Alouatta Research Articles

Socially mediated overlap in vocal interactions between free-ranging black howler monkeys.

"Conversation rules" such as overlap avoidance and coordinated overlap have been reported in nonhuman animals, and seem to be adaptive responses to the requirements of social life. Some species display both patterns in an apparently flexible way, but the social factors mediating their respective usage remain poorly documented. We investigated the potential social factors guiding the usage of these temporal rules during collective howling in six free-ranging groups of black howler monkeys (Alouatta pigra). First, we found that adult males' vocalizations rarely overlap those of other callers while most adult females' calls overlap other members' calls, especially that of other females. Second, whereas some call types (notably affiliative calls) are typically emitted without overlap, roars (agonistic loud calls) overlap more frequently. Third, coordinated overlap is more frequent during intergroup competition. Our findings support the hypothesis that overlap avoidance and coordinated overlap are two different (here sex-related) vocal alliance social behaviors, at least for some nonhuman primates. More comparative investigations are now needed to explore further their evolutionary trajectories in this lineage.

Uniform trichromacy in Alouatta caraya and Alouatta seniculus: behavioural and genetic colour vision evaluation

Primate colour vision depends on a matrix of photoreceptors, a neuronal post receptoral structure and a combination of genes that culminate in different sensitivity through the visual spectrum. Along with a common cone opsin gene for short wavelengths (sws1), Neotropical primates (Platyrrhini) have only one cone opsin gene for medium-long wavelengths (mws/lws) per X chromosome while Paleotropical primates (Catarrhini), including humans, have two active genes. Therefore, while female platyrrhines may be trichromats, males are always dichromats. The genus Alouatta is inferred to be an exception to this rule, as electrophysiological, behavioural and molecular analyses indicated a potential for male trichromacy in this genus. However, it is very important to ascertain by a combination of genetic and behavioural analyses whether this potential translates in terms of colour discrimination capability. We evaluated two howler monkeys (Alouatta spp.), one male A. caraya and one female A. seniculus, using a combination of genetic analysis of the opsin gene sequences and a behavioral colour discrimination test not previously used in this genus. Both individuals completed the behavioural test with performances typical of trichromatic colour vision and the genetic analysis of the sws1, mws, and lws opsin genes revealed three different opsin sequences in both subjects. These results are consistent with uniform trichromacy in both male and female, with presumed spectral sensitivity peaks similar to Catarrhini, at ~ 430 nm, 532 nm, and 563 nm for S-, M- and L-cones, respectively.

Attack of an infant by a female in a troop of howler monkeys (<i>Alouatta pigra</i>)


 
 
 Within the New World primate family of Atelidae, infanticidal attacks are most commonly reported in howler monkeys (Alouatta spp., Crockett, 2003; Knopff et al., 2004; Aguiar et al., 2005; Agoramoorthy and Rudran, 2009; Van Belle et al., 2010; Pavé et al., 2012). The howler monkey species that have been observed to exhibit this behaviour are black and gold howler monkeys (Alouatta caraya, Crockett, 2003; Pavé et al., 2012); Colombian red howler monkeys (A. seniculus, Agoramoorthy and Rudran, 1995; Beltrán and Stevenson, 2012); mantled howler monkeys (A. palliata, Crockett, 2003); brown howler monkeys (Martins et al., 2015); and Yucatán black howler monkeys (A. pigra, Crockett, 2003; Van Belle et al., 2010). In these documented attacks there is a lack of detail regarding the involvement of females, as the male is usually identified as the aggressor. These attacks are likely to occur following the immigration of a new male to a troop (Van Belle et al., 2010; Beltrán and Stevenson, 2012), up to five months after taking over a troop (Agoramoorthy and Rudran, 2009). A majority of infanticidal attacks in howler monkeys involve assumed unrelated assailant and victim, therefore these instances align with the sexual selection hypothesis (Hrdy, 1979).
 
 

A PLATE-ROD CONSTRUCT FOR REPAIR OF A HUMERAL DIAPHYSEAL FRACTURE IN A BLACK HOWLER MONKEY INFANT

An infant black howler monkey (Alouatta caraya), aged approximately three months, presented with atransverse fracture of the distal third of the right humeral shaft underwent surgical treatment using aplate-rod construct. A 1.00-mm diameter intramedullary pin was used in a retrograde fashion to reduceboth the fracture and plate stress. The plate-rod construct was a seven-hole 1.5-mm veterinary cuttableplate, which was installed following the principles of biological osteosynthesis. The animal presentedno pain in the postoperative exams and used the limb normally. Bone consolidation was observed foreighth weeks after surgery, showing that the treatment was effective.

Dipetalonema graciliformis (Freitas, 1964) from the red-handed tamarins (Saguinus midas, Linnaeus, 1758) in French Guiana.

Six Dipetalonema species have been reported from Neotropical monkeys, Dipetalonema gracile, Dipetalonema graciliformis and Dipetalonema caudispina being the dominant species found in French Guiana primates. Adult filarioids isolated from the abdominal cavity of tamarins (Saguinus midas) in French Guiana were morphologically and molecularly identified as D. graciliformis. Phylogenetic analysis based on DNA and amino acid sequences of the cox1 gene as well as the concatenated sequences of the cox1 and the 18S genes indicated that D. graciliformis belongs to the clade 4 (ONC4) of Onchocercidae. Blast analysis of the 18S rDNA revealed that D. graciliformis in the studied tamarins is conspecific with the filarioid circulating in howler monkeys (Alouatta macconnelli) in French Guiana, previously referred to as unidentified Onchocercidae species.

Wischnewski Spots and Black Oesophagus in Suspected Fatal Hypothermia in a Brown Howler Monkey (Alouatta guariba clamitans) and a Rabbit (Oryctolagus cuniculus)

Fatal hypothermia represents a diagnostic challenge in veterinary pathology. Wischnewski spots (WS) and black oesophagus (BO) have been described in human cases of fatal hypothermia but rarely in animals. We now describe WS and BO in suspected fatal hypothermia in a free-ranging brown howler monkey (Alouatta guariba clamitans) and a pet rabbit (Oryctolagus cuniculus). Both animals had dark spots resembling WS on the gastric mucosa and the monkey also had BO with haematin deposition. In both cases, stress factors and relatively cold environmental conditions were present prior to death.

The evolution and changing ecology of the African hominid oral microbiome

The oral microbiome plays key roles in human biology, health, and disease, but little is known about the global diversity, variation, or evolution of this microbial community. To better understand the evolution and changing ecology of the human oral microbiome, we analyzed 124 dental biofilm metagenomes from humans, including Neanderthals and Late Pleistocene to present-day modern humans, chimpanzees, and gorillas, as well as New World howler monkeys for comparison. We find that a core microbiome of primarily biofilm structural taxa has been maintained throughout African hominid evolution, and these microbial groups are also shared with howler monkeys, suggesting that they have been important oral members since before the catarrhine-platyrrhine split ca. 40 Mya. However, community structure and individual microbial phylogenies do not closely reflect host relationships, and the dental biofilms of Homo and chimpanzees are distinguished by major taxonomic and functional differences. Reconstructing oral metagenomes from up to 100 thousand years ago, we show that the microbial profiles of both Neanderthals and modern humans are highly similar, sharing functional adaptations in nutrient metabolism. These include an apparent Homo-specific acquisition of salivary amylase-binding capability by oral streptococci, suggesting microbial coadaptation with host diet. We additionally find evidence of shared genetic diversity in the oral bacteria of Neanderthal and Upper Paleolithic modern humans that is not observed in later modern human populations. Differences in the oral microbiomes of African hominids provide insights into human evolution, the ancestral state of the human microbiome, and a temporal framework for understanding microbial health and disease.

Monkeying around Anthropocene: Patterns of human-nonhuman primates’ interactions in Brazil

In Anthropocene, approximately 70% of all terrestrial ecosystems are highly modified by human activities and more than a half of all primate’s species in the world are endangered. Here we present results of a systematic review on published articles with an Ethnoprimatology approach, aiming to assess the nationwide pattern and quality of proximity/interaction between human-nonhuman primates in Brazil, a country vulnerable to high deforestation rates while having the highest primate biodiversity in the world. The first article was published 29 years ago and add up to only 36 published articles until present time. Most studies were conducted in Atlantic forest, but higher number and diversity of interactions was described for Amazon. Sapajus, being a generalist and semi-terrestrial primate, was the most cited genus and had the greatest diversity of interactions, including garbage foraging and crop-raiding. Alouatta, the second most cite one, had more symbolic/mystic relationships. Some specialized or forest-specific primates are scarcely mentioned. Studies carried out in both rural and urban environment are almost equal in number but showed differences in types of interactions they describe: garbage foraging, crop-raiding by primates and food offering by humans happening in more urbanized areas and symbolic/mystic relationships and beliefs around nonhuman primates described in rural/indigenous settlements. We urge future studies to describe interactions and proximity carefully specifying the context where they occur. It is relevant to maintain the growing curve of Ethnoprimatological studies in Brazil as a way to aggregate information about different populations of species and help to base conservation strategies of co-existence.

Wild robust capuchin monkey interactions with sympatric primates.

Examining interactions among sympatric primate species can provide interesting information about competition, cooperation, and avoidance between those species. Those interactions can be neutral, positive, or negative for the species involved. Capuchin monkeys are medium-sized primates that can encounter both larger and smaller primates in their varied habitats. Gracile capuchins (Cebus) are reported to present different types of interactions with other primates. Interactions with howler monkeys frequently include physical aggression, while interactions with spider monkeys are mostly threats and chases. Moreover, interaction types are not consistent across populations. Among robust capuchins (Sapajus spp.), however, no reports have been published. Here we describe and classify encounters of Sapajus libidinosus and S. nigritus with Alouatta caraya, A. guariba, Brachyteles arachnoides, and Callithrix jacchus in three sites in the environments of Cerrado, Caatinga (savannah-like), and Atlantic forest, and compare the interaction patterns among sites and different group sizes. The latter is a factor that can influence the outcome, and we expected capuchins in larger groups to be more aggressive toward other primates. Our results of 8421h of total contact with the capuchin groups show that, indeed, capuchins in sites with larger groups presented aggressive interactions with higher frequency. However, the other species' body size also seems important as smaller primates apparently avoided capuchins, and interactions with the larger muriquis were mostly neutral for the capuchin. Capuchins showed neutral or aggressive behaviors toward howler monkeys, with differences between the rainforest and savannah groups. We found that robust capuchins can present aggressive interactions even to primates larger than themselves and that aggressive behavior was the most common response in populations living in larger groups and drier environments.

Conservation implications of living in forest remnants: Inbreeding and genetic structure of the northernmost mantled howler monkeys

AbstractThe current unprecedented rates of environmental perturbation, particularly in rain forest ecosystems, are jeopardizing the persistence of a variety of tropical species. The development of adequate conservation programs requires incorporating the evolutionary history and population genetic information of species, especially in those threatened by habitat loss and fragmentation. Mexican mantled howler monkeys (Alouatta palliata mexicana) represent the northernmost distribution of primates in America, a Critically Endangered species mainly inhabiting forest remnants. We assessed historical and contemporary patterns of genetic variation in A. p. mexicana populations from five regions across its geographic distribution in Mexico. We employed non‐invasive sampling techniques and evaluated microsatellite loci and mitochondrial cytochrome b sequences from 127 individuals from 15 wild and two semi‐captive populations. Our data demonstrate negative genetic effects on A. p. mexicana as a result of isolation, fragmentation, and small effective population size. Results revealed two mitochondrial lineages and three genetically differentiated nuclear clusters, along with reduced nuclear genetic diversity, limited gene flow, and significant inbreeding, associated with concurrent processes of historical dispersion and contemporary landscape changes. Accordingly, we argue that A. palliata mexicana in Mexico is an independently evolving unit that meets the criteria for being assigned as an Evolutionarily Significant Unit, crucial for the preservation of the howler monkeys’ phylogenetic and functional diversity. The three genetic clusters identified are essential for the maintenance of the adaptive diversity and long‐term survival of this howler subspecies. Our genetic approach and conservation recommendations may be useful for other endangered primates inhabiting fragmented populations.Abstract in Spanish is available with online material.

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 (≤ 100m 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.

Pre‐Hispanic howler monkeys from two sites of northern Venezuela and the Orinocan connection: An archaeoprimatological study

AbstractSkeletal fragments of ursine howler monkeys (Alouatta, A. cf. arctoidea) recovered from two archaeological sites in northern Venezuela are discussed in this article. Osteological remains, material culture evidence, and historical records are put together using an archaeoprimatological approach in order to investigate the relationships between the pre‐Hispanic human societies in this region of South America and this primate taxon. The remains of howler monkeys studied suggest that Indigenous peoples of Arawakan linguistic affiliation of Orinocan origin interacted with nonhuman primates in northern Venezuela before AD 800. This interaction encompasses different meanings: the howler as a possible pet or hunting prey and thus a source of food, and the howler as a reference with symbolic value.

Facial malformations, including cleft lip and palate, in wild primates in Paraguay

Nine individual Alouatta caraya and Sapajus cay displaying facial malformations were observed across three sites in Paraguay. Six had cleft lip (with or without cleft palate), and three had malformations of the lower lip. This is the first record of cleft lip and/or palate in the genus Alouatta.

Vocal and movement responses of mantled howler monkeys (Alouatta palliata) to natural loud calls from neighbors.

Loud calls (i.e., long-range acoustic signals) regulate resource competition among neighboring groups of conspecifics in several nonhuman primate species. Ultimate explanations for primate loud calls include mate, offspring, and food defense. Additionally, loud calls may provide valuable information pertaining to the identity and health status of callers, their competitive abilities, and their spatial location. The loud calls of howler monkeys (Alouatta) have been thoroughly studied and seem to play an important function in the defense of valuable resources in a variety of socioecological contexts. Here, we examined whether the behavioral responses of mantled howler monkeys (Alouatta palliata) to natural loud calls from neighbors are linked to three factors: food availability, familiarity, and distance between groups. We studied three groups of mantled howler monkeys at La Flor de Catemaco (Los Tuxtlas, Mexico) for 15 months (1817 observation hours), during which we recorded 236 neighbor loud calls. Food availability per sedid not influence the behavior of groups receiving loud calls, although males produced longer vocal responses toward unfamiliar neighbors when food availability decreased. Groups vocalized quicker and both vocalized and moved for longer after loud calls from unfamiliar neighbors. Additionally, groups vocalized and moved for longer at shorter distances from unfamiliar neighbors compared with familiar neighbors. Finally, groups usually moved away from calling neighbors that were closer. These results indicate that the behavioral responses of mantled howler monkeys to loud calls from neighbor groups are associated with the integration of information pertaining to caller identity as well as to their ecological and spatial context.

Effects of scent enrichment on behavioral and physiological indicators of stress in zoo primates.

Captive breeding is vital for primate conservation, with modern zoos serving a crucial role in breeding populations of threatened species and educating the general public. However, captive populations can experience welfare issues that may also undermine their reproductive success. To enhance the wellbeing of endangered zoo primates, we conducted a study to assess the effects of a new scent enrichment program on captive red-ruffed lemurs (Varecia rubra), black howler monkeys (Alouatta caraya), siamangs (Symphalangus syndactylus), lar gibbons (Hylobates lar) and orangutans (Pongo pygmaeus pygmaeus). We combined behavioral observations and fecal endocrinology analyses to evaluate the effects of a series of essential oils (benzoin, lavender, lemongrass) on five captive troops (N = 19) housed at Dudley Zoo & Castle and Twycross Zoo (UK). We recorded observations of natural species-specific and abnormal stress-related behaviors for 480 h using instantaneous scan sampling. We collected 189 fecal samples and measured the fecal cortisol concentrations using radioimmunoassay. We found a significant effect of the scent enrichment on behaviors, with red-ruffed lemurs and black howler monkeys reducing their social interactions, as well as red-ruffed lemurs and lar gibbons decreasing their stress-related behaviors after they were exposed to the series of essential oils. We also found that red-ruffed lemurs displayed a significant increase in fecal glucocorticoids following exposure to essential oils. Our contradictory findings suggest that the effects of this series of essential oils may change depending on the species-specific social lives and olfactory repertoires of primates. In conclusion, we cannot recommend using these essential oils widely with zoo primates without additional evaluation.

Beyond patch size: The impact of regional context and habitat quality on three endangered primates

Deforestation has carved tropical forest landscapes into millions of different-sized patches worldwide. Research has focused on the effect of patch size on biodiversity, while neglecting patch quality effects and leaving geographic and interspecific variance to patch attributes largely unexamined. Here, we assess how patch size and quality affect the encounter rate (ER) and immature-to-female ratio (IFR) of three endangered primates – Mexican mantled howler monkey (Alouatta palliata mexicana), black howler monkey (Alouatta pigra), and spider monkey (Ateles geoffroyi) – in three rainforest regions with different forest cover. ER of spider monkeys in the best preserved region (50% forest cover) was positively related to both patch size and quality (i.e., species richness of top food species). ER of mantled howlers in the 17% forest cover region was also positively related to patch size. Yet, both ER and IFR of black howlers in the 50% forest cover region and mantled howlers in the 5% forest cover region were mainly related to patch quality. Our results demonstrate that conservation actions in human-modified landscapes must go beyond considering the effect of patch size, as animal populations can be better predicted by patch quality in some regions.

Regional context mediates the response of Mexican primates to landscape structure in fragmented rainforests

Land use change is a major threat to species' persistence. Yet, landscape attributes that shape populations remain poorly understood. Landscape-scale forest cover and matrix quality can favor population persistence, while forest fragmentation per se usually has weak effects on species. The impact of these spatial changes can, however, be influenced by the regional context. To test these hypotheses, we assessed the abundance and immature-to-female ratio (reproductive success) of two endangered howler monkeys species and their relationships with forest cover, matrix quality and forest fragmentation (forest patch density) in four Mexican regions with different deforestation levels. Responses to landscape structure differed among regions. Forest loss was negatively related to primate abundance in two regions. Yet, in the most deforested region, forest loss was positively related to the immature-to-female ratio. Matrix quality was negatively related to monkey abundance and positively related to immature-to-female ratio in regions dominated by arboreal matrices. Fragmentation was negatively related to abundance but positively to immature-to-female ratio in the best preserved region, and negatively related to immature-to-female ratio in a region dominated by treeless matrices. Thus, given that the regional context influences the effects that landscape attributes have on primates, different conservation strategies could help maintain the populations of these arboreal mammals in different regions. Preventing forest loss and restoring forest cover are paramount in highly deforested regions. Increasing matrix quality is highly valuable, especially in regions dominated by treeless matrices. Finally, increasing the number of patches through restoration can have better conservation outcomes in more forested regions.

Use of genetic tools to assess predation on reintroduced howler monkeys (Alouatta caraya) in Northeastern Argentina.

Despite strong support from the media, the reintroduction of animals into natural environments does not always achieve its goal. Alouatta caraya is the primate species facing the greatest hunting pressure due to the illegal pet trade in Argentina. Confiscations of this species are common, as is the voluntary surrender of animals by owners no longer able or willing to care for them. These animals ultimately arrive at rehabilitation centers and, in many cases, are released into natural environments that may differ from the original sites where they were captured. Until recently, the lack of genetic analysis of the individuals involved led to biased relocation decisions. We followed the reintroduction of 12 A. caraya individuals in a protected area (Isla Palacio, Misiones, Argentina). The presence of potential predators such as pumas (Puma concolor) and jaguars (Panthera onca) in this area was confirmed by camera traps, footprints and feces. After the disappearance of four A. caraya at the reintroduction site, we investigated the applicability of genetic assignment tests based on genotypic data to accurately identify predated individuals. Genetic analyses allowed us to determine the predator species (P. onca) and to identify the predated individuals as two of the reintroduced animals. This procedure is promising for identifying the remains of predated individuals, and can contribute to the design of reintroduction policies based on scientific evidence.

Flower consumption, ambient temperature and rainfall modulate drinking behavior in a folivorous-frugivorous arboreal mammal.

Water is vital for the survival of any species because of its key role in most physiological processes. However, little is known about the non-food-related water sources exploited by arboreal mammals, the seasonality of their drinking behavior and its potential drivers, including diet composition, temperature, and rainfall. We investigated this subject in 14 wild groups of brown howler monkeys (Alouatta guariba clamitans) inhabiting small, medium, and large Atlantic Forest fragments in southern Brazil. We found a wide variation in the mean rate of drinking among groups (range = 0-16 records/day). Streams (44% of 1,258 records) and treeholes (26%) were the major types of water sources, followed by bromeliads in the canopy (16%), pools (11%), and rivers (3%). The type of source influenced whether howlers used a hand to access the water or not. Drinking tended to be evenly distributed throughout the year, except for a slightly lower number of records in the spring than in the other seasons, but it was unevenly distributed during the day. It increased in the afternoon in all groups, particularly during temperature peaks around 15:00 and 17:00. We found via generalized linear mixed modelling that the daily frequency of drinking was mainly influenced negatively by flower consumption and positively by weekly rainfall and ambient temperature, whereas fragment size and the consumption of fruit and leaves played negligible roles. Overall, we confirm the importance of preformed water in flowers to satisfy the howler's water needs, whereas the influence of the climatic variables is compatible with the 'thermoregulation/dehydration-avoiding hypothesis'. In sum, we found that irrespective of habitat characteristics, brown howlers seem to seek a positive water balance by complementing the water present in the diet with drinking water, even when it is associated with a high predation risk in terrestrial sources.

Effects of two dietary fiber levels on nutrient digestibility and intestinal fermentation products in captive brown howler monkeys (Alouatta guariba).

Herbivorous primates present a selective consumption profile and morphological adaptations to use the fibrous fraction of their diets. Brown howler monkeys (Alouatta guariba) are generalist herbivores; however, when kept under human care, they usually receive diets rich in fruits and with insufficient amounts of fiber. Thus, the objective of this study was to evaluate the effects of two levels of neutral detergent fiber (NDF) in howlers on apparent total tract digestibility coefficients (ATTDC), fecal consistency, and intestinal fermentation products. A group of 26 adult howler monkeys, 13 males and 13 females, were fed two diets formulated to have 33% or 40% NDF for 11 days, according to a randomized block design (N = 26). The block factor was the enclosures with one, two, or three individuals (each enclosure corresponded to an experimental unit), totaling in eight replicates per treatment. There were no differences in dry matter and nutrients intake between treatments (p > 0.05). The diet with 33% NDF resulted in higher (p < 0.05) ATTDC of crude proteinand crude energy. However, lower fecal concentrations of short-chain fatty acids (SCFA) and dry matter were observed in the treatment with 33% NDF in contrast to the 40% NDF group (p < 0.05). We recommend the inclusion of higher fiber levels (40% NDF) in the diet of howler monkeys since there is evidence of greater production of SCFA and improvement in fecal consistency.