Red Howler Research Articles

Frugivory and seed dispersal by Red Howler Monkeys : Evolutionary aspect

L’analyse des caractéristiques morphologiques des fruits consommés par les singes hurleurs roux (Alouatta seniculus), en Guyane française, montre que les hurleurs choisissent préférentiellement des fruits pulpeux, de coloration vive et comprenant un petit nombre de graines bien protégées. Cependant, les primates peuvent être associés à la dissémination d’espèces dont les fruits ont soit une enveloppe externe indurée et indéhiscente que seuls les mammifères peuvent ouvrir à l’aide de leurs dents, soit des graines de grande taille que les oiseaux, les chauves-souris ou les autres petits animaux frugivores ne peuvent ingérer. Les fruits de Sapotaceae présentent simultanément les deux caractéristiques ; cette famille est, de plus, dominante dans le régime alimentaire des hurleurs à la Station des Nouragues. Nous avons également observé que le singe hurleur est, probablement avec les autres primates frugivores comme le singe araignée (Ateles paniscus), l’un des principaux consommateurs et disséminateurs des Sapotaceae sur le site d’étude. L’analyse du peuplement de plantules sous les dortoirs des singes hurleurs a montré qu’ils étaient des disséminateurs efficaces, en particulier pour cette famille végétale. Par ailleurs, les singes hurleurs ont un mode agrégatif de dissémination des graines qui pourrait être à l’origine de la répartition par taches de la plupart des Sapotaceae. Toutes ces observations permettent d’envisager l’existence d’une « coévolution diffuse » entre les primates et les fruits de Sapotaceae.

Diet of the red howler monkey (Alouatta seniculus) in French Guiana

We report the feeding behavior and food preferences of a troop of red howler monkeys (Alouatta seniculus) over two annual cycles in primary tropical rain forest in French Guiana. The monkeys used 195 plant species from 47 families as food. Major food categories were young leaves (54%), mature fruits (21.5%), and flowers (12.6%). Other food categories included old leaves, immature fruits, termitarium soil, bark, and moss. The monkeys were less selective than other howler groups, since 19 plant species contributed ≥1% to their diet and accounted for only 35.7% of their total diet. The Sapotaceae was the most frequently eaten plant family and represented >10% of the total diet.

Evolution of pro‐protamine P2 genes in primates

Protamines P1 and P2 form a family of small basic peptides that represent the major sperm proteins in placental mammals. In human and mouse protamine P2 is one of the most abundant sperm proteins. The protamine P2 gene codes for a P2 precursor, pro-P2 which is later processed by proteolytic cleavages in its N-terminal region to form the mature P2 protamines. We have used polymerase chain amplification to directly sequence the pro-P2 genes of the five major primate families: red howler (Alouatta seniculus) is a New World monkey (Cebidae); the two macaque species, Macaca mulatta and M. nemistrina are Old World monkeys (Cercopithecidae), the gibbon, Hylobates lar, represents one branch of the apes (Hylobatidae); the orangutan, Pongo pygmaeus, gorilla, Gorilla gorilla and two species of chimpanzee Pan paniscus and Pan troglodytes represent a second ape family (Pongidae). These pro-P2 genes are compared with that of human [Domenjoud, L., Nussbaum, G., Adham, I. M., Greeske, G. & Engel, W. (1990) Genomics 8, 127-133]. The overall size and organization of the genes are conserved within the group. The mean length of pro-P2 is 101 residues, with an increase to 102 in M. nemistrina and a decrease to 99 residues in red howler (A. seniculus). In gorilla and red howler one of two 79-bp tandem repeats that occurs 3' of the gene is deleted. Of the 101 deduced amino acids examined, an amino acid change occurs in one or more primates at 45 positions. Considering only the most recently diverged group, the human/gorilla/chimpanzee clade, this represents a very high mutation rate of 0.99 changes/100 sites in 10(6) years. This rapid mutation rate is characteristic of both members of the protamine gene family, P1 and P2. Consideration of the variable nature of the sequences at the multiple sites of proteolysis during the processing of the pro-P2 indicates either that there are several processing enzymes of differing specificities, or more likely that the folded structure of the pro-P2 limits accessibility of a non-specific protease to certain exposed sites.

Male dispersal among free-ranging red howler monkeys (Alouatta seniculus) in Venezuela.

Male dispersal among free-ranging red howler monkeys (Alouatta seniculus) in Venezuela.

Passages within a discontinuous canopy: bridging in the red howler monkey (Alouatta seniculus).

Passages within a discontinuous canopy: bridging in the red howler monkey (Alouatta seniculus).

Adoption in free-ranging red howler monkeys,Alouatta seniculus of Venezuela

This report describes three cases of infant adoption in red howler monkeys (Alouatta seniculus) of Venezuela. In one case, a lactating female adopted her infant granddaughter after the infant's mother disappeared and the infant survived for the next 25 months. In the second case, an adult female adopted her infant granddaughter for nine days while the infant's mother was still a group member. In the third case, a nulliparous female temporarily adopted an infant from a neighboring group. The details and the possible reasons for these adoption are described.

Dispersal, nepotism, and primate social behavior

High degrees of relatedness within primate social groups are thought to promote the evolution of altruistic behavior via kin selection. Dispersal, for whatever reason, should limit opportunities for nepotistic behaviors. Conversely, emigration is usually attributed to the avoidance of inbreeding depression. Actual dispersal patterns may result from a balance of these forces. Systematic behavioral differences are expected between taxa that differ in such patterns. In fact, comparisons of (a) colobines vs. cercopithecines, (b) bonnet, stumptailed, and Barbary macaques vs. Japanese and rhesus macaques, and (c) red vs. mantled howler monkeys yield a perplexing blend of unexplained differences and unmet theoretical expectations. Kin selection may be less important than generally believed, and/or methodological standardization more so.

The Influence of Dispersal Patterns and Mating Systems on Genetic Differentiation within and between Populations of the Red Howler Monkey (Alouatta seniculus)

The Influence of Dispersal Patterns and Mating Systems on Genetic Differentiation within and between Populations of the Red Howler Monkey (Alouatta seniculus)

THE INFLUENCE OF DISPERSAL PATTERNS AND MATING SYSTEM ON GENETIC DIFFERENTIATION WITHIN AND BETWEEN POPULATIONS OF THE RED HOWLER MONKEY (ALOUATTA SENICULUS).

The relationship between social structure and partitioning of genetic variance was examined in two red howler monkey populations (W and G) in Venezuela, one of which (G) was undergoing rapid growth through colonization by new troops. Rates and patterns of gene flow had been determined through radiotelemetry and direct observation data on solitary migrants, and 10 years of troop censusing. Standard electrophoresis techniques were used to examine 29 loci in blood samples taken from 137 of the study animals. Analysis of genetic variance demonstrated: (1) a significantly high level of genetic variation among troops within populations (FST = 0.225 for W and 0.142 for G), and (2) a significant excess of heterozygosity within troops relative to expected (FIS = -0.136 for W and -0.064 for G), despite relatively high levels of observed and inferred inbreeding in W. Differences between the populations in FST values conformed to those predicted based on differences in colonization rate. Comparison of partitioning of genetic variance among different genealogical subsets of troops demonstrated that the pattern of genetic differentiation observed among troops within populations was promoted by an essentially single-male harem breeding structure, a very low rate of random exchange of breeding males among troops, and a high degree of relatedness among troop females. Between-troop genetic differentiation (FST ) was thereby increased relative to that expected from other types of social organization, while the correlation between uniting gametes within troops (FIS ) was decreased. Genetic differentiation between populations (2%) corresponded to that predicted from migration rates. Such a mosaic of genetic variation, combined with differences in reproductive success observed among troops and a high troop failure rate, create conditions in which interdemic selection could result in more rapid spread of advantageous gene combinations than would be expected in a panmictic population, particularly in a colonizing situation in which the founder population is small.

Chromosome studies in the red howler monkey, <i>Alouatta seniculus stramineus</i> (Platyrrhini, Primates): description of an X<sub>1</sub>X<sub>2</sub>Y<sub>1</sub>Y<sub>2</sub>/X<sub>1</sub>X<sub>1</sub>X<sub>2</sub>X<sub>2</sub>sex-chromosome system and karyological comparisons with other subspecies

In the red howler monkey, Alouatta seniculus stramineus (2n = 47, 48, or 49), variations in diploid chromosome number are due to different numbers of microchromosomes. Males exhibit a Y;autosome translocation involving the short arm of an individual biarmed autosome. Consequently, the sex-chromosome constitution in the male is X1X2Y1Y2, with X1 representing the original X chromosome, X2 the biarmed autosome (No. 7), Y1 the Y;7p translocation product, and Y2 the acrocentric homolog of 7q. In the first meiotic division, a quadrivalent with a chain configuration can be observed in spermatocytes. Females have an X1X1X2X2 sex-chromosome constitution. Chromosome heteromorphisms were observed in pair 13, due to a pericentric inversion, and pair 19, due to the presence of constitutive heterochromatin. Microchromosomes, which varied in number between individuals, were also heterochromatic. NOR-staining was observed at two separate sites on a single chromosome pair (No. 10). A comparison of A.s. stramineus with A.s. macconnelli shows that these two subspecies have identical diploid chromosome numbers (47, 48, or 49), again due to a varying number of microchromosomes, and that they share a similar sex-chromosome constitution. Their karyotypes, however, are not identical, but can be derived from each other by a reciprocal translocation. Further comparisons with other A. seniculus subspecies reported in the literature indicate that this taxon is not karyologically uniform and that substantial chromosome shuffling has occurred between populations that have been considered to be subspecies by taxonomic criteria based on their morphometric attributes.

The reproductive consequences of male cooperation in the red howler monkey: paternity exclusion in multi-male and single-male troops using genetic markers

Variance in male reproductive success in single and multi-male red howler (Alouatta seniculus) troops was examined through paternity exclusion using genetic markers. Coalitions of relatives were compared to coalitions of non-relatives with regard to duration, stability, and number of offspring expected for each participant based on paternity exclusion results. No evidence of paternity by males living outside of the troop was found. In multi-male troops, only the dominant male was found to father offspring conceived during his tenure. This was the only male observed to mount females. In both troops examined genetically wherein a status change had occurred, paternity changed with status. Coalitions of relatives and potential relatives lasted significantly longer than coalitions of non-relatives, and experienced fewer status changes between males. A direct advantage of forming a coalition for both dominant and subordinate red howler males resulted from the superior competitive ability of coalitions over single males in establishing and maintaining tenure in the limited number of female troops in the population. Although the mating success of a subordinate male in a coalition appears to be extremely low, his chances of achieving membership in a bisexual troop as a single male may be even lower. Since the majority of troops in the population during any given year were multi-male or age-graded male (85%–96%), the number of troops that a single male would be able to invade unaided was very small. A subordinate male may be able to assume dominance, particularly if he is a subadult. In coalitions in which males are related, the subordinate male will further benefit from inclusive fitness. A dominant male that forms a coalition with a relative can expect to have longer reproductive tenure than in a troop with a non-relative, thereby producing more offspring and directly enhancing his fitness. Anecdotal evidence suggests that males choose relatives over non-relatives as coalition partners when possible.

Primate species richness in relation to habitat structure in Amazonian rainforest fragments

Factors affecting species richness in fragmented habitat are often of interest to conservation programs. Groups of red howler monkeys Alouatta seniculus, white-faced sakis Pithecia pithecia and golden-handed tamarins Saguinus midas occurred in five small (approx. 10 ha) fragments of Amazonian rainforest. However, not all of these species occurred in every fragment. The purpose of this study was to identify some of the factors affecting the number and distribution of primate species among these areas. To determine whether habitat structural diversity influenced primate species richness, height, diameter at breast height (DBH) and number of trees, DBH and number of lianas (woody vines) as well as height and number of palms in 15 20 × 20 m quadrats in each fragment were recorded. Also, height and number of secondary growth plants surrounding reserves were sampled. Structurally ‘complex’ reserves had high mean number of trees, high mean number of lianas, low mean percentage large trees (> 10 cm DBH) per quadrat, and streams. These characteristics were correlated with high species richness. P. pithecia occurred in the most structurally ‘complex’ fragments, S. midas in fragments surrounded by relatively tall secondary growth and A. seniculus in all five fragments. The relationships between the habitat requirements of the three species and their occurrence in these fragments are discussed.

Inferring patterns of aggression from red howler monkey injuries.

Venezuelan red howler monkeys in a semideciduous habitat typically survive injuries and disabilities. Intraspecific physical aggression was the most frequently observed and inferred cause of injury. Thirty-eight percent of 119 howlers of all ages examined during capture had scars or other evidence of "damage." Overall, the sexes did not differ significantly in total number of injuries or number of individuals classified as "damaged." The incidence of injury was not independent of age-sex class. The subadult male class had the highest percentage of "damaged" individuals. However, when total injuries per age class were examined for each sex separately, only females showed a pattern that was significantly different than expected based on age (i.e., exposure to injury factors). Subadult females experienced more injuries than expected, whereas adult females had fewer injuries. Troop status (resident troop, natal troop, or extratroop) was not significantly related to the number of injuries in adult and subadult males. Thin finding was not surprising, because adult and subadult males of all status classes are involved in aggression related to breeding competition. Extratroop females had more injuries than expected, and natal females had the fewest injuries. The higher incidence of injuries on subadult females and extratroop females is consistent with aggression-mediated emigration of some females and observed resistance to female immigration by resident females. Overall, 74% of injuries were located on anterior-ventral portions of the body, consistent with the face-to-face fighting observed in howlers. Sociobiological costs of aggression in red howlers are difficult to assess because many howlers, despite frequent and severe injury, subsequently survive and reproduce. We recommend caution in inferring mortality from injuries, especially when social mobility and emigration out of the study area are common.

Positional behavior and limb bone adaptations in red howling monkeys (Alouatta seniculus).

Morphological adaptations to climbing (a scansorial mode of quadrupedal, arboreal locomotion practised on twigs and small branches) are identified by relating anatomical details of limb bones to a sample of 6,136 instantaneous observational recordings on the positional behavior and support uses of 20 different free-ranging, adult red howlers. Our findings are used to infer the original habitat in which proto-red howlers may have acquired such adaptations and to hypothesize that climbing and its related anatomy are a primitive condition for anthropoids.

Red howler monkey birth data I: Seasonal variation.

A large set of birth data from a population of red howler monkeys (Alouatta seniculus) in two habitats found a consistent birth "dip," with births occurring less frequently in early wet season (May-July) than during the remaining months. In one of two habitats, births were negatively correlated with rainfall, and viable conceptions were positively correlated with rainfall. The observed degree of within-troop birth synchrony appeared to reflect populational synchrony with environmental factors. Correlations between births and the phenology of plant foods were not striking, but there was weak support for the hypothesis that births are timed to maximize the availability of weaning foods. Reduced births in early wet season also minimize the number of Infants who would experience the transition to independent locomotion and feeding during the peak of the dry season when probable low moisture content of foods and high daytime temperatures might be disadvantageous. However, there was no relationship between season of birth and infant mortality.

Red howler monkey birth data II: Interannual, habitat, and sex comparisons.

Data presented in this paper are derived from the births and subsequent histories of red howler infants born in two habitats. Overall the sex ratio of infants at birth was about 1:1. Infant survivorship (at 1 yr) was about 80%, and 44% of infant mortality was attributed to infanticide by males. Survivorship curves indicated a dramatic sex difference, with far fewer females than males known to be alive at age 7 yr. However, this sex difference may be inflated because emigrant males are more easily identified than emigrant females, and females may be dispersing beyond the boundaries of the study area at a higher rate. Annual birthrate varied somewhat from year to year and was positively related to rainfall. Annual birthrate tended to be higher in the habitat with lower density and higher growth rate. Consistent with the trends, in annual birthrate, variation in interbirth interval length (TBR after births of surviving infants was related primarily to habitat differences and annual variation in rainfall. Season of birth and maternal age class had no effect on IBI. Infant sex had mostly nonsignificant effects on IBI. A small sample indicated that IBI's were significantly longer after the births of females who eventually became natal breeders than after the births of females who eventually emigrated. This difference might reflect differential parental (maternal) investment of some sort.

The significance of call duration in howler monkeys

The “loud” calls of forest primates consist of repeated sounds that elicit a response from other members of the species. Recent studies suggest that these calls are often displays by the males that permit them to assess the strength of their opponents. Previous research on red howler monkeys supported the hypothesis that howling functions in assessment of competing individuals, as an alternative to energetically expensive chases and fights. As the second step in the attempt to understand the evolution of howling in genus Alouatta,one aspect—call duration — was compared in two species,the mantled howler (Alouatta palliata)and the red howler (A. seniculus).In A. palliatathe median howl duration was 3.5 sec and the interhowl interval was 20.0 sec, while in A. seniculusthe median howl duration was 19.0 sec and the interhowl interval was 3.0 sec. During the dawn chorus, the total duration of calling in A. seniculusmay be 10 or more times greater than that in A. palliata.The latter species appears to be limited in the duration of howls it can produce, so it increases the amount of calling by reducing the interhowl interval. At least four factors may be important in the evolution of the observed differences in call structure: constraints of the acoustic environment, alternate forms of display used by A. palliata,the presence or absence of competing males within the troop, and the effect of female calls on male howling. The observations suggest that the use of the male loud call may reflect differences in the nature of male-male competition and female support more than it reflects the constraints of the acoustic environment.

Loud calls of adult male red howling monkeys (Alouatta seniculus).

Loud calls of adult male red howlers (Alouatta seniculus) inhabiting a deciduous and semideciduous open woodland site in Venezuela were recorded opportunistically and categorized by ear and sonographically as barks and roars. Five to six different bark syllables were identified as occurring singly or in sequences of doublets and triplets. In barks, spectral energy was concentrated in bands at 350-400 Hz, 900-1,100 Hz, 1,800-2,200 Hz and 3,000-3,500 Hz, but not all higher bands were present in each syllable. Roars appeared sonographically like prolonged barks composed of a pulsated preface, a long legato climax and a brief, fractionated and at times pulsated coda; each part varied internally to the ear and in acoustic structure. All loud calls were of the noisy type (nonharmonic energy over a broad frequency range). Acoustic characteristics of the calls are interpreted in terms of the subserving vocal tract anatomy. I compare loud calls of red howlers with those of mantled (A. palliata) and black (A. caraya) howlers.

Dominance Rank, Secondary Sex Ratio, and Reproduction of Offspring in Polygynous Primates

One question in evolutionary biology which is central to understanding reproductive strategies and parental efforts at rearing offspring is why organisms produce certain offspring sex ratios (Trivers and Willard 1973; Charnov 1982). Fisher (1930) argued that since each individual has a mother and a father, both sexes contribute genes equally to the next generation. All else being equal, if members of one sex were overproduced, their ability to reproduce would be limited by the availability of members of the less abundant sex and natural selection would favor any predisposition to produce offspring of the less abundant sex. In this fashion, Fisher reasoned, selection would adjust the offspring sex ratio in an outbreeding population until total parental investment (PI, Trivers 1972) in the two sexes was equal. Fisher (1930) assumed, but did not clearly state, that all parents were alike in their ability to rear reproductively successful sons and daughters (Patterson and Emlen 1980). A model proposed by Trivers and Willard (1973), however, specified how deviations from equal PI may be favored by natural selection according to the influence of maternal condition on the reproduction of offspring. The TriversWillard model proposed that in polygynous species if some condition of mothers (e.g., dominance rank) influences the condition and, as a result, the reproductive success (RS) of sons more than daughters, then selection should result in the evolution and maintenance of mechanisms by which females in poor condition invest less in sons than daughters and/or females in good condition invest more in sons than daughters. This model is particularly relevant for primates, since the majority of species are polygynous (Clutton-Brock and Harvey 1977). Since the dominance rank of a monkey's social group and family has a strong

Besprechungen/Reviews

Book reviewed in this article:Zeitschriften/Periodicals: Reinhardt, V., und A. ReinhardtZeitschriften/Periodicals: Losey, G. S. Jr. (1982): Ecological cues and experience modify interspecific aggression by the damselfishZeitschriften/Periodicals: Sekulic, R. (1982): The function of howling in red howler monkeysZeitschriften/Periodicals: Nijssen, A. (1982): The relation between the eating system and the grooming system in ratsZeitschriften/Periodicals: Sordahl, T. A. (1982): Antipredator behavior of American avocet and black‐necked stilt chicksZeitschriften/Periodicals: Muszalski Shy, M. (1982): Interspecific feeding among birdsZeitschriften/Periodicals: Burkhardt, D. (1982): Birds, berries and UV. A note on some consequences of UV vision in birdsZeitschriften/Periodicals: Beilharz, R. G., und K. Zeeb (1982): Social dominance in dairy cattleZeitschriften/Periodicals: Porter, F. L., und G. F. McCracken (1983): Social behavior and allozyme variation in a captive colony of Carollia perspicillataZeitschriften/Periodicals: Krebs, J. R., und N. B. Davies (1981): Öko‐Ethologie (Behavioural ecology)Zeitschriften/Periodicals: Voith, V. L., and P. L. Borchelt, eds. (1982): Symposium on animal behavior