Papers by Eduardo Fernandez-Duque
Parental Care Dynamics in the Monogamous Owl Monkey (Aotus azarae)
The maternal relief hypothesis for the evolution of biparental care proposes that extensive pater... more The maternal relief hypothesis for the evolution of biparental care proposes that extensive paternal care reduces the reproductive and energetic burden of the female. We evaluate this hypothesis focusing on a genetically monogamous owl monkey population in Formosa, Argentina, where paternal care is substantial. We describe activity patterns and social proximity of pairmates before and after the birth of an infant using focal scan sampling. During the first field season of a 3-year study we collected 42 hours of data from three reproducing pairs two months before and two months after the birth season. Both parents spent more time moving (males: 18±8% vs 21±2%; females: 19±3% vs 22±2%) and less time foraging (males: 38±11% vs 23±9%; females: 38±6% vs 26±12%) after the birth of the infant suggesting a negative energetic balance due to the presence of an infant. Only females spent more time resting after the birth of an infant (males: 33±5% vs. 30±15%; females: 21±2% vs 31±14%) indicati...
Long-term behavioral studies require the permanent identification of individ- uals. The need for ... more Long-term behavioral studies require the permanent identification of individ- uals. The need for individual identification is even more crucial for sexually monomorphic species since not even the sexes can be differentiated by the field observer. Owl monkeys (Aotus spp.) are sexually monomorphic primates in- habiting the forests of Central and South America. We report here on the methods and drug
Primates, 2008
Owl monkeys (Aotus azarai) are small, territorial, socially monogamous primates that show intense... more Owl monkeys (Aotus azarai) are small, territorial, socially monogamous primates that show intense infant care by the adult male in the group. It has been hypothesized that male care may be adaptive because it increases offspring survival and/or reduces the metabolic costs to the female of raising the offspring. Alternatively, males may provide care even when they are not related to the infants to increase future reproductive opportunities. We describe changes in infant care patterns that took place following the eviction of the resident male by a solitary male in an owl monkey population in the Argentinean Chaco. The resident male and mother provided all infant care during the first month of life of the infant, until the male was evicted. During the 3-day male replacement event, care of the infant was shared among the mother, a 4year-old sister, and a 1-year-old brother. The new male began contributing to infant care soon after entering the group, carrying, and interacting socially with the infant in much the same way as any male regularly does. However, despite receiving biparental care from both the original and new resident males, the infant disappeared at the age of four months and was presumed dead. These are the first reports of care by sibling and by non-putative fathers in wild owl monkeys. Given the significant amount time that new pairs of owl monkeys spend before reproducing, it is possible that male care in owl monkeys functions as mating effort as much as or more than parenting effort.
PLoS ONE, 2010
Primates show activity patterns ranging from nocturnality to diurnality, with a few species showi... more Primates show activity patterns ranging from nocturnality to diurnality, with a few species showing activity both during day and night. Among anthropoids (monkeys, apes and humans), nocturnality is only present in the Central and South American owl monkey genus Aotus. Unlike other tropical Aotus species, the Azara's owl monkeys (A. azarai) of the subtropics have switched their activity pattern from strict nocturnality to one that also includes regular diurnal activity. Harsher climate, food availability, and the lack of predators or diurnal competitors, have all been proposed as factors favoring evolutionary switches in primate activity patterns. However, the observational nature of most field studies has limited an understanding of the mechanisms responsible for this switch in activity patterns. The goal of our study was to evaluate the hypothesis that masking, namely the stimulatory and/or inhibitory/disinhibitory effects of environmental factors on synchronized circadian locomotor activity, is a key determinant of the unusual activity pattern of Azara's owl monkeys. We use continuous longterm (6-18 months) 5-min-binned activity records obtained with actimeter collars fitted to wild owl monkeys (n = 10 individuals) to show that this different pattern results from strong masking of activity by the inhibiting and enhancing effects of ambient luminance and temperature. Conclusive evidence for the direct masking effect of light is provided by data showing that locomotor activity was almost completely inhibited when moonlight was shadowed during three lunar eclipses. Temperature also negatively masked locomotor activity, and this masking was manifested even under optimal light conditions. Our results highlight the importance of the masking of circadian rhythmicity as a determinant of nocturnality in wild owl monkeys and suggest that the stimulatory effects of dim light in nocturnal primates may have been selected as an adaptive response to moonlight. Furthermore, our data indicate that changes in sensitivity to specific environmental stimuli may have been an essential key for evolutionary switches between diurnal and nocturnal habits in primates.
Size, Site Fidelity, and Overlap of Home Ranges and Core Areas in the Socially Monogamous Owl Monkey (Aotus azarae) of Northern Argentina
International Journal of Primatology, 2014
In addition to environmental factors, social variables such as group size may play an important r... more In addition to environmental factors, social variables such as group size may play an important role in explaining primate ranging patterns. In this study we investigated range sizes, site fidelity, and range overlaps of owl monkeys (Aotus azarae) in Northern Argentina. We calculated the size of home range and core areas for 18 groups in our study area. For the six most intensively studied groups we tested whether precipitation as a crude proxy for food availability or group size had an influence on range size, assessed the degree of site fidelity by quantifying overlaps of annual ranges and core areas, and calculated the amount of range overlap between neighboring groups for each year. We used the kernel density estimation method to calculate home ranges as 90% kernel and core areas as 50% kernel. Home range size (mean ± SD) was 6.2 ha (± 1.8) and core area size 1.9 (± 0.6). Rainfall and group size were not statistically significant predictors of range sizes. Site fidelity was high, with a range overlap of 82% (± 11) between consecutive years. Neighboring groups overlapped over 48% (± 15) of the outer parts of their group ranges and 11% (± 15) of their core areas. We found no evidence that larger groups occupy larger areas than smaller groups, suggesting that food availability might be above a critical threshold for owl monkeys so that larger groups do not need to extend their foraging areas to meet their energy requirements. Our findings indicate that ranges remain stable over several years as groups visit the same locations of fruit trees within their range. We showed that owl monkeys exhibit a considerable degree of range overlap. However, we suggest that this range overlap might be spatial rather than temporal, which maximizes access to clumped feeding resources in overlapping areas that are used at distinct times, while excluding other males from access to females in exclusively used areas.
Chronobiology International, 2012
Among the more than 40 genera of anthropoid primates (monkeys, apes, and humans), only the South ... more Among the more than 40 genera of anthropoid primates (monkeys, apes, and humans), only the South American owl monkeys, genus Aotus, are nocturnal. However, the southernmostly distributed species, Aotus azarai azarai, of the Gran Chaco may show considerable amounts of its 24-h activity during bright daylight. Due to seasonal changes in the duration of photophase and climatic parameters in their subtropical habitat, the timing and pattern of their daily activity are expected to show significant seasonal variation. By quantitative long-term activity recordings with Actiwatch AW4 accelerometer data logger devices of 10 wild owl monkeys inhabiting a gallery forest in Formosa, Argentina, the authors analyzed the seasonal variation in the temporal niche and activity pattern resulting from entrainment and masking of the circadian activity rhythm by seasonally and diurnally varying environmental factors. The owl monkeys always displayed a distinct bimodal activity pattern, with prominent activity bouts and peaks during dusk and dawn. Their activity rhythm showed distinct lunar and seasonal variations in the timing and daily pattern. During the summer, the monkeys showed predominantly crepuscular/nocturnal behavior, and a crepuscular/ cathemeral activity pattern with similar diurnal and nocturnal activity levels during the cold winter months. The peak times of the evening and morning activity bouts were more closely related to the times of sunset and sunrise, respectively, than activity-onset and -offset. Obviously, they were better circadian markers for the phase position of the entrained activity rhythm than activity-onset and -offset, which were subject to more masking effects of environmental and/or internal factors. Total daily activity was lowest during the two coldest lunar months, and almost twice as high during the warmest months. Nighttime (21:00-06:00 h) and daytime (09:00-18:00 h) activity varied significantly across the year, but in an opposite manner. Highest nighttime activity occurred in summer and maximal daytime activity during the cold winter months. Dusk and dawn activity, which together accounted for 43% of the total daily activity, barely changed. The monkeys tended to terminate their nightly activity period earlier on warm and rainy days, whereas the daily amount of activity showed no significant correlation either with temperature or precipitation. These data are consistent with the dual-oscillator hypothesis of circadian regulation. They suggest the seasonal variations of the timing and pattern of daily activity in wild owl monkeys of the Argentinean Chaco result from a specific interplay of light entrainment of circadian rhythmicity and strong masking effects of various endogenous and environmental factors. Since the phase position of the monkeys' evening and morning activity peaks did not vary considerably over the year, the seasonal change from a crepuscular/nocturnal activity pattern in summer to a more crepuscular/cathemeral one in winter does not depend on a corresponding phase shift of the entrained circadian rhythm, but mainly on masking effects. Thermoregulatory and energetic demands and constraints seem to play a crucial role. (Author correspondence: [email protected])
International Journal of …, 2002
The night monkeys (Aotus azarai) of Formosa, Argentina provide an opportunity to investigate the ... more The night monkeys (Aotus azarai) of Formosa, Argentina provide an opportunity to investigate the influences of ambient temperature and photoperiod on reproduction in a highly seasonal environment: the Chaco. Between 1997 and 2000, we collected data to evaluate the relationship between rainfall, ambient temperature, photoperiod and food availability and the annual distribution of mating behavior and births in 15 groups of monkeys in the forests of the Eastern Argentinean Chaco. Our data show that the area is highly seasonal, characterized by significant fluctuations in rainfall, temperature, photoperiod and food availability. There are two rain peaks in April and November and a dry season lasting from June to August. Monthly mean temperatures were on average 11 • C lower during winter months than they were during summer months. Temperatures <10 • C and >33 • C were also frequent through the year. Days are 3 h longer during the summer than during the winter months. Insect abundance and the percentage of tree species producing fruits, flowers or new leaves reached a low in the coldest winter months. Mating was infrequent, and we only observed it between May and September. Half the births (n = 13) occurred during a 2-week period in October. Infant survival during the first 6 mo of life was high (96%). Our findings suggest an environmental control of reproduction. Changes in photoperiod and temperature may promote reproductive activity in females that might conceive and begin 640 Fernandez-Duque, Rotundo, and Ramirez-Llorens pregnancy at a time void of high temperatures that could be metabolically challenging.
International Journal of …, 2011
The benefits to researchers of capturing and collaring free-ranging primates are numerous, but so... more The benefits to researchers of capturing and collaring free-ranging primates are numerous, but so are the actual and potential costs to the individuals. We aimed to 1) evaluate quantitatively the possible demographic long-term costs of radio-collaring a free-...
Folia Primatologica, 2007
Sakis (genus Pithecia ) commonly live in socially monogamous groups, but data from wild populatio... more Sakis (genus Pithecia ) commonly live in socially monogamous groups, but data from wild populations on group dynamics and on the turnover of reproductive-age animals are rare. Here we describe the replacement of the adult male in one group of sakis in the ...
Journal of molecular evolution, 2010
The arginine vasopressin V1a receptor gene (AVPR1A) has been implicated in increased partner pref... more The arginine vasopressin V1a receptor gene (AVPR1A) has been implicated in increased partner preference and pair bonding behavior in mammalian lineages. This observation is of considerable importance for studies of social monogamy, which only appears in a small subset of primate taxa, including the Argentinean owl monkey (Aotus azarai). Thus, to investigate the possible influence of AVPR1A on the evolution of social behavior in owl monkeys, we sequenced this locus in a wild population from the Gran Chaco. We also assessed the interspecific variation of AVPR1A in platyrrhine species that represent a set of phylogenetically and behaviorally disparate taxa. The resulting data revealed A. azarai to have a unique genic structure for AVPR1A that varies in coding sequence and microsatellite repeat content relative to other primate and mammalian species. Specifically, one repetitive region that has been the focus in studies of human AVPR1A diversity, ''RS3,'' is completely absent in A. azarai and all other platyrrhines examined. This finding suggests that, if AVPR1A modulates behavior in owl monkeys and other neotropical primates, it does so independent of this region. These observations have also provided clues about the process by which the range of social behavior in the Order Primates evolved through lineage-specific neurogenetic variation.
International Journal of Primatology, 2008
Given its broad geographical distribution, Aotus is a productive genus for comparative studies th... more Given its broad geographical distribution, Aotus is a productive genus for comparative studies that evaluate how different ecological factors influence the morphology, behavior, ecology, and demography of closely related species. During 18 mo we collected demographic, ranging, and activity data from owl monkeys (Aotus vociferans) in Yasuní National Park in eastern Ecuador. To collect demographic data, we monitored the trail
Folia …, 2010
Anecdotal reports of predation as well as observed predation attempts and rates of animal disappe... more Anecdotal reports of predation as well as observed predation attempts and rates of animal disappearance provide some of the most relevant data for evaluating the influence that predation risk may have on primate behavioural ecology. Here, we report rates of ...
Conservation Biology, 1994
Abstract: Meta-analysis is the application of quantitative methods to the problem of comparing an... more Abstract: Meta-analysis is the application of quantitative methods to the problem of comparing and combining results from separate but similar analytic studies. Despite its pop-ularity in the social sciences and epidemiology, meta-analysis has remained virtually unknown in the ...
Double effort: Parental behavior of wild Azara's owl monkeys in the face of twins
American Journal of Primatology, 2014
In species of mammals that habitually bear single offspring, like most anthropoid primates, the o... more In species of mammals that habitually bear single offspring, like most anthropoid primates, the occurrence of twins is expected to impose considerable energetic costs on the caretakers. The question then arises of how caregivers cope with the potentially increased costs of raising twins. These increased costs should lead to differing developmental rates in twins when compared to singletons, and/or to changes in the caregivers&amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;#39; behavior. Likewise, time budgets of parents of singletons are expected to differ from those of adults without offspring. Additionally, if twinning was an adaptive response to favorable ecological conditions, it should be more likely in years with high food abundance. Following the birth in 2011 of two sets of twins in a wild population of pair-living Azara&amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;#39;s owl monkeys (Aotus azarae) in Northern Argentina, we used long-term demographic, behavioral, and phenological data to compare (a) the proportion of time that singleton and twin infants were carried by either parent; (b) adult time budgets and ranging behavior in groups with zero, one, or two infants; and (c) the availability of food in 2011 with food availability in other years. Twins, like singletons, were carried nearly exclusively by the male, and they were carried slightly more than singletons, suggesting a relatively inflexible pattern of infant care in the species. Time budgets showed that twin parents foraged more and moved less than singleton parents or groups without infants, despite the fact that phenological data indicate that fruit availability in 2011 was not substantially higher than in some of the other years. Overall, twinning thus presumably increased costs to breeders, especially males, but its effect on animals&amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;#39; long-term reproductive success remains unclear.
Density and population structure of owl monkeys (Aotus azarai) in the Argentinean chaco
American Journal of Primatology, 2001
Owl monkeys are small monogamous primates ranging over a wide area extending from Panama to the C... more Owl monkeys are small monogamous primates ranging over a wide area extending from Panama to the Chaco region of northern Argentina. The Chaco, an alluvial plain covering over one million km2 of Argentina, Bolivia, Brazil, and Paraguay, consists of a mosaic of grasslands, savannas, xeric thorn forests, and gallery forests. The region shows significant seasonal variation in climate, rainfall, and food availability. The goal of this study was to determine the density, size, and structure of a population of Aotus azarai in the seasonal gallery forests of the eastern Argentinean Chaco. Reported population density, as well as group size and composition are based on data collected from 11 groups contacted on approximately 900 occasions, and observed for over 2,000 hours during a three-year period. Group and individual densities were 16 groups/km2 and 64 individuals/km2, respectively. Approximately half of the groups (n = 5) were small groups which had three individuals most of the time and never more than four, whereas the remaining groups were large groups composed of four or five individuals, and sometimes even six or seven individuals. This is the first study of A. azarai based on monitoring of a relatively large number of distinct groups. Our data suggest that owl monkeys in the seasonal subtropical forests of Formosa live at a density as high as those reported for owl monkey populations observed in tropical forests. The data also show that the social groups in the owl monkey population are of comparable size and composition to those characteristic of populations in the tropics.
American Journal of Primatology, 2008
Accounts of food sharing within natural populations of mammals have focused on transfers to offsp... more Accounts of food sharing within natural populations of mammals have focused on transfers to offspring or transfers of food items that are difficult to obtain (such as meat). Five groups of socially monogamous owl monkeys (Aotus azarai azarai) in Formosa, Argentina were observed during 107 hr to determine the pattern of food sharing under natural conditions. There were a total of 42 social interactions involving food with food being transferred on eight occasions. Adult males transferred food to young more often than did adult females. All types of food that were readily obtained and eaten by all age/sex classes were transferred to young. Adult females also transferred food to their mates. This type of food sharing is very rare among animals and may have social benefits specific to monogamous mammals with paternal care. Am.
mtDNA diversity in azara's owl monkeys (Aotus azarai azarai) of the Argentinean Chaco
American Journal of Physical Anthropology, 2011
Owl monkeys (Aotus spp.) inhabit much of South America yet represent an enigmatic evolutionary br... more Owl monkeys (Aotus spp.) inhabit much of South America yet represent an enigmatic evolutionary branch among primates. While morphological, cytogenetic, and immunological evidence suggest that owl monkey populations have undergone isolation and diversification since their emergence in the New World, problems with adjacent species ranges, and sample provenance have complicated efforts to characterize genetic variation within the genus. As a result, the phylogeographic history of owl monkey species and subspecies remains unclear, and the extent of genetic diversity at the population level is unknown. To explore these issues, we analyzed mitochondrial DNA (mt DNA) variation in a population of wild Azara&amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;#39;s owl monkeys (Aotus azarai azarai) living in the Gran Chaco region of Argentina. We sequenced the complete mitochondrial genome from one individual (16,585 base pairs (bp)) and analyzed 1,099 bp of the hypervariable control region (CR) and 696 bp of the cytochrome oxidase II (COII) gene in 117 others. In addition, we sequenced the mitochondrial genome (16,472 bp) of one Nancy Ma&amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;#39;s owl monkey (A. nancymaae). Based on the whole mtDNA and COII data, we observed an ancient phylogeographic discontinuity among Aotus species living north, south, and west of the Amazon River that began more than eight million years ago. Our population analyses identified three major CR lineages and detected a high level of haplotypic diversity within A. a. azarai. These data point to a recent expansion of Azara&amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;#39;s owl monkeys into the Argentinean Chaco. Overall, we provide a detailed view of owl monkey mtDNA variation at genus, species, and population levels.
Behavioral ecology and sociobiology, Dec 22, 2010
Species differ widely with regard to parental investment strategies and mechanisms underlying tho... more Species differ widely with regard to parental investment strategies and mechanisms underlying those strategies. The passing of benefits to likely genetic offspring can be mediated through a number of different computational and behavioral systems. We report results from an agent-based model in which offspring maintain proximity with parents and parents transmit benefits to offspring without the capacity of either parent or offspring to “recognize” one another. Instead, parents follow a simple rule to emit benefits after ...
Access to Electric Light Is Associated with Shorter Sleep Duration in a Traditionally Hunter-Gatherer Community
Journal of biological rhythms, Jan 18, 2015
Access to electric light might have shifted the ancestral timing and duration of human sleep. To ... more 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 ...
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Papers by Eduardo Fernandez-Duque