Eduardo Fernandez-Duque

Impending extinction crisis of the world's primates: why primates matter

Impending extinction of the world’s primates due to human activities; immediate global attention is needed to reverse the trend. Nonhuman primates, our closest biological relatives, play important roles in the livelihoods, cultures, and religions of many societies and offer unique insights into human evolution, biology, behavior, and the threat of emerging diseases. They are an essential component of tropical biodiversity, contributing to forest regeneration and ecosystem health. Current information shows the existence of 504 species in 79 genera distributed in the Neotropics, mainland Africa, Madagascar, and Asia. Alarmingly, ~60% of primate species are now threatened with extinction and ~75% have declining populations. This situation is the result of escalating anthropogenic pressures on primates and their habitats—mainly global and local market demands, leading to extensive habitat loss through the expansion of industrial agriculture, large-scale cattle ranching, logging, oil and gas drilling, mining, dam building, and the construction of new road networks in primate range regions. Other important drivers are increased bushmeat hunting and the illegal trade of primates as pets and primate body parts, along with emerging threats, such as climate change and anthroponotic diseases. Often, these pressures act in synergy, exacerbating primate population declines. Given that primate range regions overlap extensively with a large, and rapidly growing, human population characterized by high levels of poverty, global attention is needed immediately to reverse the looming risk of primate extinctions and to attend to local human needs in sustainable ways. Raising global scientific and public awareness of the plight of the world’s primates and the costs of their loss to ecosystem health and human society is imperative.

Access to Electric Light Is Associated with Shorter Sleep Duration in a Traditionally Hunter-Gatherer Community

Access to electric light might have shifted the ancestral timing and duration of human sleep. To test this hypothesis, we studied two communities of the historically hunter-gatherer indigenous Toba/Qom in the Argentinean Chaco. These communities share the same ethnic and sociocultural background, but one has free access to electricity while the other relies exclusively on natural light. We fitted participants in each community with wrist activity data loggers to assess their sleep-wake cycles during one week in the summer and one week in the winter. During the summer, participants with access to electricity had a tendency to a shorter daily sleep bout (43 ± 21 min) than those living under natural light conditions. This difference was due to a later daily bedtime and sleep onset in the community with electricity, but a similar sleep offset and rise time in both communities. In the winter, participants without access to electricity slept longer (56 ± 17 min) than those with access to electricity, and this was also related to earlier bedtimes and sleep onsets than participants in the community with electricity. In both communities, daily sleep duration was longer during the winter than during the summer. Our field study supports the notion that access to inexpensive sources of artificial light and the ability to create artificially lit environments must have been key factors in reducing sleep in industrialized human societies.

Demography and life history of wild red titi monkeys (Callicebus discolor) and equatorial sakis (Pithecia aequatorialis) in Amazonian Ecuador: A 12-year study

We investigated demographic patterns and life history traits from several groups of red titi monkeys (Callicebus discolor) and equatorial sakis (Pithecia aequatorialis) monitored throughout the first 12 years (November 2003 through May 2015) of an ongoing research project in the Yasuní National Park and Biosphere Reserve, Ecuador. The saki groups ranged in size between two and six individuals, comprising either one adult male and one adult female or multiple adult‐sized males or females, plus immatures. Deviations from a pair‐living structure resulted when two different daughters of the resident female grew up and successfully reproduced in their natal group and when an adult‐sized male temporarily immigrated into the group when it already contained an adult male. The titi groups also ranged in size between two and six individuals, but almost exclusively lived in groups with one adult individual of each sex. No titi offspring were observed to breed in their natal groups, and both male and female offspring dispersed when they were between 2.1 and 5.0 years old. In both titi and saki groups, vacant breeding positions resulting from the disappearance of an adult group member were promptly occupied by immigrants of the same sex as the disappeared group member. We recorded nine saki and 28 titi births. Eighty‐three percent of the titi births occurred between September and January, suggesting reproductive seasonality. The mean interbirth interval after an infant survived its first 6 months was 21.3 ± SE 1.9 months (N = 3) for sakis and 14.5 ± SE 1.5 months (N = 14) for titis. Saki infant survival was 70%, and juvenile survival 57%. Titi infant survival was 88%, and juvenile survival was 53%. This 12‐year study provides important insights into the functioning and maintenance of pair‐living and social monogamy in two little‐known platyrrhine species. Am. J. Primatol. 78:204–215, 2016.

Social monogamy in wild owl monkeys (Aotus azarae) of Argentina: the potential influences of resource distribution and ranging patterns

Using published and new data from a population of monogamous owl monkeys in the Argentinean Chaco, I examine the hypothesis that social monogamy is a default social system imposed upon males because the spatial and/or temporal distribution of resources and females makes it difficult for a single male to defend access to more than one mate. First, I examine a set of predictions on ranging patterns, use of space, and population density. This first section is followed by a second one considering predictions related to the abundance and distribution of food. Finally, I conclude with a section attempting to link the ranging and ecological data to demographic and life‐history parameters as proxies for reproductive success. In support of the hypothesis, owl monkey species do live at densities (7–64 ind/km2) that are predicted for monogamous species, but groups occupy home ranges and core areas that vary substantially in size, with pronounced overlap of home ranges, but not of core areas. There are strong indications that the availability of food sources in the core areas during the dry season may be of substantial importance for regulating social monogamy in owl monkeys. Finally, none of the proxies for the success of groups were strongly related to the size of the home range or core area. The results I present do not support conclusively any single explanation for the evolution of social monogamy in owl monkeys, but they help us to better understand how it may function. Moreover, the absence of conclusive answers linking ranging, ecology, and reproductive success with the evolution of social monogamy in primates, offer renewed motivation for continuing to explore the evolution of monogamy in owl monkeys. Am. J. Primatol. 78:355–371, 2016.

Social monogamy, male–female relationships, and biparental care in wild titi monkeys (Callicebus discolor)

Titi monkeys (Callicebus spp.) are one of two primate genera that live almost exclusively in groups with one adult-size individual of each sex and exhibit extensive biparental care of offspring. We provide a quantitative description of infant care and pairmate behavior in natural groups of Callicebus discolor that contributes to a limited literature on the behavioral ecology of wild titi monkeys. We collected data during a 3-year period from two social groups living in primary tropical rainforest at the Tiputini Biodiversity Station in Amazonian Ecuador before and after the birth of five infants. In order to evaluate the potential social and energetic costs associated with biparental care of offspring, we examined the relationships between infant care, pairmate behavior, and adult activity budgets. We found that males were almost exclusively responsible for transporting, grooming, sharing food, and playing with infants. As predicted, we found that, following the birth of an infant, adults groomed their partners less, spent less time in contact, and that huddling between pairmates decreased. Contrary to our predictions, after the birth of an infant, females did not increase the time spent feeding, and males did not decrease the time spent moving nor increase their resting time. Overall, our data suggest that the pair may experience social costs during times of intense infant care but that any putative energetic costs associated with infant care are not mitigated by adjusting physical activity. Future studies should investigate energy intake and expenditure, and consider how the variation observed in pairmate social relationships may affect reproductive success.

Evolutionary Biology and Conservation of Titis, Sakis and Uacaris: Pair-mate relationships and parenting in equatorial saki monkeys ( Pithecia aequatorialis ) and red titi monkeys ( Callicebus discolor ) of Ecuador

Socially-monogamous primates are often described as displaying a suite of behavioral characteristics that includes a prolonged and essentially exclusive mating relationship between mates, joint participation of mates in territory defense, and extensive male involvement in offspring care. Amongst the pitheciins, titi monkeys (Callicebus spp.), and saki monkeys (Pithecia spp.) frequently live in sociallymonogamous groups. We present here comparative data collected over four years on the social interactions of Neotropical adult male and female titi monkeys (Callicebus discolor, n = 2 groups) and saki monkeys (Pithecia aequatorialis, n = 1 group comprising 2 different male-female pairs) in the Yasuní National Park and Biosphere Reserve in Ecuador. Our data suggest that these two pitheciins do not both fit the mold of “classic” social monogamy. Despite their similar grouping patterns, the two species differ markedly in the quality of the social relationships between pairmates. Saki pairmates are less affiliative and engage less in behaviors thought to be instrumental to the development and maintenance of pair bonds (e.g., grooming, coordinated vocal displays) than titi pairmates. There are also dramatic differences in the extent to which males invest directly in offspring. While titi males invest heavily in infants, saki males provide little direct paternal care. Male sakis may be providing indirect investment, but they certainly do not seem to mitigate the energetic costs of infant care for their partners to the same extent as titi males do. Thus, male sakis apparently remain in sociallymonogamous relationships for reasons disassociated from paternal care. Our results suggest that different ecological and/or social factors may underlie the expression of social monogamy in these two pitheciins. INTRODUCTION Socially-monogamous primates are often described as displaying a suite of behavioral characteristics that includes a high degree of affiliation and social tolerance among pairmates (Kleiman 1977; Fuentes 2002; Reichard 2003). Traditional conceptions of pair bonding also imply that the affiliation is mutual, with both individuals being responsible for maintaining their close spatial association (Anzenberger 1988; Palombit 1996; Fernandez-Duque et al. 2000). Among the pitheciins, titis (Callicebus spp.), conform to this “classic” pattern of social monogamy. They are always encountered in small groups of two to five individuals, the nucleus of which is an adult male and an adult female (Kinzey 1981; Wright 1985; Robinson et al. 1987; Defler 2004; Carrillo et al. 2007; Norconk 2007). In wild groups, pairmates typically stay within a few meters of each other during feeding, traveling and resting periods, and show coordinated activities (Mason 1966; Robinson 1979; Robinson 1981; Kinzey and Wright 1982; Wright 1985; Mendoza and Mason 1986; Price and Piedade 2001). Based on the high degree of intimacy, coordination, and interdependence between pairmates, the existence of a strong and specific mutual attachment or “bond” is regularly inferred (Mason 1975; Anzenberger 1988; FernandezDuque et al. 1997). The existence of a pairbond has been unequivocally demonstrated in captivity, where pairmates show clear behavioral and physiological signs of distress following separation (Mendoza and Mason 1986). Our understanding of pairmate relationships in sakis (Pithecia spp.) is far less clear than in titis. Sakis have also been reported to live in small social groups that include a single breeding pair and up to several young. Although there have also been studies reporting larger groups (Norconk 2007), most of those groups were found in island habitats that limit the dispersal possibilities of individuals (Setz and Gaspar 1997; Vié et al. 2001; Norconk 2006), or during censuses of non-habituated individuals that limit the possibility of precise group identification (Lehman et al. 2001). Thus, there is little demographic evidence suggesting routine deviation from social monogamy in Pithecia. Additionally, our knowledge of saki social behavior is likewise limited, since there have only been a handful of studies focused on identified and habituated individuals (Setz and Gaspar 1997; Norconk 2006; Di Fiore et al. 2007). Coordinated displays and joint participation in territory defense are also thought to reflect the existence of a pair bond between the male and the female of a socially monogamous group (Robinson 1979; Robinson 1981; Mitani 1984; Raemaekers and Raemaekers 1985). Titis use ranges with relatively little overlap, and routinely perform behaviors at the borders of those ranges that include duetting and joint visual displays (Mason 1968; Robinson 1981; Wright 1985; Price and Piedade 2001). The two adults perform these behaviors in a highly coordinated fashion, sitting or standing side-by-side while calling or displaying. For sakis, on the other hand, the specific contributions of male and female pairmates to inter-group interactions or territory defense remain unexamined. The limited data available on use of space by sakis in non-island habitats indicate that their ranges may be somewhat exclusive and defended (Vié et al. 2001; Norconk et al. 2003). Preliminary playback experiments in Pithecia aequatorialis suggest that the male may respond more to a potential intruder than the female (Di Fiore & Fernandez-Duque, unpublished data, 2006). Finally, extensive male involvement in infant care is also commonly associated with social monogamy (Kleiman 1981; Kleiman and Malcolm 1981; Palombit 1999; Maestripieri 2002). Among the pitheciins, the involvement of the titi male in infant care is one of the most unique aspects of the social organization of the genus (Wright 1984; Mendoza and Mason 1986; Hoffman et al. 1995; Norconk 2007). The male carries the infant most of the time and also plays, grooms, and shares food with the infant. Although studies of infant care in free-ranging habituated groups have been somewhat limited (Kinzey and Becker 1983; Wright 1984; Tirado-Herrera and Heymann 2000; TiradoHerrera and Heymann 2004), there have been several detailed studies of parental behavior and infant development in captive groups (Fragaszy et al. 1982; Mendoza and Mason 1986; Hoffman et al. 1995). These studies suggest that, in titis, the infant may be primarily attached to the putative father rather than the mother (Mendoza and Mason 1986; Hoffman et al. 1995). In all of the other pitheciin genera, by contrast, direct paternal care is relatively absent. Male sakis do not routinely transport infants, although they may play and interact socially with older young (Norconk 2007). The extent to which strong pair bonds characterize sakis like they do in titis has not been investigated. Nor have there been evaluations of paternal care in sakis that consider the services that males may provide to females and their offspring, such as antipredator vigilance or territory defense. In the following paragraphs, we give a descriptive overview of the patterns of pairmate relationships and paternal care seen in Equatorial saki monkeys (P. aequatorialis) and red titi monkeys (Callicebus discolor), based on comparative data collected from two groups of titis and one group of sakis in western Amazonia. METHODS Area of study Since 2003, we have been studying three species of monogamous primates (owl monkeys: Aotus vociferans; titi monkeys: Callicebus discolor; saki monkeys: Pithecia aequatorialis) at the Tiputini Biodiversity Station (76° 08’ W, 0° 38’ S), located in the Yasuní National Park and Biosphere Reserve in Ecuador (Carrillo et al. 2007; Di Fiore et al. 2007; Fernandez-Duque et al. in press). The study site, on the left bank of the Río Tiputini, covers approximately 650 hectares of primary tropical rainforest that can be accessed by an extensive trail system (Figure 1). Rainfall in the region typically totals more than 3000 mm per year (Di Fiore and Rodman 2001). INSERT FIGURE 1 ABOUT HERE Groups of Study The saki group has been monitored continuously since November 2003. During that month, we darted and captured the adult male and fitted him with a radio collar following procedures we have also used to capture owl monkeys (Aotus azarai) in Argentina (Fernandez-Duque and Rotundo 2003), as well as owl monkeys (Aotus vociferans), titi monkeys (Callicebus discolor), capuchins (Cebus albifrons), squirrel monkeys (Saimiri), spider monkeys (Ateles belzebuth), and woolly monkeys (Lagothrix lagotricha) in Ecuador (Di Fiore & Fernandez-Duque, unpublished data, 2007). At the time of darting, the group consisted of an adult male, an adult female, and a male juvenile of approximately six months of age. The original adult male was replaced by a new adult male in October 2004 (Di Fiore et al. 2007); the dependent juvenile dispersed in October 2007, when he was approximately 4.5 years of age; and two infants were born to the adult female in March 2005 and November 2006. The first infant disappeared in February 2006 when it was approximately 11 months old and the second one is in the group as of December 2007. Regarding the titis, we report data collected from one fully-habituated group studied since November 2003 and a second group added to the study in October 2006. The first group consisted initially of two animals, an adult male and an adult female. During these years, the female gave birth to two offspring. The first one was born in January 2004 and disappeared in November 2006 when it was almost three years of age. The second one, born in January 2005, disappeared in February 2006 when it was 13 months old. The original adult female disappeared in March 2007, and she was replaced by a new adult female shortly thereafter. A new infant was born to the new female in December 2007. The second group consisted of an adult male-female pair when it was added to the study. Two infants were born in this group, one in November 2006 and the other in November 2007. Dat

Transparency, usability, and reproducibility: Guiding principles for improving comparative databases using primates as examples

Recent decades have seen rapid development of new analytical methods to investigate patterns of interspecific variation. Yet these cutting‐edge statistical analyses often rely on data of questionable origin, varying accuracy, and weak comparability, which seem to have reduced the reproducibility of studies. It is time to improve the transparency of comparative data while also making these improved data more widely available. We, the authors, met to discuss how transparency, usability, and reproducibility of comparative data can best be achieved. We propose four guiding principles: 1) data identification with explicit operational definitions and complete descriptions of methods; 2) inclusion of metadata that capture key characteristics of the data, such as sample size, geographic coordinates, and nutrient availability (for example, captive versus wild animals); 3) documentation of the original reference for each datum; and 4) facilitation of effective interactions with the data via user friendly and transparent interfaces. We urge reviewers, editors, publishers, database developers and users, funding agencies, researchers publishing their primary data, and those performing comparative analyses to embrace these standards to increase the transparency, usability, and reproducibility of comparative studies.

Do Predators and Thermoregulation Influence Choice of Sleeping Sites and Sleeping Behavior in Azara’s Owl Monkeys (Aotus azarae azarae) in Northern Argentina?

The spatiotemporal aspects of sleeping behavior are indicative of the ecological pressures that primate species face. We investigated the potential influence of predation and thermoregulatory constraints on sleeping site choice and sleep-related behaviors in a population of cathemeral owl monkeys (Aotus azarae azarae) in Formosa, Argentina. During 10 mo, we recorded data on 153 diurnal sleeping bouts (N = 5 groups), sleeping tree physical characteristics (diameter at breast height [DBH], height, foliage), sleeping sites within the tree, and grouping and positional behavior while sleeping. We also conducted a vegetation survey of potential sleeping trees. Our study groups used only 17 of 58 available tree species, slept in the top fifth of trees, and slept at sites midway between the trunk and crown exterior. Tree DBH, height, and sleeping site height varied among groups according to the forest subtypes within their home ranges. Group members slept in a huddle when temperatures were between 5° and 35°C, and slept separately only with temperatures >20°C. During the wet, hot summer, they slept more frequently under dense foliage; in the dry, cold winter, they preferred sites with light foliage and direct sun exposure, potentially to facilitate sunbathing, which occurred almost exclusively during the winter. While several sleeping site characteristics were consistent with minimizing predation risk, our results also suggest a tradeoff between predator exposure and warmer conditions at sleeping sites, especially during winter. Our results support the predation avoidance and thermoregulatory constraint hypotheses, furthering the possibility that these pressures were also contributing factors in the evolution of their cathemeral activity pattern.

Chemical composition of glandular secretions from a pair-living monogamous primate: Sex, age, and gland differences in captive and wild owl monkeys (Aotus spp.)

Broadening our knowledge of olfactory communication in strictly monogamous systems can inform our understanding of how chemosignals may facilitate social and reproductive behavior between the sexes. Compared to other social and mating systems, relatively little is known about olfactory communication in strictly monogamous non‐human primates. Furthermore, platyrrhines are not well represented in chemical analyses of glandular secretions. We conducted semi‐quantitative headspace gas chromatography with mass spectrometry to investigate the chemical components of glandular secretions from the subcaudal and pectoral glands of a strictly pair‐living platyrrhine, the owl monkey (Aotus spp.). In this study, the first chemical analysis of a wild platyrrhine population, our goals were to (1) conduct a robust analysis of glandular secretions from both captive and wild owl monkey populations and (2) identify whether biologically relevant traits are present in glandular secretions. We also compared and contrasted the results between two Aotus species in different environmental contexts: wild Aotus azarae (N = 33) and captive A. nancymaae (N = 104). Our findings indicate that secretions from both populations encode sex, gland of origin, and possibly individual identity. These consistent patterns across species and contexts suggest that secretions may function as chemosignals. Our data also show that wild A. azarae individuals are chemically discriminated by age (adult or subadult). Among the captive A. nanycmaae, we found chemical differences associated with location, possibly caused by dietary differences. However, there was no noticeable effect of contraception on the chemical profiles of females, nor evidence that closely related individuals exhibit more similar chemical profiles in A. nancymaae. Overall, our data suggest that glandular secretions of both wild and captive Aotus convey specific information. Future studies should use behavioral bioassays to evaluate the ability of owl monkeys to detect signals, and consider whether odor may ultimately facilitate social and sexual relationships between male and female owl monkeys.

Hormonal correlates of development and natal dispersal in wild female owl monkeys (Aotus azarae) of Argentina

ABSTRACT Pair‐living and socially monogamous primates typically do not reproduce before dispersing. It is currently unclear whether this reproductive suppression is due to endocrine or behavioral mechanisms. Cooperatively breeding taxa, like callitrichids, may forego reproduction in natal groups because they reap inclusive fitness benefits and/or they are avoiding inbreeding. However, neither of these benefits of delayed reproduction appear to adequately explain the lack of reproduction prior to leaving the natal group in pair‐living monogamous species. In this study, we determined whether wild Azaras owl monkeys (Aotus azarae) in the Argentinean Chaco establish reproductive maturity prior to dispersing. We utilized 635 fecal extracts to characterize reproductive hormone profiles of 11 wild juvenile and subadult females using enzyme immunoassays. Subadult females showed hormone profiles indicative of ovulatory cycling and had mean PdG and E1G concentrations approximately five times higher than juveniles. Contrary to expectations from the inbreeding avoidance hypothesis, female owl monkeys do not delay puberty, but rather commence ovarian cycling while residing in their natal group. Still, subadults appear to have a period during which they experience irregular, non‐conceptive cycles prior to reproducing. Commencing these irregular cycles in the natal group may allow them to develop a state of suspended readiness, which could be essential to securing a mate, while avoiding costs of ranging solitarily. Our results indicate that reproductive suppression in female owl monkeys is not due to endocrine suppression. We suggest that adults likely use behavioral mechanisms to prevent subadults from reproducing with unrelated adult males in their natal group. HIGHLIGHTSFemale owl monkeys of the Argentinean Chaco do not reproduce before natal dispersal.Subadult female owl monkeys commence ovarian cycling while still in the natal group.Subadult females experience irregular, non‐conceptive cycles prior to reproducing.