their nocturnal habits, monogamous social organization and small size and arboreality, we will never fully paternal care, features that should make them of interest understand owl monkey biology unless to the public. Following a brief historical perspective on we complement field research with detailed our knowledge of owl monkey biology, I describe in observations and measurements from captive detail, drawing from research with both captive and wild individuals. animals, those aspects that make owl monkeys unusual among primates and mammals. First, owl monkeys are A brief historical perspective on our the only anthropoids with nocturnal habits, and the study knowledge about owl monkey biology is pre- of their remarkable activity patterns has benefited enor- sented, drawing attention to the fact that for mously from an integrated approach that combined field several decades, most of our understanding research with research in semi-natural conditions and the laboratory. Second, up until recently, our understanding came from captive populations and field of social monogamy and the involvement of the ΗΗ demographic studies. Drawing from research in infant care, two defining characteristics of the genus, with both captive and wild animals, the have been primarily informed by studies of captive indi- aspects that make owl monkeys unusual viduals. In the future, a truly integrated laboratory–field among primates and mammals are described approach that focuses on certain areas that cannot be examined in only one or the other setting (e.g. reproduc- in some detail. Then, a few areas of research tive biology, communication, energetics) will offer that offer unique opportunities for synergistic unique opportunities for synergistic interactions between interactions between zoo and field research zoo and field research that will have both intellectual and are focused upon in the final section. practical benefits. Key-words: alloparental care; cathemerality; HISTORICAL PERSPECTIVE ON THE monogamy; nocturnality; pair bonds; paternal care; reproduction; territoriality. STUDY OF OWL MONKEY BIOLOGY Even in the late 1990s, most field data on INTRODUCTION neotropical primates were coming from relatively few genera (Alouatta, Ateles, The most salient features of owl monkeys are Cebus, Leontopithecus, Saimiri) at long-term their nocturnal habits, monogamous social research sites or from studies of one or two organization and intensive paternal care. groups in a single location (e.g. Northern Some of these characteristics should make muriqui Brachyteles hypoxanthus or Tufted them of interest to the public, yet owl capuchin Cebus apella: Strier, 1994; Garber monkeys are rarely displayed in zoos. et al., 2009; Fernandez-Duque et al., in Owl monkeys can become a great model to press). Except for a few isolated cases accomplish a thorough integration of zoo and (Cabrera, 1939; Crile & Quiring, 1940; Park, Int. Zoo Yb. (2012) 46: 80–94 © 2012 The Author. International Zoo Yearbook © 2012 The Zoological Society of London OWL MONKEYS: IN THE WILD AND IN CAPTIVITY 81 1940; Mann, 1956; Hanson & Montagna, et al., 1997). More recently, Aotus was placed 1962; Morrison & Simoes, 1962; Moynihan, in its own separate family Aotidae (Rylands 1964), it is only in the 1970s that the first et al., 2000; Rylands & Mittermeier, 2009). reports of studies specifically conducted with When first described, the genus only owl monkeys appeared in the scientific included a single species Aotus trivirgatus. literature (Erkert, 1976; Thorington et al., Following the discovery of various karyo- 1976; Heltne, 1977; Wright, 1978; Dixson types (Brumback et al., 1971; Brumback, et al., 1979; Hunter et al., 1979). Initially, 1973, 1974; Brumback & Willenborg, 1973; most field studies were primarily focused on Ma et al., 1976, 1978), Hershkovitz (1983) estimates of density, population structure, divided the genus into nine species organized distribution and taxonomy, with little attempt in two groups based on their karyotypes, at examining aspects of behavioural ecology. coloration of the neck and susceptibility to However, 30 years of field research have pro- Plasmodium falciparum, one of the patho- vided a solid understanding of species distri- gens of human malaria. The grey-necked bution. Owl monkeys range from Panamá to group occurs to the north and the red-necked northern Argentina and from the foothills of group to the south of the Amazon River. the Andes to the Atlantic Ocean (Hernández- More recently, extensive and systematic Camacho & Cooper, 1976; Wright, 1981; research using phenotype, karyotype and Hershkovitz, 1983; Hernández-Camacho & molecular data led researchers to recognize Defler, 1985; Zunino et al., 1985; Aquino & up to 11 species (Galbreath, 1983; Mudry de Encarnación, 1988, 1994; García & Tarifa, Pargament et al., 1984; Mudry et al., 1990; 1988; Aquino et al., 1992; Fernandes, 1993; Pieczarka et al., 1993; Torres et al., 1998; Peres, 1993; Ford, 1994; de Sousa e Silva & Rylands et al., 2000; Defler et al., 2001; Nunes, 1995; Kinzey, 1997; Bennett et al., Defler & Bueno, 2003; Plautz et al., 2009; 2001; Barnett et al., 2002; Defler, 2003, Menezes et al., 2010; Babb et al., 2011). 2004; Villavicencio Galindo, 2003; Castaño Although it is no longer tenable to classify all & Cardona, 2005; Cornejo et al., 2008; owl monkey diversity as A. trivirgatus (even Fernandez-Duque, Di Fiore et al., 2008; Mal- if this form of classification should be donado et al., 2010; Pyritz et al., 2010; Ruiz- remembered when evaluating the published Garcia et al., 2010; Svensson et al., 2010). literature), it is imperative that adequate Owl monkeys, also known as night biogeographic, genetic, morphological and monkeys, belong in the genus Aotus. Several behavioural information is obtained and taxonomic issues remain largely unsettled, considered before any taxon is given species including the classification at the family and status. subfamily levels, and the number of recog- Although there were a few short-term nized species and subspecies (Defler & studies in the late 1970s and 1980s, to date, Bueno, 2007). Regarding its suprageneric the behavioural ecology of most species classification, the genus was, for many years, in the genus Aotus has not been thoroughly placed alternatively in the Atelidae or in the studied in the wild. There has been reasonable Cebidae families. Based on morphological population biology and demographic data data, owl monkeys were considered to be about Nancy Ma’s night monkey Aotus nan- closely related to the pithecines within the cymaae and Spix’s night monkey Aotus vocif- atelids (Rosenberger, 1981; Schneider & erans (Aquino & Encarnación, 1986b, 1988, Rosenberger, 1996). A close affinity between 1989, 1994; Aquino et al., 1990, 1992, 1993; owl monkeys and the atelines has also Moya et al., 1990) convincingly showing that been suggested based on dentition (Tejedor, these species are found in small groups with 1998, 2001). However, analysis of molecu- only one breeding pair of adults. A set of lar genetic data led researchers to place the relatively brief studies on Black-headed genus within the cebids (Schneider & Rosen- night monkey Aotus nigriceps, A. vociferans, berger, 1996; Schneider et al., 1996; Porter A. nancymaae and Bolivian night monkey Int. Zoo Yb. (2012) 46: 80–94 © 2012 The Author. International Zoo Yearbook © 2012 The Zoological Society of London 82 NEW WORLD PRIMATES: IN SITU AND EX SITU CONSERVATION Aotus azarai boliviensis provided the first monkey A. a. azarai of the Argentinean and valuable behavioural-ecology data in the Paraguayan Chaco shows peaks of activity 1970s and 1980s (Wright, 1978, 1984, 1985, during the day, as well as during the night 1986, 1994; Aquino & Encarnación, 1986a; (Wright, 1989; Arditi, 1992; Rotundo García & Braza, 1987, 1993; Puertas et al., et al., 2000; Fernandez-Duque et al., 2010; 1992, 1995; Bicca-Marques & Garber, 2004; Fernandez-Duque, 2011). Carretero-Pinzón et al., 2008; Fernandez- The integration of studies from the wild Duque, Di Fiore et al., 2008; Marín-Gómez, and captivity, and from the wild using labo- 2008). Those studies contributed the first ratory technology, has provided an under- quantitative information to confirm the gen- standing of the mechanisms regulating eral nocturnal habits of most species, the cathemerality and nocturnality. The strictly relatively small groups including only one nocturnal Grey-handed night monkey Aotus reproducingΘand the territorial use of space. griseimembra of Colombia was the focus of a Without doubt, the relatively slow pace for series of laboratory experiments analysing learning about the genus, when compared circadian rhythms of locomotor activity, with the impressive progress made in many as well as the regulation of those rhythms by other Neotropical taxa, is because of the light (Erkert,