Social modulation of testosterone levels in male black howlers (Alouatta pigra)

The influence of social factors on the modulation of male testosterone levels has been demonstrated among several vertebrate species. In addition to sexual activity, parental care and reproductive competition affect testosterone secretion. We examined variations in testosterone levels among male black howlers (Alouatta pigra) in various social contexts. Fecal samples were collected from nine males living in five different groups in the Mexican state of Campeche. The potential for intragroup and extragroup competition varied among the groups. The number of resident males living in the groups was the only variable that significantly explained variations in testosterone levels. Males living in unimale groups had higher testosterone levels; the highest testosterone levels were recorded for males that had experienced a shift from multimale to unimale group compositions. In this species, the probability of being challenged by extragroup males and evicted from the group during immigration events increases when males live in unimale groups. Therefore, our results suggest that male black howlers respond to competition for group membership by increasing their testosterone levels. In this context, testosterone secretion represents an anticipatory response to reproductive conflicts. Therefore, although males living in unimale groups have exclusive access to females, they face higher physiological costs associated with sustaining high testosterone levels for extended time periods.     

Departure of juvenile malePresbytis entellus from the natal group

Five bisexual groups (four unimale and one multimale) were studied at Ambagarh Reserve Forest from 1985 to 1987 in relation to factors influencing departures of male juveniles from their natal troops. Of 20 male juveniles observed, 11 left their natal groups, 4 died or disappeared, and 5 remained. The male juveniles left their natal groups only after a takeover by a new adult male. The weaned juvenile males either were chased away by the new adult male or left voluntarily.     

Population Size and Characteristics of <Emphasis Type="Italic">Alouatta pigra</Emphasis> Before and After a Major Hurricane

Although some environmental risks and resources are known to affect the evolution of primate social groups, we know little about the effect of major natural disturbances on primate populations. Hurricane Iris hit the Monkey River watershed in southern Belize in October 2001, presenting a unique opportunity to document the effects of a natural disaster under circumstances wherein some pre-hurricane data were available. We measured the characteristics of the population of black howlers in the affected forest 3.5 years after the storm and compared the population data with pre-hurricane data from a 52-ha study area, that may represent the larger continuous riverine forest and from which all monkeys were known. From February to May 2004, we sampled 28.77 km² of the 96-km² forest fragment via five transects walked 12 times each. From these data we estimate that the population in the watershed has dropped from 9784 to 1181 monkeys, a reduction of 88%, reflected by both a 79% drop in the number of social groups and a 38% reduction in group size. Before the storm, 75% of the social groups were multimale; after the storm, 74% of the groups were unimale. While the ratio of adult females to males improved slightly, the ratio of adults to immatures, and adult females to immatures more than doubled, indicating a much lower potential for growth. These data provide a quantitative assessment of how a major natural disturbance can affect a primate population.     

Male Competition,Mating Success and Female Choice in a Seasonally Breeding Primate (Erythrocebus patas)

Mammals with restricted breeding seasons often show brief but intense bouts of male competition for mates and male reproductive success has been attributed to male competitive abilities, with the most aggressively successful males able to control access to fertile females, or with females choosing to mate with such males. We studied male competition, mating behaviour and female mate selection in patas monkeys, a primate with a restricted breeding period. We observed two habituated patas groups in Laikipia District, Kenya, during Jun.-Aug. 1983. During the study, one group had a single resident male while the other group had multiple adult males. Within the multimale group, experienced adult males were no more successful than the subadult male. The sole resident male had a significantly higher rate of fights won (p < 0.02) although he did not differ from the multimale group males in rate of aggression or initiation of fights. We found no significant differences in either mating success or female preference based on males' experience or residency. The rates at which males copulated with and were solicited by females were not significantly correlated. We found no evidence of stable dominance ranks among males in the multimale group and aggressive success was not significantly correlated with copulation rate for males in the multimale group. Subadult males were responsible for the majority of copulations observed during the final third of the breeding season. Our observations of this patas population showed a fluid number of males in groups, with the same groups able to shift rapidly from single to multimale structure. This fluidity may result from the large fluctuations in numbers of breeding-age males and females observed over 4 yr of studying this population.     

Shifts in Social Structure of Black Howler (Alouatta pigra) Groups Associated with Natural and Experimental Variation in Population Density

We examined variation in the group structure of black howlers (Alouatta pigra) using the adult composition of 48 social groups. We compared the structure of groups at 5 sites with different population densities and variation in group structure over time with rising population density. In addition, we examined changes in the group structure of monkeys that were translocated from an area of high population density to an area with a much lower population density. We found at low population densities, groups comprised either heterosexual pairs or a single male with two females. At high population densities groups tended to be multimale and often contained >2 adult females. We suggest the relative costs and benefits of dispersal by maturing adults varies with population density, and in Alouatta pigra results in a shift from single to multimale groups of larger size with increasing population density.     

Number of males in primate groups: Comparative tests of competing hypotheses

Primate social groups frequently contain multiple males. Male group size has been hypothesized to result from male mating competition, but the selective factors responsible for the evolution of multimale groups are unclear. Short breeding seasons create situations that are not conducive for single males to monopolize mating access to females, and may therefore favor the formation of large male groups. Alternatively, since the costs of mate defense increase with the spatial clumping of females, female group size may be a primary determinant of the number of males in a primate group. We used comparative methods designed to control for the potentially confounding effects of hidden third variables associated with phylogeny to test the breeding season and female group size hypotheses for the evolution of multimale groups. Our results revealed no association between breeding season duration and the number of males in groups. In contrast, we provide support for the female group size hypothesis by demonstrating a strong pattern of correlated evolution between female and male group size. © 1996 Wiley-Liss, Inc.     

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.     

Growth of Mantled Howler Groups in a Regenerating Costa Rican Dry Forest

We examined population dynamics in mantled howlers (Alouatta palliata palliata) in a regenerating tropical dry forest in Santa Rosa National Park (SRNP), Costa Rica. The population has grown at a rate of about 7% per annum during the past decade. The growth in numbers from 342 in 1984 to 554 in 1992 reflects an increase in the number of groups (from 25 to 34) and a slight increase in their average size (from 13.6 to 16.3). Population density has increased from 4.9 to 7.9 individuals per km ². Santa Rosa's population density and group compositions are similar to those at several other mantled howler sites, but densities of mantled howlers are much higher at two other well-studied sites: La Pacifica and Barro Colorado Island (BCI). We relate the low density of howlers at Santa Rosa to local historical and ecological factors. Howler populations at high and low densities differ in average group size and sex ratio. At high population densities, groups are larger and include more adult females. The number of male howlers per group appears to be more strictly limited and less variable than the number of females is. However, there is greater variation in male group membership at Santa Rosa than at La Pacifica or BCI, and at Santa Rosa there are more generating forests available into which males and females can disperse and form new groups. We present case studies describing two ways in which new howler groups are formed, and we suggest that, compared to females and compared to males at high density sites, males are relatively advantaged in the uncrowded habitats at Santa Rosa and other low density sites.     

Survey of the black howler monkey,<Emphasis Type="Italic">Alouatta pigra</Emphasis>, population at the Mayan site of Palenque,Chiapas, Mexico

A survey of the population of the black howler monkey (Alouatta pigra) present at the Mayan site of Palenque was conducted during 2000. A total of 911 man/hours, spread over 112 days were spent surveying the 600 ha area of pristine forest at the site for howler troops. We detected the presence of 136 individuals of which 131 were members of 20 troops, the rest were 3 solitary adult males and 2 adult males travelling as a pair. Ecological density was estimated at 23 individuals/km². Mean troop size was 7.0 individuals and it ranged from 2–12 individuals; 60% of the troops were multimale. All sighting of howler monkeys were in evergreen rain forest and 75% were in trees ≥20 m in height. The reported densities and mean troop size are higher than those reported for the species in Guatemala and in central Quintana Roo, Mexico. The vegetation of the forest contains tree species reported to be used by species ofAlouatta in the Moraceae, Sapotaceae, Leguminosae, and Lauraceae plant families. Protection of a large perimeter area (ca 1700 ha) around the archeological site by the Mexican government ensures the conservation of the forest and of the black howler monkey population present at the site.     

Abnormal Pelage Color in an Isolated Population of <Emphasis Type="Italic">Alouatta guariba clamitans</Emphasis> Cabrera, 1940 in South Brazil

We located 4 brown howlers (1 adult male, 2 adult females, and 1 juvenile male) showing abnormally lighter pelage in 3 social groups comprising 5, 6, and 9 individuals in a 20 ha-forest fragment in the State of Rio Grande do Sul, Brazil. Two additional groups composed only of normally colored individuals also live in the fragment, which is isolated from nearby fragments by 267–1009 m. They were the only brown howlers with abnormal pelage color out of a total of 386 individuals belonging to 67 groups in 21 fragments in the 5876-ha study area. The isolation of the forest fragment, its high howler density (2.2 individuals⁄ha), and large group size (8.8 ± 2.4 individuals) may decrease the likelihood of successful immigration into the population, leading to an increased probability of inbreeding that may facilitate the expression of rare alleles.     

Resource distribution and group size in the common langur Semnopithecus entellus in southern India

We investigated the influence of resource abundance and distribution on the group size and composition of the common langur Semnopithecus entellus in the contiguous forests of Bandipur National Park, Mudumalai Wildlife Sanctuary and Nagarahole National Park in southern India. We also explored any additional effect of predator pressure and the risk of take-over on the same attributes. Data on group composition and vegetation were collected from January to May 2006. The size and composition of 94 bisexual groups were obtained. The group size varied from 7 to 40 and the groups included unimale and multimale groups. Thirty-five all-male groups were encountered. Vegetation was sampled from 17 grids of dimension 1 km x 1 km, each containing twelve 25 m x 25 m plots. The list of food species was compiled from previous studies and observations made during the study period. The mean basal area of all the food trees within each plot and its coefficient of variation at the level of the grid were used to represent resource abundance and distribution, respectively. The number of adult females and males within groups were analyzed separately to test for differential effects on age-sex categories. Group size increased as resources became spatially more heterogeneous. The abundance of resources had a negative effect on group size. This study did not find evidence supporting the direct effect of predator presence or of the risk of take-over. Contrary to what were expected, adult males reacted more strongly and predictably to resources than did adult females. The group attributes and their relationship with food resource abundance and distribution differed between two sites in the study area possibly owing to langur subspecies differences.     

Subgrouping Patterns in a Group of Wild <Emphasis Type="Italic">Cebus apella nigritus</Emphasis>

Seasonal patterns of group fragmentation, including the size of subgroups and percentage of time spent in subgroups, may provide information on individual decision-making in response to resource distribution. Age-sex class composition of subgroup membership can offer insights into the social dynamics of the group as a whole. At most field sites, capuchins (Cebus spp.) form stable groups with no evidence of group fragmentation. Here I describe seasonal subgrouping patterns, including proportion of time spent in subgroups, subgroup size, age-sex membership, dyadic fidelity, stability of membership, and the effect of subgrouping on individual foraging efficiency, in a group of wild Cebus apella nigritus. From September 1996 to August 1997 the study group at the Estação Biológica de Caratinga, Brazil divided into 148 different subgroups, on 99 of 194 census days. In contrast to expectations for subgrouping patterns as a response to seasonal distribution of resources, the proportion of days spent in subgroups did not vary significantly by season. Subgroup composition was relatively fluid, with multimale multifemale subgroups the most common throughout the year. Unimale multifemale subgroups were restricted to the wet season; in contrast, all-male subgroups and unimale unifemale subgroups occurred in the dry season. For both males and females, low rank predicted membership in smaller subgroups. For males, but not females, subgrouping coincided with increased foraging efficiency, as measured by increased time spent ingesting food and decreased time spent traveling on days with subgrouping compared to days with the group in a cohesive unit.     

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. Am. J. Primatol. 71:153–164, 2009. © 2008 Wiley‐Liss, Inc.     

Demography of fluctuating prairie vole populations: comparison of demographic variables among phases of fluctuations

We tested for differences in the proportion of reproductively active males and females, proportion of the population composed of young and immigrants, and monthly survival (total, adult, young) among phases (trough, increase, and decline) and among habitats (alfalfa, bluegrass, and tallgrass) of 30 population fluctuations ofMicrotus ochrogaster Wagner, 1842 over 25 years in east-central Illinois USA. Total population survival and survival of adults and young were greatest during the increase phase, among fluctuations, irrespective of habitat. The proportion of reproductively active adult males and females was lowest during the decline phase, an effect of lower reproduction during the winter. These results suggest that phase-specific changes in survival were the primary demographic factor driving population fluctuations ofM. ochrogaster in our study sites. We conclude that small-scale spatially different population fluctuations may be explained by the same mechanisms that explain fluctuations within a population.     

Impact of Male Infanticide on the Social Structure of Mountain Gorillas

Infanticide can be a major influence upon the social structure of species in which females maintain long-term associations with males. Previous studies have suggested that female mountain gorillas benefit from residing in multimale groups because infanticide occurs when one-male groups disintegrate after the dominant male dies. Here we measure the impact of infanticide on the reproductive success of female mountain gorillas, and we examine whether their dispersal patterns reflect a strategy to avoid infanticide. Using more than 40 years of data from up to 70% of the entire population, we found that only 1.7% of the infants that were born in the study had died from infanticide during group disintegrations. The rarity of such infanticide mainly reflects a low mortality rate of dominant males in one-male groups, and it does not dispel previous observations that infanticide occurs during group disintegrations. After including infanticide from causes other than group disintegrations, infanticide victims represented up to 5.5% of the offspring born during the study, and they accounted for up to 21% of infant mortality. The overall rates of infanticide were 2–3 times higher in one-male groups than multimale groups, but those differences were not statistically significant. Infant mortality, the length of interbirth intervals, and the age of first reproduction were not significantly different between one-male versus multimale groups, so we found no significant fitness benefits for females to prefer multimale groups. In addition, we found limited evidence that female dispersal patterns reflect a preference for multimale groups. If the strength of selection is modest for females to avoid group disintegrations, than any preference for multimale groups may be slow to evolve. Alternatively, variability in male strength might give some one-male groups a lower infanticide risk than some multimale groups, which could explain why both types of groups remain common.     

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.     

Population regulation in the Wood Mouse Apodemus sylvaticus (L.)

Watts 1969 described the population cycle of the Wood Mouse Apodemus sylvaticus as a decline in numbers in spring, a stable period in summer and an increase phase in autumn. Aggression by adult males was considered an important aspect of population regulation limiting male survival in spring and juvenile recruitment in summer. However, recent studies of range behaviour and experimental investigations suggest that male A. sylvaticus are not relevant in population regulation and that the principal regulating factors act on female reproductive success. Female reproductive activity is determined by spatial interactions which, in turn, are determined primarily by the density of females and the proportion of female immigrants in the population. The only impact adult males may have on population size is through infanticide and competition with the females for food.     

Reproductive resilience to food shortage in a small heterothermic primate

The massive energetic costs entailed by reproduction in most mammalian females may increase the vulnerability of reproductive success to food shortage. Unexpected events of unfavorable climatic conditions are expected to rise in frequency and intensity as climate changes. The extent to which physiological flexibility allows organisms to maintain reproductive output constant despite energetic bottlenecks has been poorly investigated. In mammals, reproductive resilience is predicted to be maximal during early stages of reproduction, due to the moderate energetic costs of ovulation and gestation relative to lactation. We experimentally tested the consequences of chronic-moderate and short-acute food shortages on the reproductive output of a small seasonally breeding primate, the grey mouse lemur (Microcebus murinus) under thermo-neutral conditions. These two food treatments were respectively designed to simulate the energetic constraints imposed by a lean year (40% caloric restriction over eight months) or by a sudden, severe climatic event occurring shortly before reproduction (80% caloric restriction over a month). Grey mouse lemurs evolved under the harsh, unpredictable climate of the dry forest of Madagascar and should thus display great potential for physiological adjustments to energetic bottlenecks. We assessed the resilience of the early stages of reproduction (mating success, fertility, and gestation) to these contrasted food treatments, and on the later stages (lactation and offspring growth) in response to the chronic food shortage only. Food deprived mouse lemurs managed to maintain constant most reproductive parameters, including oestrus timing, estrogenization level at oestrus, mating success, litter size, and litter mass as well as their overall number of surviving offspring at weaning. However, offspring growth was delayed in food restricted mothers. These results suggest that heterothermic, fattening-prone mammals display important reproductive resilience to energetic bottlenecks. More generally, species living in variable and unpredictable habitats may have evolved a flexible reproductive physiology that helps buffer environmental fluctuations.     

Infant–Nonmother Interactions of Free-Ranging Mantled Howlers (Alouatta palliata) in Costa Rica

Proximate and ultimate explanations of interactions between infants and nonmothers vary depending upon the relatedness of the interactors. We investigated interactions of infants and nonmothers from a 22-month continuous study and from the long-term monitoring of the mantled howler population of La Pacifica, Guanacaste Province, Costa Rica. Relatedness is low or absent in these mantled howler groups. Juvenile females appeared to practice care skills with older infants, but as most first infants died, they failed to benefit. Infant positive interactions with adults occurred with the mother and probable father. Other adult females behaved aggressively toward the youngest infants. Mothers were retentive of infants and responded negatively to these interactions, suggesting that they perceived them as threatening. Interactions with infants appear to reflect competition in groups of unrelated adults. A review of other populations of Alouatta palliata and other species of howlers indicate variability in social group size and suggest variability in intragroup relatedness. We suggest that further study will confirm that social behavior (including interactions with infants) will vary by resource availability (group size) and associated demographic patterns (male and female migration) that affect relatedness in howler social groups.     

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.