Detection of the mosquito-borne flaviviruses, West Nile, Dengue, Saint Louis Encephalitis, Ilheus, Bussuquara, and Yellow Fever in free-ranging black howlers (Alouatta caraya) of Northeastern Argentina.

Several medically important mosquito-borne flaviviruses have been detected in Argentina in recent years: Dengue (DENV), St. Louis encephalitis (SLEV), West Nile (WNV) and Yellow Fever (YFV) viruses. Evidence of Bussuquara virus (BSQV) and Ilheus virus (ILHV) activity were found, but they have not been associated with human disease. Non-human primates can act as important hosts in the natural cycle of flaviviruses and serological studies can lead to improved understanding of virus circulation dynamics and host susceptibility. From July-August 2010, we conducted serological and molecular surveys in free-ranging black howlers (Alouatta caraya) captured in northeastern Argentina. We used 90% plaque-reduction neutralization tests (PRNT90) to analyze 108 serum samples for antibodies to WNV, SLEV, YFV, DENV (serotypes 1and 3), ILHV, and BSQV. Virus genome detection was performed using generic reverse transcription (RT)-nested PCR to identify flaviviruses in 51 antibody-negative animals. Seventy animals had antibodies for one or more flaviviruses for a total antibody prevalence of 64.8% (70/108). Monotypic (13/70, 19%) and heterotypic (27/70, 39%) patterns were differentiated. Specific neutralizing antibodies against WNV, SLEV, DENV-1, DENV-3, ILHV, and BSQV were found. Unexpectedly, the highest flavivirus antibody prevalence detected was to WNV with 9 (8.33%) monotypic responses. All samples tested by (RT)-nested PCR were negative for viral genome. This is the first detection of WNV-specific antibodies in black howlers from Argentina and the first report in free-ranging non-human primates from Latin-American countries. Given that no animals had specific neutralizing antibodies to YFV, our results suggest that the study population remains susceptible to YFV. Monitoring of these agents should be strengthened to detect the establishment of sylvatic cycles of flaviviruses in America and evaluate risks to wildlife and human health.

Sex differences in the behavior of wild Alouatta caraya infants.

Several primates show sex-based differences in activity patterns and social interactions during infancy. These differences have been associated with adult social and reproductive functions of males and females and are related to male-male competition. Our goal was to describe behavioral patterns of wild Alouatta caraya male and female infants, a species with sexual dimorphism in body size and behavioral strategies during adulthood. We also examined the relationship between life history variables, infant sex and age, activity patterns, and social interactions in order to determine whether males and females follow different trajectories during early growth. Over a 27-month study, we observed 21 male infants and 14 female infants across two similar sites in northern Argentina. Data were analyzed using generalized linear mixed model (GLMM) tests. We found no differences in suckling time or weaning age between males and females (9.7 vs. 9.4 months), but male infants spent more time feeding on solid food and resting than female infants. Males also invested more time in contact with their mothers than did female infants, and mothers rejected and broke contact with males more frequently than with females. Other behavioral categories did not differ between the sexes. Our results suggest that higher nutritional demands of males compared with females may affect some behaviors. However, mothers of sons did not experience immediate trade-offs between current and future reproduction. Other behaviors, similarly expressed by the two sexes, suggest a similar developmental trajectory between male and female A. caraya infants, meaning that most differences emerge following the infant period.

How do demographic and social factors influence parent-offspring conflict? The case of wild black and gold howler monkeys (Alouatta caraya).

In this study, we examined the influence of demography and social context on mother-offspring conflict in wild black and gold howler monkeys (Alouatta caraya) inhabiting two nearby sites in northern Argentina, one comprising continuous forest and one fragmented forest. These sites differed in population density (3.25 vs. 1.04 individuals/ha), degree of home range overlap between neighboring groups (70 vs. 31%), and rate of intergroup encounters (2 vs. 0.02-1 encounters/day), though not in interbirth interval or rate of infant mortality. During a 27-month study (September 2008 through November 2010), we observed 37 mother-offspring dyads across the two sites. We found a very similar pattern of mother-offspring conflict in both populations; specifically, the sites did not differ in any of the variables used to characterize the mother-offspring relationship (the time spent in contact, the rate at which the mother makes and breaks contact, the rate at which the infant breaks contact, the rate of maternal rejection, and signs of infant distress) except one (the rate at which the infant makes contact). Although mother-offspring conflict is a dynamic process that varies over time, our results suggest that the different demographic and social contexts found at the two study sites did not have a marked effect on quantitative aspects of the mother-offspring relationship in these populations of black and gold howlers. Finally, this study suggests that the environmental variability (ecological, demographic, and social traits) leads to a set of strategies used both by infants and mothers with a main goal of conflict resolution, with mothers specifically aiming to cope with the tradeoff between current and future reproduction.

Who is coordinating collective movements in black and gold howler monkeys?

Decisions about when and where to travel are likely to have a strong influence on the feeding, ecology, and foraging strategies of individual primates living in a cohesive social group. Specifically, given differences in age, sex, reproductive status, or social dominance, particular group members may benefit from remaining at their present location while others may benefit from traveling to another area of their range to feed or rest. In this study, we present data on movement coordination in two groups of wild black and gold howler monkeys inhabiting Isla Brasilera (27º 20'S and 58º 40'W) in northern Argentina. We examine how factors such as sex, age, reproductive status, and dominance affect patterns of group movement coordination at feeding or resting sites, and in the context of intergroup encounters. Two groups were followed five days a month from sunrise to sunset during June to November 2004. Using focal and scan sampling techniques, we recorded 262 group displacements, the identity of the individual initiating and leading displacement, and the identity of the first individual to arrive at feeding, resting, or intergroup encounter sites. We found that overall age was the only factor that influenced group coordination: adults led more often (94.5 %) than immature individuals (5.5 %) in both groups. We did not find differences among adults. However, we found that males lead more often than females at intergroup encounters, consistent with the male-mate defense hypothesis. The distributed leadership pattern among adults observed in this study may suggest that adult individuals make equally shared consensus decisions. This pattern should be further examined using this individual-level approach in other populations of black and gold howlers, other species of howlers, and in other atelines in which within-group social tolerance is the rule rather than the exception.

Preliminary study of mother-offspring conflict in black and gold howler monkeys (Alouatta caraya).

Parent-offspring conflict has been scarcely studied in Neotropical primates. In this study, we explored mother-offspring conflict in a group of wild black and gold howler monkeys (Alouatta caraya) in northeastern Argentina. We used the all-occurrences technique to record behaviors, completing 712 h of observation. The results showed that all immature individuals between 2 and 23 months expressed conflict with regard to suckling or traveling with their mothers. Successful suckling attempts negatively correlated with the age of the immatures, occurring least frequently with the presence of newborns. In the juvenile period, the decline in successful attempts was a consequence of juveniles reducing suckling attempts and mother rejection.

Births in wild black and gold howler monkeys (Alouatta caraya) in Northern Argentina.

Previous studies on births in nonhuman primates suggest that births are expected to occur at night to avoid predators. Here, we describe birth-related behaviors in wild black and gold howler monkeys, Alouatta caraya and address the various ideas proposed in the literature about the timing of births in group-living nonhuman primates. We collected data on females' birth-related behaviors through continuous focal observations and scan samples. Focal observations on females giving birth were taken for the remainder of the day after noticing a female was in labor. We recorded behaviors and the spatial distribution of the whole group using scan samples taken every 10 min from sunrise to sunset the same day of birth. We recorded five births at the continuous forest (CF) over a 25 months period (January 2004-December 2004 and September 2005-September 2006) and two births in the fragmented forest (FF) over a 13 months period (September 2005-September 2006). From these, four births were during daylight (two at CF and two at FF) and three during the night at CF. Our descriptions of A. caraya births contribute to a growing data set on the timing of parturition in wild nonhuman primates and suggest that a clear pattern of nocturnal births is not universal across nonhuman primate species.

Habitat fragmentation and population size of the black and gold howler monkey (Alouatta caraya) in a semideciduous forest in Northern Argentina.

A population of black and gold howler monkeys (Alouatta caraya) living near the southern limit of its distribution in a semideciduous forest located in northern Argentina was studied in 2003 to evaluate the possible effects of habitat fragmentation - owing to logging - on its density and social organization within it. Aerial photographs taken in 1982, 1992, and 2001 were used to compare maps of vegetation. These maps were used to evaluate changes in the area covered by forest fragments. From March to June 2003, 10-day monthly surveys of howlers were made in each fragment. A total of 232 individual howlers were counted, belonging to 34 groups plus a solitary adult female. Groups ranged from 2 to 19 individuals (mean = 6.82, SD = 4.23), and 21% of the groups contained more than one adult male. Adults accounted for 55% of the individuals, immatures for 45%, and infants represented 13% of the total. Data obtained were compared with information available for the same population for 1982 and 1995. Results revealed no significant changes in the area of fragments, the crude and ecological density of howlers, and group composition. Group sizes and group composition of howlers suggest that the population remained stable over the past 22 years. The density, number of groups, and individuals appears not to be affected by fragmentation and logging, but crude density was low compared with other less-disturbed habitats. The status of the population remains uncertain owing to isolation, and because there are no protected areas to ensure its stability for the future.