Birth of a wild black howler monkey (Alouatta pigra) at an anthropogenic site.

We present the first description of a diurnal live birth of a wild black howler monkey (Alouatta pigra). The mother formed part of a group of five individuals inhabiting an anthropogenic setting in the tropical lowlands of southeast Mexico. A total of 7 h and 50 min passed from the rupture of the amniotic sac early in the day to the crowning of the infant from the birth canal. The delivery of the infant lasted ~ 3 min. We describe the event while referencing images and time points in a supplementary video recording. We place our findings in the context of the available reports of live births in the Alouatta genus, time of day, birth duration, and group activity budget on the day of the birth. While primates tend to give birth at night to reduce complications from group interactions, the observed birth took place during the day, which may have been possible due to an alteration in group time allocation. Our report provides in-depth details of the events of a birth and important information regarding the natural history of the black howler monkey.

Dispersal patterns in black howler monkeys (Alouatta pigra): Integrating multiyear demographic and molecular data.

Dispersal is a fundamental process in the functioning of animal societies as it regulates the degree to which closely related individuals are spatially concentrated. A species' dispersal pattern can be complex as it emerges from individuals' decisions shaped by the cost-benefit tradeoffs associated with either remaining in the natal group or dispersing. Given the potential complexity, combining long-term demographic information with molecular data can provide important insights into dispersal patterns of a species. Based on a 15-year study that integrates multiyear demographic data on six groups with longitudinal and cross-sectional genetic sampling of 20 groups (N = 169 individuals, N = 21 polymorphic microsatellite loci), we describe the various dispersal strategies of male and female black howler monkeys (Alouatta pigra) inhabiting Palenque National Park, Mexico. Genetically confirmed dispersal events (N = 21 of 59 males; N = 6 of 65 females) together with spatial autocorrelation analyses revealed that the dispersal pattern of black howlers is bisexual with strong sex-biases in both dispersal rate (males disperse more often than females) and dispersal distance (females disperse farther than males). Observational and genetic data confirm that both males and females can successfully immigrate into established groups, as well as form new groups with other dispersing individuals. Additionally, both males and females may disperse singly, as well as in pairs, and both may also disperse secondarily. Overall, our findings suggest multiple dispersal trajectories for black howler males and females, and longer multiyear studies are needed to unravel which demographic, ecological and social factors underlie individuals' decisions about whether to disperse and which dispersal options to take.

La dispersión es un proceso fundamental en el funcionamiento de las sociedades animales, ya que regula el grado en que los individuos parentados se concentran espacialmente. El patrón de dispersión de una especie puede ser complejo ya que surge de las decisiones de los individuos conformadas por las compensaciones de costo-beneficio asociadas con permanecer en el grupo natal o dispersarse. Dada esta posible complejidad, la combinación de información demográfica a largo plazo con datos moleculares puede proporcionar información importante sobre los patrones de dispersión de una especie en particular. Basado en un estudio de 15 años que integra datos demográficos de seis grupos sociales con muestreo genético longitudinal y transversal de 20 grupos (N = 169 individuos, N = 21 loci de microsatélites polimórficos), describimos las diversas estrategias de dispersión de machos y hembras del mono aullador negro (Alouatta pigra) que habitan el Parque Nacional Palenque, México. Los eventos de dispersión confirmados genéticamente (N = 21 de 59 machos; N = 6 de 65 hembras), junto con los análisis de autocorrelación espacial revelaron que el patrón de dispersión de los monos aulladores negros es bisexual con fuertes sesgos sexuales en ambas tasas de dispersión (los machos se dispersan más a menudo que las hembras) y distancia de dispersión (las hembras se dispersan más lejos que los machos). Los datos de observación y genéticos confirman que tanto machos como hembras pueden inmigrar con éxito a grupos ya establecidos, así como formar nuevos grupos con otros individuos que se están dispersando. Además, tanto los machos como las hembras pueden dispersarse individualmente, así como en parejas, y ambos también pueden dispersarse secundariamente. En general, nuestros hallazgos sugieren múltiples trayectorias de dispersión para aulladores negros de los dos sexos, y se necesitan más estudios para desentrañar qué factores demográficos, ecológicos y sociales subyacen en las decisiones de los individuos sobre si dispersarse y qué opciones de dispersión tomar.

Cognitive maps in the wild: revealing the use of metric information in black howler monkey route navigation.

When navigating, wild animals rely on internal representations of the external world - called 'cognitive maps' - to take movement decisions. Generally, flexible navigation is hypothesized to be supported by sophisticated spatial skills (i.e. Euclidean cognitive maps); however, constrained movements along habitual routes are the most commonly reported navigation strategy. Even though incorporating metric information (i.e. distances and angles between locations) in route-based cognitive maps would likely enhance an animal's navigation efficiency, there has been no evidence of this strategy reported for non-human animals to date. Here, we examined the properties of the cognitive map used by a wild population of primates by testing a series of cognitive hypotheses against spatially explicit movement simulations. We collected 3104 h of ranging and behavioural data on five groups of black howler monkeys (Alouatta pigra) at Palenque National Park, Mexico, from September 2016 through August 2017. We simulated correlated random walks mimicking the ranging behaviour of the study subjects and tested for differences between observed and simulated movement patterns. Our results indicated that black howler monkeys engaged in constrained movement patterns characterized by a high path recursion tendency, which limited their capacity to travel in straight lines and approach feeding trees from multiple directions. In addition, we found that the structure of observed route networks was more complex and efficient than simulated route networks, suggesting that black howler monkeys incorporate metric information into their cognitive map. Our findings not only expand the use of metric information during route navigation to non-human animals, but also highlight the importance of considering efficient route-based navigation as a cognitively demanding mechanism.

Using natural travel paths to infer and compare primate cognition in the wild.

Within comparative psychology, the evolution of animal cognition is typically studied either by comparing indirect measures of cognitive abilities (e.g., relative brain size) across many species or by conducting batteries of decision-making experiments among (typically) a few captive species. Here, we propose a third, complementary approach: inferring and comparing cognitive abilities through observational field records of natural information gradients and the associated variation in decision-making outcomes, using the ranging behavior of wild animals. To demonstrate the feasibility of our proposal, we present the results of a global survey assessing the availability of long-term ranging data sets from wild primates and the willingness of primatologists to share such data. We explore three ways in which such ranging data, with or without the associated behavioral and ecological data often collected by primatologists, might be used to infer and compare spatial cognition. Finally, we suggest how ecological complexity may be best incorporated into comparative analyses.

Ranging behavior and the potential for territoriality in pair-living titi monkeys (Plecturocebus discolor).

Patterns of ranging behavior and space use are key for evaluating current ideas about the evolution and maintenance of pair-living and sexual monogamy as they provide insights into the dispersion of females, the potential for territoriality, and whether males are limited to defending an area that can support only one female and her offspring. We examined ranging behavior and space use to evaluate the potential for territoriality in five groups of red titi monkeys (Plecturocebus discolor) during a 10-year study in Ecuadorian Amazonia. Mean home range size, calculated using a time-sensitive local convex hull estimation procedure, was 4.0 ± 1.4 ha. Annual home ranges of neighboring groups overlapped, on average, 0%-7%. Mean daily path length was 670 ± 194 m, resulting in defendability indices of 2.2-3.6 across groups. Groups visited, on average, 4 of 12 sections of their home range border area per day, but that was not more often than would be expected by chance, and intergroup encounters were infrequent. We did not find evidence of active monitoring for intruders in border areas, in that groups did not travel either faster or slower when at the border than when in central areas of their range. The absence of overt monitoring might be compensated for by engaging in loud calls, which the study groups did throughout their home ranges; these calls may serve as an advertisement of occupancy and a deterrent to intruding conspecifics. Our finding that red titis have a high potential for territoriality is consistent with several of the main hypotheses proposed to explain pair-living in mammals.

Effects of variation in forest fragment habitat on black howler monkey demography in the unprotected landscape around Palenque National Park, Mexico.

Habitat loss and fragmentation are leading threats to biodiversity today, and primates are particularly vulnerable to anthropogenic habitat disturbance. However, few studies have examined how differential effects of variation in forest fragment characteristics on males and females in a primate population may affect demography and population persistence. We quantified the effects of variation in forest fragment characteristics on the within-fragment demography of black howler monkeys (Alouatta pigra) in forest fragments around Palenque National Park, Mexico, and how these effects differed between adult males and females. We quantified forest loss in the landscape between 2000 and 2017, and used a redundancy analysis to examine the effects of 15 variables quantifying fragment dimensions, forest composition and physical structure, and isolation on fragment population size and density, the proportion of adult males and females in the fragment population, and the mean number of adult males and females per group in 34 fragments (N = 393 monkeys). We hypothesized that (i) population size is positively correlated with fragment area, while population density is negatively correlated, and (ii) the composition of fragment populations results from differential effects of fragment variables on adult males and females. Forest cover decreased by 23.3% from 2000 to 2017. Our results showed a significant effect of fragment variables on population demography in fragments, accounting for 0.69 of the variance in the demographic response variables. Population size increased with fragment area and connectivity, while density decreased. Larger, less isolated fragments with better connectivity, characteristics indicative of abundant secondary growth, and those with more diverse vegetation but lower Simpson's evenness indices tended to have more adult females per group and a higher proportion of adult females in the population. In contrast, fragments that were largely similar in characteristics of forest composition and structure, but that were more isolated from nearby fragments, had more adult males per group and a higher proportion of adult males. These results may stem from black howler females preferentially remaining in natal groups and fragments when possible, and dispersing shorter distances when they disperse, while males may be more likely to disperse between fragments, traveling longer distances through the matrix to more isolated fragments. These differential effects on males and females have important conservation implications: if females are more abundant in larger, less isolated fragments, while males are more abundant in more isolated fragments, then to effectively conserve this population, both landscape connectivity and fragment areas should be maintained and increased.

Demographic population structure of black howler monkeys in fragmented and continuous forest in Chiapas, Mexico: Implications for conservation.

For wild primates, demography studies are increasingly recognized as necessary for assessing the viability of vulnerable populations experiencing rapid environmental change. In particular, anthropogenic changes such as habitat loss and fragmentation can cause ecological and behavioral changes in small, isolated populations, which may, over time, alter population density and demographic structure (age/sex classes and group composition) in fragment populations relative to continuous forest populations. We compared our study population of Endangered black howler monkeys (Alouatta pigra) in 34 forest fragments around Palenque National Park (PNP), Mexico (62 groups, 407 individuals), to the adjacent population in PNP, protected primary forest (21 groups, 134 individuals), and to previous research on black howlers in fragments in our study area (18 groups, 115 individuals). We used χ2 and Mann-Whitney U tests to address the questions: (a) what is the current black howler demographic population structure in unprotected forest fragments around PNP? (b) How does it compare to PNP's stable, continuous population? (c) How has it changed over time? Compared to the PNP population, the fragment populations showed higher density, a significantly lower proportion of multimale groups, and significantly fewer adult males per group. The population's age/sex structure in the fragmented landscape has been stable over the last 17 years, but differed in a higher proportion of multifemale groups, higher density, and higher patch occupancy in the present. In the context of conservation, some of our results may be positive as they indicate possible population growth over time. However, long-term scarcity of adult males in fragments and associated effects on population demographic structure might be cause for concern, in that it may affect gene flow and genetic diversity. The scarcity of adult males might stem from males experiencing increased mortality while dispersing in the fragmented landscape, whereas females might be becoming more philopatric in fragments.

The evolution of pair-living, sexual monogamy, and cooperative infant care: Insights from research on wild owl monkeys, titis, sakis, and tamarins.

"Monogamy" and pair bonding have long been of interest to anthropologists and primatologists. Their study contributes to our knowledge of human evolutionary biology and social evolution without the cultural trappings associated with studying human societies directly. Here, we first provide an overview of theoretical considerations, followed by an evaluation of recent comparative studies of the evolution of "social monogamy"; we are left with serious doubts about the conclusions of these studies that stem from the often poor quality of the data used and an overreliance on secondary sources without vetting the data therein. We then describe our field research program on four "monogamous" platyrrhines (owl monkeys, titis, sakis, and tamarins), evaluate how well our data support various hypotheses proposed to explain "monogamy," and compare our data to those reported on the same genera in comparative studies. Overall, we found a distressing lack of agreement between the data used in comparative studies and data from the literature for the taxa that we work with. In the final section, we propose areas of research that deserve more attention. We stress the need for more high-quality natural history data, and we urge researchers to be cautious about the uncritical use of variables of uncertain internal validity. Overall, it is imperative that biological anthropologists establish and follow clear criteria for comparing and combining results from published studies and that researchers, reviewers, and editors alike comply with these standards to improve the transparency, reproducibility, and interpretability of causal inferences made in comparative studies.

Arboreal route navigation in a Neotropical mammal: energetic implications associated with tree monitoring and landscape attributes.

BACKGROUND: Although navigating along a network of routes might constrain animal movement flexibility, it may be an energetically efficient strategy. Routinely using the same route allows for visually monitoring of food resources, which might reduce the cognitive load and as such facilitate the process of movement decision-making. Similarly, locating routes in areas that avoid costly landscape attributes will enhance their overall energy balance. In this study we determined the benefits of route navigation in an energy minimiser arboreal primate, the black howler monkey (Alouatta pigra). METHODS: We monitored five neighbouring groups of black howler monkeys at Palenque National Park, Mexico from September 2016 through August 2017. We recorded the location of the focal group every 20 m and mapped all travel paths to establish a route network (N = 1528 travel bouts). We constructed linear mixed models to assess the influence of food resource distribution (N = 931 trees) and landscape attributes (slope, elevation and presence of canopy gaps) on the location of routes within a route network. RESULTS: The number of food trees that fell within the visual detection distance from the route network was higher (mean: 156.1 ± SD 44.9) than randomly simulated locations (mean: 121.9 ± SD 46.4). Similarly, the number of food trees found within the monkey's visual range per meter travelled increased, on overage, 0.35 ± SE 0.04 trees/m with increasing use of the route. In addition, route segments used at least twice were more likely to occur with increasing density of food resources and decreasing presence of canopy gaps. Route segments used at least four times were more likely to occur in elevated areas within the home ranges but only under conditions of reduced visual access to food resources. CONCLUSIONS: Route navigation emerged as an efficient movement strategy in a group-living arboreal primate. Highly used route segments potentially increased visual access to food resources while avoiding energetically costly landscape features securing foraging success in a tropical rainforest.

Ranging behavior and potential for territoriality in equatorial sakis (Pithecia aequatorialis) in Amazonian Ecuador.

OBJECTIVES: Territoriality refers to the consistent defense of an area within the home range (HR) against intrusions of conspecifics. It implies exclusive space use with low degree of overlap among neighboring groups, high site fidelity, specific ranging behavior such as high mobility relative to HR size and frequent visits of territory borders, and monitoring behavior. We examined ranging behavior and use of space to evaluate territoriality in Pithecia aequatorialis in Ecuador. MATERIALS AND METHODS: Between 2005 and 2015, we monitored one main study group continuously and five additional groups for shorter periods (5 months to 2.5 years) at the Tiputini Biodiversity Station, in eastern Ecuador. We scored the location of the study groups at 20 min intervals during, on average, 5 days per month. We estimated saki HRs and core areas (CAs) using the fixed kernel density method (95 and 50%, respectively). RESULTS: The average HR size was 57 ha and the average CA 14 ha. The degree of overlap between HRs of neighboring groups was low (2-9%). For the main study group, the average overlap between annual HRs was 82%. Mean daily path length across groups was 1,151 m; the defensibility index varied between 1.1 and 2.3 (values >1 are suggestive of territoriality), and the fractional monitoring rate varied between 0.06 and 0.15 (values >0.08 are suggestive of territoriality). Groups did not visit their HR borders (100 m inner buffer) more often than would be expected by chance. Travel speed and directness were comparable between the borders and the centers of groups' HRs. DISCUSSION: Our multiyear study suggests that equatorial sakis show low degree of range overlap and high site fidelity and have the potential to be territorial, given their high mobility relative to HR size that allows for frequent border monitoring. Nevertheless, their movement patterns in border areas did not reveal evidence for monitoring behavior.

Patterns in Gut Microbiota Similarity Associated with Degree of Sociality among Sex Classes of a Neotropical Primate.

Studies of human and domestic animal models indicate that related individuals and those that spend the most time in physical contact typically have more similar gut microbial communities. However, few studies have examined these factors in wild mammals where complex social dynamics and a variety of interacting environmental factors may impact the patterns observed in controlled systems. Here, we explore the effect of host kinship and time spent in social contact on the gut microbiota of wild, black howler monkeys (Alouatta pigra). Our results indicate that closely related individuals had less similar gut microbial communities than non-related individuals. However, the effect was small. In contrast, as previously reported in baboons and chimpanzees, individuals that spent more time in contact (0 m) and close proximity (0-1 m) had more similar gut microbial communities. This pattern was driven by adult female-adult female dyads, which generally spend more time in social contact than adult male-adult male dyads or adult male-adult female dyads. Relative abundances of individual microbial genera such as Bacteroides, Clostridium, and Streptococcus were also more similar in individuals that spent more time in contact or close proximity. Overall, our data suggest that even in arboreal primates that live in small social groups and spend a relatively low proportion of their time in physical contact, social interactions are associated with variation in gut microbiota composition. Additionally, these results demonstrate that within a given host species, subgroups of individuals may interact with the gut microbiota differently.

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.

Individual participation in intergroup contests is mediated by numerical assessment strategies in black howler and tufted capuchin monkeys.

Asymmetries in resource-holding potential between opposing groups frequently determine outcomes of intergroup contests. Since both numerical superiority and high intergroup dominance rank may confer competitive advantages, group members should benefit from assessing the relative strength of rivals prior to engaging in defensive displays. However, differences in individual assessment may emerge when cost-benefit trade-offs differ among group members. We examine the influence of numerical superiority and intergroup dominance relationships on individual participation in intergroup encounters in black howler monkeys (Alouatta pigra) and tufted capuchin monkeys (Sapajus nigritus). Black howlers responded with longer vocal displays during encounters with neighbours with an equal number of resident males, while tufted capuchins increased their participation with increasing relative male group size. Within each species, males and females responded similarly to varying numerical odds, suggesting that despite pay-off asymmetries between males and females, both sexes were similarly influenced by numerical asymmetries in deciding to participate in collective group defence. Whereas the outcome of contests among tufted capuchins was determined by relative male group size, reflected in a pronounced intergroup dominance hierarchy, the absence of dominance relationships among black howler groups may have provoked prolonged vocal displays in order to assess rival groups with matching competitive abilities.

Female participation in collective group defense in black howler monkeys (Alouatta pigra).

Many group-living animals actively defend a home range against neighboring groups. In many of these societies, males are the primary participants during group defense, while female participation ranges from seldom to frequent. Among howler monkeys (Alouatta spp.), loud calls (i.e., howling) are often used in the context of intergroup spacing as a form of cooperative group defense. Males initiate and lead these howling bouts, but females occasionally participate as well. During a 28-month study, I examined social and ecological factors influencing the participation of adult females in naturally occurring howling bouts of five multimale-multifemale groups of black howler monkeys (A. pigra) at Palenque National Park, Mexico. I calculated the percentage of time each female participated during howling bouts for which the participation of all resident females could be recorded ≥80% of the time (N = 287). At least one female was observed to participate in 53% of the vocal displays. Female participation was significantly greater during howling bouts that were part of visual intergroup encounters compared to spontaneous calls or calls in response to nearby calls when there was no visual contact with rival groups. Female calling behavior was not influenced by the presence of infants vulnerable to infanticide or by the proximity to food resources. Nonetheless, in four of the five study groups, one female called significantly more than the other resident female(s), suggesting that these females played a special role within the group's social dynamics, not previously recognized for this species.

The function of loud calls in black howler monkeys (Alouatta pigra): food, mate, or infant defense?

Loud calling (i.e., howling) is the single most distinctive behavioral attribute of the social system of howler monkeys (Alouatta spp.), yet no general consensus exists regarding its main function. During a 28-month study of five groups of black howler monkeys (Alouatta pigra) at Palenque National Park, Mexico, we examined whether howling mainly functioned in the defense of food resources, mates, or infants vulnerable to infanticide. We recorded 602 howling bouts. Howling occurred more frequently when monkeys were feeding, particularly on fruits, and less frequently when they were resting than would be expected by chance. Furthermore, howling was concentrated in areas of the home range in which major feeding sites were located. Howling did not occur more frequently when vulnerable infants or potentially fertile females were present versus absent, nor did the howling rate increase with an increasing number of vulnerable infants or potentially fertile females in the group. Howling bouts lasted on average 14.4 ± SE 0.5 min, and call duration was not influenced by the presence of vulnerable infants or potentially fertile females. The duration of spontaneous calls, however, was positively correlated to the percentage of feeding time in the vicinity of howling locations. In addition, vocal displays lasted longer when neighboring groups and extragroup males were within visual contact compared with spontaneous calls and calls in response to nearby calls in which there was no visual contact between callers. Our findings suggest that loud calls in black howler monkeys are multifunctional, but most frequently occur in the defense of major feeding sites. These calls also may function in the defense of infants and mates during encounters with extragroup males.

A comparison of scan and focal sampling for the description of wild primate activity, diet and intragroup spatial relationships.

We used data collected during two concurrent studies of black howler monkeys (Alouatta pigra) in Palenque National Park, Mexico, to compare systematically three methods of behavioral data collection [group activity scan sampling (group scans), instantaneous focal individual sampling (instantaneous focals) and continuous focal individual sampling (continuous focals)] and three methods of proximity data collection [group proximity scan sampling (group proximity scans), focal individual proximity scan sampling (focal proximity scans) and instantaneous focal individual nearest neighbor sampling (focal nearest neighbor samples)]. We conducted pairwise comparisons of data among methods using Pearson correlations and one-sample t tests. A series of Kruskal-Wallis tests were performed to compare the activity and proximity patterns of adult males, adult females and juveniles described by each method. The three behavioral data collection methods generally provided similar information about activity and diet. However, important differences for both activity and proximity data existed among methods. Instantaneous focals overestimated the percentage of time spent in social interactions, while group scans overestimated time spent moving and underestimated time spent feeding. Group proximity scans and focal proximity scans provided similar spatial data, while focal nearest neighbor samples were more appropriate for determining the influence of one individual on another at any given moment. These biases suggest the importance of deliberate method selection during project design and highlight the need for taking methods into account when comparing studies.

Genetic structure and kinship patterns in a population of black howler monkeys, Alouatta pigra, at Palenque National Park, Mexico.

We investigated the genetic structure and kinship patterns of black howler monkeys (Alouatta pigra) at Palenque National Park, Mexico. Fecal samples from 49 individuals residing in eight social groups were successfully genotyped for 19 polymorphic microsatellite markers known to be variable in other ateline primates. Overall, genetic diversity was low (H(o) = 0.588) with an average of 4.2 alleles per loci (range = 2-8). We found that intergroup genetic variation among adults was relatively high (mean between-group F(ST) = 0.119), largely due to the genetic divergence of one study group from the others. Intragroup kinship patterns showed that in most social groups, either adult males, adult females, or individuals of both sexes resided with same-sexed adult kin, suggesting that some black howler males and females may not disperse from their natal group or may disperse with related individuals. Of the six sampled immigrant males, two males joined established groups by themselves, and four males formed two pairs that each took over the social group they joined after evicting the resident males. Males in both these coalitions were genetically closely related, while the two solitary immigrants were not closely related to any of the resident males present in the group they joined.

Observed infanticides following a male immigration event in black howler monkeys, Alouatta pigra, at Palenque National Park, Mexico.

This study describes two cases of directly observed and one case of nearly observed infanticide after an adult male immigrated into a multimale-multifemale group of black howler monkeys (Alouatta pigra) at Palenque National Park, Mexico. The immigrant male entered the group alone, injured the central adult male, presumably evicted the noncentral adult male, and killed all three young infants present over the course of three consecutive days in February 2010. Three weeks after the infanticide events, the three adult females who lost their infants were observed to sexually solicit and copulate with both the infanticidal male and the injured central male. Multimale mating is an effective reproductive strategy that females employ to confuse paternity and reduce the risk of infanticide, but the extent to which promiscuous mating after infanticide events is part of a counterstrategy in this species is still unknown. More cases of infanticide will need to be observed to assess the degree to which infanticide avoidance shapes the social system of the black howler monkey.

Sexual behavior across ovarian cycles in wild black howler monkeys (Alouatta pigra): male mate guarding and female mate choice.

We studied two multimale-multifemale groups of black howler monkeys (Alouatta pigra) during a 14-month study (June 2006-July 2007) in Palenque National Park, Mexico to evaluate the ways in which their sexual behavior changes across ovarian cycles. We analyzed 231 fecal samples, collected every 2.2+/-1.4 days from five females. For four females, estradiol and progesterone profiles revealed an average (+/-SE) cycle length of 18.3+/-1.4 days. Copulations occurred significantly more frequently during the periovulatory period (POP), defined as the estimated day of ovulation +/-3 days (N=18). This was largely the result of cycling females soliciting sexual interactions during their POPs. Females directed their solicitations significantly more often toward "central" males of their group, who had close spatial associations with females at other times, compared with "noncentral" males, who did not associate closely with females. Central males rarely solicited sexual interactions, but instead monitored the females' reproductive status by sniffing their genitals, and maintained significantly closer proximity to females during their POPs, suggesting male mate guarding when conceptions are most likely to occur. Our findings indicate that the reproductive strategies of black howler central males and females coincide, highly skewing mating opportunities toward central males. Black howler females, however, occasionally choose to copulate with noncentral resident males or extra-group males during their POPs, undermining the ability of central males to monopolize all reproductive opportunities.

Group size and composition influence male and female reproductive success in black howler monkeys (Alouatta pigra).

It has been argued that grouping patterns might influence the reproductive performance of individuals. Increasing group size results in greater travel costs and competition over depletable food resources, which could lead to reduced individual reproductive success. However, in groups with an increasing number of males, female reproductive success is predicted to augment because larger male groups might better protect immatures from infanticidal attacks. In contrast, male reproductive success is predicted to decrease with number of males in a group because fertilization cannot be shared between males. In this paper, we test these predictions on the Mesoamerican black howler monkey (Alouatta pigra) with data on group size and composition for 120 groups from eight populations of black howler monkeys existing in eight protected forests in Mexico and Guatemala. Male and female reproductive success were calculated as a deviation of the observed number of infants (or immatures) from the expected number of infants (or immatures), relative to the number of males and females in a group. Results indicate that both male and female reproductive success decreased with group size. Male reproductive success decreased with an increasing number of males in a group and with increasing proportion of males relative to females in a group. Decreased female reproductive success was associated with increasing number of females in a group, and female reproductive success had a tendency to increase with increasing number of males in a group. These results suggest that in black howler monkeys, living in larger groups might negatively affect the reproductive success of each member. Our findings are similar to those reported for a population of a sister species, Alouatta palliata, living in larger groups.