Taxonomy of theAlouatta seniculus group: Biochemical and chromosome data

Wild populations ofAlouatta belzebul andA. seniculus from Brazil were surveyed in relation to 20 protein loci. Estimates of genetic variability demonstrated thatA. seniculus presents the highest level of heterozygosity among several New World monkey species studied for the same loci. Additional information from DNA and chromosomes suggest thatA. seniculus andA. belzebul are not the closest species in theHershkovitz’sAlouatta seniculus group.     

Genetic structure of an isolated population of mantled howler monkeys (Alouatta palliata) on Barro Colorado Island, Panama

Habitat fragmentation may influence genetic variability through reductions in population size and the physical isolation of conspecifics. We explored the effects of these factors on genetic diversity in a population of mantled howler monkeys (Alouatta palliata) on Barro Colorado Island (BCI), Panama. The study population was established in 1914 when an unknown number of resident individuals were isolated from the surrounding mainland by damming of the Río Chagres to create the Panama Canal. Analyses of 10 microsatellite loci indicated that, despite this isolation, the howler monkeys on BCI exhibit levels of genetic diversity (H _S = 0.584 ± 0.063) among the highest reported for any species of Alouatta. These data also revealed that although relatedness among adults in a social group was significantly greater than zero, the BCI population is not highly genetically structured. Tests for genetic bottlenecks based on departures from equilibrium expectations failed to reveal evidence of a recent reduction in population size. In contrast, coalescent modeling indicated that this population has likely experienced a marked decline within the last few 100 years. These findings generate new insights into the genetic structure of A. palliata and suggest that while the formation of BCI may not have substantially reduced genetic variation in these animals, genetic diversity has been influenced by historical changes in population size.     

Population trends of the mantled howler groups of La Pacifica,Guanacaste, Costa Rica

A complete survey of La Pacifica in Guanacaste Province, Costa Rica was conducted in July 1984 in order to determine whether the howler (Alouatta palliata) population had declined since 1972 as a result of deforestation. During the 6-day survey, 257 howlers were located, representing 16 different social groupings and nine solitary animals. The total number of howlers, the number and location of groups, and the age-sex composition were very similar to a 1972–1976 survey of the same population. Age-sex composition of La Pacifica howler groups was similar to those of another population of mantled howlers in Costa Rica and of populations in Mexico and in Panama, although La Pacifica had a higher mean number of adult females per group. There was no evidence to support the hypothesis that the La Pacifica howler population has declined in recent times.     

Grooming in brown howler monkeys,Alouatta fusca

The grooming behavior of a group of brown howler monkeys was studied for one year in an Atlantic forest reserve of southeastern Brazil. A total of 290 grooming bouts were recorded and analyzed. The two adult females directed most of the grooming (91%), while the adult male was the major recipient (37%). Grooming between females, and between them and their siblings, also occurred quite often. On average, the group spent 2% of its daily time grooming, with a higher frequency around noon. There were significant differences, however, in time spent grooming between seasons; grooming was more abundant during the coldest seasons (autumn–winter) and rarer in hotter ones (spring–summer). A significant negative correlation was found between grooming time and temperature, but contrary to expectations, grooming time failed to correlate with both the group' diet and the demands of food-gathering, as measured by travelling time and day range length. A comparison of grooming behavior with other species of the genus suggests that brown, red (A. seniculus), and black howler monkeys (A. caraya) are more similar to each other than to mantled howlers (A. palliata), a result that probably is linked with the differing social structure and group size of the latter species. © 1995 Wiley-Liss, Inc.     

Seroprevalence of Trypanosoma cruzi and Leishmania mexicana in Free‐Ranging Howler Monkeys in Southeastern Mexico

Natural infection of wild mammals by protozoa parasites is quite common in nature. For Neotropical Primates different infections of parasites that are etiological agent of disease in human have been identified. In particular, infections by Trypanosoma cruzi and Leishmania sp., have been reported for some New World primate species, but there are no reports of infection with these parasites in any primate species in Mexico. A serological study was conducted on two howler monkey species (Alouatta pigra and A. palliata) from the Mexican states of Campeche and Tabasco. A total of 55 serum samples (20 samples from A. pigra, 20 samples from A. palliata, and 15 samples from semifree ranging A. palliata of Los Tuxtlas, Veracruz as negative controls) were analyzed for the detection of immunoglobulin G antibodies against T. cruzi and Leishmania mexicana through enzyme linked immunosorbent assay test, indirect immunofluorescence assay and Western blot. The overall prevalence of antibodies in howler monkeys was 17.5% for T. cruzi and 30% for L. mexicana. Our results also indicate that A. pigra is more susceptible to develop leishmaniasis than A. palliata. Finally, the finding of positive serology in these primates should be given serious consideration for public health, given the potential role of these primate species as wild reservoirs for these diseases and the increasing contact of monkeys with human populations due to habitat loss and fragmentation. Am. J. Primatol. 75:161‐169, 2013. © 2012 Wiley Periodicals, Inc.     

Mandible/basihyal relationships in red howler monkeys (Alouatta seniculus): A craniometrical approach

The morphological relationships between the cranium and basihyal of red howler monkeys (Alouatta seniculus) were analyzed based on measurements of 36 cranial and 3 basihyal dimensions and observations of the female specimen in spirits. In this study, 115 crania from 111 red howler monkeys and 4 mantled howler monkeys (Alouatta palliata) were used. The analyses from the standpoints of the correlation coefficients, principal component analysis, discriminant function analysis, age changes and sex differences were performed and the following results were obtained: (1) The cranial measurements closely related to the basihyal measurements were mandibular length, occipital breadth, facial length, ramus height, cranial base length, bigonial breadth and pr-i length. (2) Age changes for the mandibular measurements in males of red howler monkeys were remarkable, and, in particular, the development of the gonion toward posterior and lateral directions were characteristic. (3) The largest sex differences were found in the mandibular measurements of red howler monkeys among the Anthropoidea of seven genera compared. (4) The existence of a “cline” in the cranial measurements of the red howler monkey was recognized. (5) The inter-species differences in the crania between the red howler monkey and mantled howler monkey are obvious, metrically and non-metrically. Based on the results mentioned above, the morphological relationships between the mandible and basihyal in the red howler monkey are discussed.     

Locomotor and postural behavior in Alouatta palliata and Cebus capucinus

Positional behavior of two platyrrhine monkeys, Alouatta palliata and Cebus capucinus, was observed at La Pacifica and Santa Rosa National Park, Costa Rica. Frequency data for locomotion, postures, support diameters, orientation of supports, and use of canopy were recorded on focal males and females. Alouatta palliata is a frequent user of arboreal quadrupedalism (47%) and climbing (37%), with bridging (10%) representing the next most frequent type of locomotion. Intraspecific comparisons show the smaller-sized females of Alouatta to prefer very small diameter supports, the lower canopy, and to climb more frequently than the larger males—a pattern opposite to that which has been documented to occur with increasing body size across species. A more limited study on Cebus capucinus shows this species to be highly quadrupedal (54%) with moderately high locomotor frequencies for climbing (26%) and leaping (15%).     

Longitudinal Assessment of Immature-to-Adult Ratios in Two Groups of Costa Rican Alouatta palliata

We used immature-to-adult female ratios (IFR), which indicate replacement rates, to assess changes in and viabilities of nonhuman primate groups and populations. Heltne et al. (1975) concluded that the howling monkey (Alouatta palliata) population at La Pacifica (Guanacaste, Costa Rica) was declining, as the IFR was <1.5, the ratio thought needed for a sustainable population. Our population surveys of 1984, 1991, and 1998 revealed that the number of monkeys in the population was stable, but the number of groups had increased and mean group size decreased. To examine these group-level changes, we present the IFR and immature-to-adult (IAR) ratios for La Pacifica Groups 2 and 18, which we have studied longitudinally for 18 and 10 years, respectively. Group 2 was larger than Group 18, but both groups showed similar mean IFRs for the study periods. The mean IFR for each group exceeded the population IFR. The annual IFRs varied more in the smaller group than in the larger group, and the IARs for these groups varied more than the IFRs did. All annual IFRs in the groups were below the hypothesized critical value of 1.5. Given these group and population values, we examined this critical IFR value with respect to mantled howler life history characteristics, particularly interbirth intervals and juvenile emigration, both of which preclude ratios 1.5, and compared the La Pacifica mantled howler population ratios with those of other populations. Group size, in conjunction with these ratios, might be more predictive of sustainable groups and populations.     

Anthropogenic edges impact howler monkey (Alouatta palliata) feeding behaviour in a Costa Rican rainforest

Anthropogenic forest fragmentation impacts many aspects of animal behaviour, including feeding ecology. With forests increasingly fragmented in tropical regions due to human development, the proportion of forest edge (≤?100 m from clear-cut regions) is higher relative to forest interior. Forest edges differ in vegetation from interior, making it important to better understand how anthropogenic edges impact the feeding behaviour of primates such as mantled howler monkeys (Alouatta palliata). We predicted that howler monkeys would feed on higher-quality plant resources, from a larger number of tree families, and from larger trees in forest interior compared to anthropogenic forest edge. We surveyed howler monkey feeding behaviour across forest zones in a fragmented rainforest in Costa Rica, La Suerte Biological Research Station. We observed individual monkeys for 30-minute periods, collecting data on their feeding behaviour and tree use at 2-minute intervals. We measured feeding trees and recorded the plant parts and taxonomy of resources consumed. Monkeys consumed more leaves and fewer stems and fed from a smaller number of tree families in the forest interior, while they consumed fewer leaves and more stems and fed from a larger number of tree families in the forest edge. Monkeys also fed from larger, taller trees in the forest interior than the edge. The differences in howler monkey feeding behaviour between forest zones attest to the impact of human disturbance on howler monkey feeding ecology.

     

Parasites of Wild Howlers (Alouatta spp.)

A literature review of howler parasites provides the basis for an overview of the ecological significance of parasite surveys in primates. Within this framework, we have added insights into the interactions between primate hosts and their parasites from a long-term study in Costa Rica. We collected fecal samples from mantled howlers (Alouatta palliata) over a 9-year period (1986–1994 inclusive) and analyzed them for parasite eggs, larvae, cysts, and oocysts. We found many misperceptions inherent in the typical methodology of primate parasite surveys and in the reporting of the findings. Our work in Costa Rica suggests that a snapshot effect occurs with most surveys. A static view does not reflect the dynamic and changing ecological interaction between host and parasite. We describe some problems with parasite data analyses that emphasize the need for long-term longitudinal surveys in wild primate groups.     

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.     

In situ hybridization (FISH) maps chromosomal homologies between Alouatta belzebul (Platyrrhini,Cebidae) and other primates and reveals extensive interchromosomal rearrangements between howler monkey genomes

We hybridized whole human chromosome specific probes to metaphases of the black-and-red howler monkey Alouatta belzebul in order to establish chromosomal homology between humans and black-and-red howlers. The results show that the black-and-red howler monkey has a highly rearranged genome and that the human chromosome homologs are often fragmented and translocated. The number of hybridization signals we obtained per haploid set was 40. Nine human chromosome probes gave multiple signals on different howler chromosomes, showing that their synteny is disturbed in A. Belzebul. Fourteen black-and-red howler autosomes were completely hybridized by one human autosomal paint, six had two signals, three had three signals, and one chromosome had four signals. Howler chromosomes with multiple signals have produced 12 chromosomal syntenies or hybridization associations which differ from those found in humans: 1/2, 2/20, 3/21, 4/15, 4/16, 5/7, 5/11, 8/18, 9/12, 10/16, 14/15, and 15/22. The hybridization pattern was then compared with those found in two red howler taxa and other mammals. The comparison shows that even within the genus Alouatta numerous interchromosomal rearrangements differentiate each taxa: A. belzebul has six unique apomorphic associations, A. seniculus sara and A. seniculus arctoidea share seven derived associations, and additionally A. seniculus sara has four apomorphic associations and A. seniculus arctoideaseven apomorphic associations. A. belzebul appears to have a more conserved karyotype than the red howlers. Both red and black-and-red howlers are characterized by Y-autosome translocations; the peculiar chromosomal sex system found in the red howler taxa could be considered a further transformation of the A. belzebul sex system. The finding that apparently morphologically similar or even identical taxa have such extreme genomic differences has important implications for speciation theory and neotropical primate conservation. Am. J. Primatol. 46:119–133, 1998. © 1998 Wiley-Liss, Inc.     

Color Vision Variation as Evidenced by Hybrid L/M Opsin Genes in Wild Populations of Trichromatic Alouatta New World Monkeys

Platyrrhine (New World) monkeys possess highly polymorphic color vision owing to allelic variation of the single-locus L/M opsin gene on the X chromosome. Most species consist of female trichromats and female and male dichromats. Howlers (genus Alouatta) are an exception; they are considered to be routinely trichromatic with L and M opsin genes juxtaposed on the X chromosome, as seen in catarrhine primates (Old World monkeys, apes, and humans). Yet it is not known whether trichromacy is invariable in howlers. We examined L/M opsin variation in wild howler populations in Costa Rica and Nicaragua (Alouatta palliata) and Belize (A. pigra), using fecal DNA. We surveyed exon 5 sequences (containing the diagnostic 277th and 285th residues for λ_max) for 8 and 18 X chromosomes from Alouatta palliata and A. pigra, respectively. The wavelengths of maximal absorption (λ_max) of the reconstituted L and M opsin photopigments were 564 nm and 532 nm, respectively, in both species. We found one M–L hybrid sequence with a recombinant 277/285 haplotype in Alouatta palliata and two L–M hybrid sequences in A. pigra. The λ_max values of the reconstituted hybrid photopigments were in the range of 546~554 nm, which should result in trichromat phenotypes comparable to those found in other New World monkey species. Our finding of color vision variation due to high frequencies of L/M hybrid opsin genes in howlers challenges the current view that howlers are routine and uniform trichromats. These results deepen our understanding of the evolutionary significance of color vision polymorphisms and routine trichromacy and emphasize the need for further assessment of opsin gene variation as well as behavioral differences among subtypes of trichromacy.     

Howling on the edge: Mantled howler monkey (Alouatta palliata) howling behaviour and anthropogenic edge effects in a fragmented tropical rainforest in Costa Rica

The function of long calling is a subject of interest across animal behaviour study, particularly within primatology. Many primate species have male‐specific long‐distance calls, including platyrrhines like the folivorous howler monkey (Alouatta spp.). Howler monkeys may howl to defend resources such as feeding trees or areas of rich vegetation from other monkey groups. This study tests the ecological resource defence hypothesis for howling behaviour in the mantled howler monkey (Alouatta palliata) and investigates how anthropogenic forest fragmentation may influence howling behaviour. More specifically, this study examines how howling bout rate, duration, precursors and tree species richness, DBH, and canopy cover vary in 100 m anthropogenic edge and interior forest zones at La Suerte Biological Research Station (LSBRS), a fragmented tropical rainforest in Costa Rica. Results show that tree species richness and canopy cover are higher in forest interior at this site, suggesting that monkeys should howl at greater rates in the interior to defend access to these higher‐quality vegetation resources. Overall, our results supported the ecological resource defence hypothesis. The main howl precursor was howling from neighbouring groups. Although howling rate did not differ between forest zones, howling bouts from forest interior were longer, had a greater number of howls per bout and were preceded by different precursors than howls from anthropogenic edge zones, including more howls from neighbouring groups. Our findings provide some of the first evidence for behavioural edge effects in primate vocal communication behaviour.     

Habitat selection and seasonal patterns of activity and foraging of mantled howling monkeys(Alouatta Palliata) in Northeastern Costa Rica

I conducted a 15- month ecological study of habitat preferences and activity and foraging patterns of two troops of mantled howling monkeys, Alouatta palliata,in a lowland rain forest at La Selva Biological Reserve in northeastern Costa Rica. The two troops specialized on different habitats in spite of the fact that both of them had all habitats available and were not constrained by neighboring troops since the population density of howlers is low (7- 15 howlers/km ² ).Troop 1 spent the majority of time in primary forest (80%) followed by secondary forest (10%), while troop 2 spent the majority of time in undisturbed riparian habitat (60%) followed by primary forest (30%). Habitat sampling indicates that neither the total number of stems, species, or families nor the diversity (Shannon index) or evenness is a good indicator for howler habitat selection. Instead the density of trees from the 12 species most commonly consumed by each troop is the most important factor. Activity and foraging patterns were not dependent upon the season as has been described for howling monkeys in forests with a more pronounced dry season at Barro Colorado Island, Panama, and La Pacifica in northwestern Costa Rica. This is likely a result of the more constant food supply at La Selva, combined with less intraspecific competition due to the low howler density. The intraspecific variability of foraging patterns and troop- specific habitat specialization observed in Alouatta palliatashould be considered in the conservation biology of primates. Primate relocation programs should include not only an ecological assessment of the release site but also a comparison of the release site with the habitat that the groups currently occupy.     

Phenotypic polymorphism and allele differentiation of isozymes in fodder beet,multigerm sugar beet and monogerm sugar beet

Summary Thirteen enzymes (MDH, SDH, LAP, PGM, PX, IDH, GPI, 6PGD, APH, GOT, GDH, ME and SOD) of 3 cultivated beet (B. vulgaris L.) gene pools, comprising 12 accessions of fodder beet, 11 of old multigerm sugar beet and 10 of modern monogerm sugar beet, were investigated using horizontal starch gel electrophoresis. Eleven accessions of primitive or wild B. vulgaris were also included for the comparison of isozymes. Variation in isozyme phenotypes was investigated to detect diversity in the three cultivated forms of beet. Phenotypic variation was observed in all except ME and SOD, which were monomorphic. A high degree of phenotypic polymorphism (Pj) was found in GDH, PGM, IDH, APH and MDH. Differences in phenotypic polymorphism in MDH, GPI and PX were recognized between fodder beet and both sugar beet groups. Average polymorphism for 13 enzymes in both sugar beets was significantly higher than that in fodder beet. For 13 enzymes, the existence of high isozyme diversity in both sugar beet gene pools was revealed. Allele frequencies in 13 alleles of five enzyme-coding loci, Lap, Px-1, Aph-1, Got-2 and Gdh-2, were investigated. New alleles, Px-1 ¹ and Got-2 ¹, were found in fodder beet accessions. No significant differences of average allele frequencies of five loci between fodder beet and both sugar beets were recognized. Several unique alleles and different isozyme phenotypes were observed in the accessions of B. vulgaris ssp. macrocarpa and ssp. adanensis. Future utilization of cultivated beet gene pools for sugar beet breeding is discussed from the viewpoint of genetic resources.     

Diet and activity in black howler monkeys (<Emphasis Type="Italic">Alouatta pigra</Emphasis>) in southern Belize: does degree of frugivory influence activity level?

This study reports on the diet and activity budgets of Central American black howling monkeys (Alouatta pigra) at Monkey River, Belize. This is a previously unstudied population, close to the southern boundary of the species range, and it provides comparative data on A. pigra from a new study site. Both diet and activity are within the ranges reported for other A.pigra sites and for mantled howlers (A. palliata). No age-sex differences could be discerned in either diet or activity, though monthly variation was apparent. The monkeys switch from consuming leaves 86% of the time in January to March to consuming 67% fruit in April to July. This difference was statistically significant, and provided the opportunity to compare activity levels of the monkeys over two dietary periods, one characterized primarily by folivory, the other by frugivory. Howlers are often seen as a relatively inactive species, something that is associated with a low quality, folivorous diet. However, A. pigra have been described as being as frugivorous as possible and as folivorous as necessary. Yet, despite the opportunistic consumption of large quantities of high-energy foods, A. pigra has been observed as conforming to the howler lifestyle, resting as much as 80% of the day. The data in this paper support both of these reports. Black howlers at Monkey River Belize are typically inactive, maintaining high levels of inactivity even during months characterized by frugivory, suggesting that diet is more flexible and varied than is behavior and calling into question the assumption that howler inactivity is due to the digestion of large quantities of leaves.     

Genetic variation of cassava (Manihot esculenta Crantz) cultivated by Chibchan Amerindians of Costa Rica

This study focuses on the genetic diversity of the cassava (Manihot esculenta Crantz) grown by the Chibchan Amerindians of Costa Rica. The authors collected cassava in various locations within two Amerindian Reserves: Talamanca, inhabited by Cabecares and Bribris, and Coto Brus, inhabited by Guaymi. Through the use of isozyme electrophoretic techniques we found variation for six out of nine systems analyzed, namely DIA, EST, IDH, MDH, PGI, and SKD. No variation was found in ADH, PGD, and PGM systems. We analyzed the distribution of variation within and between the reserves, and found most of the variation occurred within reserves (Gst = 0.1084). Only low levels of genetic differentiation were found between reserves (Nei’s genetic distance = 0.0088). The high levels of genetic variation within reserves that we found concur with results of previous studies on cassava grown by South American Amerindians and farmers. The role of the breeding system of cassava and the agricultural practices of Amerindians in the maintenance of high levels of genetic diversity are discussed.     

Notes on the geographic distribution of howling monkeys in the marajó archipelago, pará, Brazil

I review the distribution of genus Alouattain the Marajó Archipelago based on geographic variation of pelage color patterns. Specific differences exist among the labeled specimens at Museu Paraense Emílio Goeldi, which are confirmed via new field information from wild populations. The animals from Marajó, Caviana, and Mexiana Islands possess color patterns of Alouatta belzebul,while Alouatta seniculusis confirmed as the species that inhabits Gurupá Island. The high variability of pelage coloration of the animals from Marajó, Caviana, and Mexiana Islands includes all phenotypes formerly designated as different subspecies. The howler populations from these three islands belong to the same subspecies as those populations that inhabit the region of Tucurui dam reservoir (area 4). Finally, it seems that, as also suggested by chromosome studies, A. belzebulprobably comprises different epiphenotypes without taxonomic validity.     

Behavioral ecology ofAlouatta seniculus in Andean cloud forest

The behavior and ecology ofAlouatta palliate àre well studied; we report here on the first long-term study of anotherAlouatta species, the red howler monkey,A. seniculus. AlthoughA. seniculus was studied at a high elevation in the Colombian Andes, it exhibits many behavioral and ecological similarities to lowlandA. palliata. Continuous focal sampling indicates thatA. seniculus spends 78.5% of its time resting, 5.6% moving, and 12.7% feeding. It has a day range of 1.09 km and a home range of 22 ha. Like its more northern relative,A. seniculus spends more than 50% of its feeding time on leaves–especially young leaves–but on a dry-weight basis, fruits comprise the majority of its diet. The small home and day ranges observed as well as the large amounts of time spent resting are all argued to be aspects of a relatively folivorous foraging strategy. Daily food intake is estimated to be 1.23 kg fresh weight (0.266 kg dry weight). Foraging efficiency (yield/time) varies by a factor of almost 6 across major food types, with item size and distribution being the key determinants. Food preferences change markedly over the activity period, with high-energy sources predominating early and high-protein sources late.