Alouatta Research Articles

Passive acoustic monitoring of the diel and annual vocal behavior of the Black and Gold Howler Monkey.

Passive acoustic monitoring, when coupled with automated signal recognition software, allows researchers to perform simultaneous monitoring at large spatial and temporal scales. This technique has been widely used to monitor cetaceans, bats, birds, and anurans but rarely applied to monitor primates. Here, we evaluated the effectiveness of passive acoustic monitoring and automated signal recognition software for detecting the presence and monitoring the roaring behavior of the Black and Gold Howler Monkey (Alouatta caraya) over a complete annual cycle at one site in the Brazilian Pantanal. The diel pattern of roaring activity was unimodal, with high vocal activity around dawn. The howler monkey showed a clear seasonal pattern of roaring activity, with most of the roars detected during the wet season (74.9%, peak activity during November and December). The maximum vocal activity occurred during the period of maximum flowering and fruit production in the study area, suggesting a potential role of roaring in defending major feeding sites, which is in agreement with the findings of previous studies on the species. However, we cannot rule out the possibility that roaring may serve different purposes. Vocal activity was negatively associated with relative air humidity, which might be related to lower vocal activity on wetter and rainy days, while vocal activity was not related to minimum air temperature. Automated signal recognition software allowed us to detect the species in 89% of the recordings in which it was vocally active, but with a reduced time cost, since the time investment for data analyses was 2% of recording time. The good performance of the recognizer might be related to the long and loud roars of the howler monkey. Further research should be performed to evaluate the effectiveness of automated signal recognition for detecting the calls of different species of primates and under different environmental conditions.

Maternal care according to offspring sex and maternal physical condition in mantled howler monkeys (Alouatta palliata).

The Trivers-Willard hypothesis (TWH) posits that maternal care will be biased in favor of the sex that provides the greatest fitness returns per unit of investment, depending on maternal physical condition. Our aim was to examine the TWH in mantled howler monkeys living at Los Tuxtlas (Veracruz, Mexico). The biological attributes of mantled howler monkeys (Alouatta palliata) meet the assumptions of TWH better than those of other explanations, so we expected that females in better physical condition should bias maternal care toward sons, whereas mothers in worse physical condition should bias care toward daughters. Between December 2017 and March 2019, we studied mother-infant interactions in 20 dyads with focal-animal sampling and continuous recording (N = 204h). We performed genetic analysis to determine offspring sex (N = 7 daughters and 13 sons) and measured C-peptide in urine samples of mothers to assess their physical condition (N = 46 samples). Mothers in better physical condition spent less time in contact with their sons but more time in contact with their daughters. For proximity behavior, mothers in better physical condition spent more time near their sons and less time near their daughters. These results suggest a bias in maternal care towards daughters, contrary to our predictions. In light of current models of maternal investment, our results support that mothers obtain higher fitness returns through daughters.

Disentangling the importance of social and ecological information in goal-directed movements in a wild primate

Memories linked to specific locations provide information for animals to plan future actions and anticipate the occurrence of events. Here, we examined goal-directed travel towards locations where biologically meaningful events had previously taken place to elucidate the relative importance of past social and ecological information for route planning. We inferred goal-directed travelling by detecting long sections of straight-line travel, followed by significant directional changes along travel trajectories of five neighbouring groups of black howler monkeys, Alouatta pigra, at Palenque National Park, Mexico. Post hoc, we determined at the approached locations: (1) the behaviour of the group; (2) the occurrence of previous intergroup interactions; and (3) the ecological properties of the feeding tree (i.e. importance in diet, level of phenological synchrony). The likelihood of goal-directed travel towards a location to engage in loud calling increased after having experienced an encounter with a neighbouring group at that same location in the past. Additionally, the likelihood of goal-directed travel towards a location to forage on fruits increased when the approached tree was considered important in the diet with highly synchronous phenological cycles. Our results indicate that route planning in wild animals involves an integration of both social and ecological variables.

Risk awareness of black-and-gold howler monkeys living in an urban environment in south-west Paraguay

Abstract As urbanisation increases, wild primates are exposed to urban environments which come with a distinct and often novel set of risks. Urban habitats can form a matrix of forest fragments and anthropogenic structures, including buildings, electric cables and roads, which can limit movement and force species to live in hazardous areas. We studied five groups of urban black and gold howler monkey (Alouatta caraya) in Pilar, Paraguay, to investigate whether the monkeys are aware of anthropogenic risks based on their patterns of self-scratching behaviour, an indicator of stress, and how they used the space available to them. Using a Risk Index created for the study, we ranked the level of risk attributed to different zones of their home range, awarding each zone with a hazard score. Using Quantum GIS and kernel density estimation, we determined the relationship between habitat use and hazard score. Using a Spearman’s rank correlation, we found nonsignificant relationships between the hazard score and self-scratching behaviour for four groups, suggesting a lack of awareness. However, there was a significant negative relationship between the hazard score and home range use for four groups, indicating that they spent more time in areas with lower levels of anthropogenic risk.

Monkeys on a free-floating island in a Colombian river: further support for over-water colonization

Further to the debate associated with the viability of land-bound mammals being able to colonize remote frontiers by way of long-distance over-water dispersal, observations are documented of monkeys (red howlers, Alouatta seniculus) occupying free-standing trees within a large floating island on the Magdalena River in north-west Colombia. Also, we contribute to the discussion related to the 15.0–12.5 Ma (Middle Miocene) arrival of the howler monkeys in Central America, which is well before the Panama Isthmus had fully emerged 3.0–2.8 Ma (Late Pliocene). We speculate it was by way of a raft similar to the ones reported here, possibly from a river entering the sea from northern Colombia.

Female reproductive energetics in mantled howler monkeys (Alouatta palliata): A follow-up study.

Reproduction entails several challenges to primate females, among which energetic costs are remarkable at certain stages of the reproductive cycle. Still, females may use behavioral and physiological strategies to cope with those challenges. We had previously reported covariation between female energetic condition through the reproductive cycle and time-budget adjustments in mantled howler monkeys (Alouatta palliata). Accordingly, we suggested that behavioral flexibility allowed coping with the energetic challenges of reproduction. Subsequent evidence from the same population, however, suggested otherwise, so we performed a follow-up study on the variation in female reproductive energetics based on a larger sample of females. We studied 48 free-ranging adult females at Los Tuxtlas (Mexico). We assessed energy balance via urinary C-peptide concentrations (2717 urine samples), behavioral energy intake and expenditure (5728 sampling hours), and physiological energy expenditure via fecal triiodothyronine metabolites (fTH3; 3138 fecal samples). We found that energy balance varied among reproductive states: (a) cycling was a period of low C-peptide concentrations; (b) the highest C-peptide concentrations occurred during gestation; and (c) the beginning of lactation marked a notable decrease in C-peptide concentrations, which then improved at mid-lactation to again decline at lactation offset. These peaks and valleys in energy balance did not seem to be associated with variation in energy acquisition but were rather mirrored by activity levels and fTH3 during lactation. Energy balance was not preserved through the reproductive cycle, supporting previous contentions that the reproductive performance of female mantled howler monkeys may be energetically constrained. The contrast between these and results that we have previously reported, highlights the importance of conducting follow-up studies to continually improve our understanding of the reproductive energetics of primate females.

Coding-Complete Genome Sequence of a Yellow Fever Virus Isolated from a Baby Howler Monkey (Alouatta caraya) from São Paulo State, Brazil, in 2016.

We report a coding-complete sequence of a yellow fever virus, strain JabSPM02, containing the 3' untranslated region and all coding regions. The virus was recovered from an infected howler monkey from a rural area in São Paulo State, Brazil. Our findings show that it belongs to the South America 1E genotype.

Organization Theory and the Resource-Based View of the Firm: The Great Divide

The resource-based view of the firm has become dominant within the field of strategic management, yet it has had surprisingly little influence within organization theory. In this article, we document the divide between strategy and organization theory and propose an interpretation. Choices of theories are largely driven by a researcher’s dependent variables, and the questions “Why do firms do what they do?” and “Why do some firms perform better than others?” can have distinct answers. Thus, strategic management scholars and organization theorists are like howler monkeys and spider monkeys, coexisting peacefully in the same ecosystem by dining on different dependent variables. We further speculate on the looming existential crisis for both fields as traditional firms are increasingly unsustainable due to the transformation wrought by the digital revolution in product markets and the markets for capital, labor, and supplies.

Molecular detection of Apicomplexa protozoa in tissues from Alouatta guariba clamitans

ABSTRACT: The brown howler monkey (Alouatta guariba clamitans) is a primate species widely distributed in South America. Infections by protozoa are common in primates. However, studies on protozoa in primates in Brazil are scarce, so the goal of this study was to investigate DNA from the apicomplexan protozoa Neospora caninum, Sarcocystis spp. and Toxoplasma gondii in tissues of A. guariba clamitans. DNA extraction was performed on tissue samples from the heart, brain, liver, spleen, lung and intestine of six A. guariba clamitans from Santa Maria, Central Region of Rio Grande do Sul, Brazil. Conventional PCR was performed using 18S rRNA gene general primers for Apicomplexa and also specific primers to amplify Neosporaspp. and Toxoplasma gondii DNA. All animals were positive in the 18S PCR and the genetic sequencing confirmed the presence of Sarcocystis spp. DNA in the tissues of four animals belonging to at least two species (S. neurona and S. gigantea) and T. gondii DNA in the other two animals. One positive sample for T. gondii was genotypically characterized as atypical by the restriction fragment length polymorphism technique. N. caninum DNA was not detected in the tested samples. The presence of Apicomplexa protozoan DNA in the tissues of the six animals tested in this study highlights the importance of howler monkeys as maintainers of these pathogens in nature.

Effects of anthropogenic habitat disturbance and Giardia duodenalis infection on a sentinel species' gut bacteria.

Habitat disturbance, a common consequence of anthropogenic land use practices, creates human–animal interfaces where humans, wildlife, and domestic species can interact. These altered habitats can influence host–microbe dynamics, leading to potential downstream effects on host physiology and health. Here, we explored the effect of ecological overlap with humans and domestic species and infection with the protozoan parasite Giardia duodenalis on the bacteria of black and gold howler monkeys (Alouatta caraya), a key sentinel species, in northeastern Argentina. Fecal samples were screened for Giardia duodenalis infection using a nested PCR reaction, and the gut bacterial community was characterized using 16S rRNA gene amplicon sequencing. Habitat type was correlated with variation in A. caraya gut bacterial community composition but did not affect gut bacterial diversity. Giardia presence did not have a universal effect on A. caraya gut bacteria across habitats, perhaps due to the high infection prevalence across all habitats. However, some bacterial taxa were found to vary with Giardia infection. While A. caraya's behavioral plasticity and dietary flexibility allow them to exploit a range of habitat conditions, habitats are generally becoming more anthropogenically disturbed and, thus, less hospitable. Alterations in gut bacterial community dynamics are one possible indicator of negative health outcomes for A. caraya in these environments, since changes in host–microbe relationships due to stressors from habitat disturbance may lead to negative repercussions for host health. These dynamics are likely relevant for understanding organism responses to environmental change in other mammals.

Mantled Howler Monkeys (Alouatta palliata) in a Costa Rican Forest Fragment Do Not Modify Activity Budgets or Spatial Cohesion in Response to Anthropogenic Edges

Forest fragmentation increases forest edge relative to forest interior, with lower vegetation quality common for primates in edge zones. Because most primates live in human-modified tropical forests within 1 km of their edges, it is critical to understand how primates cope with edge effects. Few studies have investigated how primates inhabiting a fragment alter their behaviour across forest edge and interior zones. Here we investigate how anthropogenic edges affect the activity and spatial cohesion of mantled howler monkeys (Alouatta palliata) at the La Suerte Biological Research Station (LSBRS), a Costa Rican forest fragment. We predicted the monkeys would spend greater proportions of their activity budget feeding and resting and a lower proportion travelling in edge compared to forest interior to compensate for lower resource availability in the edge. We also predicted that spatial cohesion would be lower in the edge to mitigate feeding competition. We collected data on activity and spatial cohesion (nearest neighbour distance; number of individuals within 5 m) in forest edge and interior zones via instantaneous sampling of focal animals. Contrary to predictions, the monkeys spent equal proportions of time feeding, resting and travelling in forest edge and interior. Similarly, there were no biologically meaningful differences in the number of individuals or the distance between nearest neighbours in the edge (1.0 individuals; 1.56 m) versus the interior (0.8 individuals; 1.73 m). Our results indicate that A. palliata at LSBRS do not adjust their activity or spatial cohesion patterns in response to anthropogenic edge effects, suggesting that the monkeys here exhibit less behavioural flexibility than A. palliata at some other sites. To develop effective primate conservation plans, it is therefore crucial to study primate species’ responses to fragmentation across their geographic range.

Safety and immunogenicity of 17DD attenuated yellow fever vaccine in howler monkeys (Alouatta spp.).

Alouatta spp. are highly susceptible to yellow fever (YF) infection and develop an often fatal disease. The threat posed by an outbreak started in 2016 leads us to investigate vaccination as a potential tool in preventing YF in non-human primates (NHP). Susceptible howler monkeys were immunized with three different concentrations of the human Brazilian commercial YF17DD vaccine. Post-vaccination viremia/RNAemia, immunogenicity, and safety were characterized. The vaccine did not produce YF clinical manifestations in any of the NHPs. After immunization, all animals seroconverted demonstrating the ability of the YF vaccine to induce humoral response in Alouatta species. The present work has demonstrated the safe and immunogenic profile of the existing YF 17DD vaccine in howler monkeys. This knowledge may support further studies with other susceptible monkey species and provide a possible solution for controlling epizootics and preventing the devastation of endangered species.

Temporal patterns of visitation of birds and mammals at mineral licks in the Peruvian Amazon.

Mineral licks are key ecological resources for many species of birds and mammals in Amazonia, providing essential dietary nutrients and clays, yet little is known about which species visit and their behaviors at the mineral licks. Studying visitation and behavior at mineral licks can provide insight into the lives of otherwise secretive and elusive species. We assessed which species visited mineral licks, when they visited, and whether visits and the probability of recording groups at mineral licks were seasonal or related to the lunar cycle. We camera trapped at 52 mineral licks in the northeastern Peruvian Amazon and detected 20 mammal and 13 bird species over 6,255 camera nights. Generalized linear models assessed visitation patterns and records of groups in association with seasonality and the lunar cycle. We report nocturnal curassows (Nothocrax urumutum) visiting mineral licks for the first time. We found seasonal trends in visitation for the black agouti (Dasyprocta fuliginosa), red howler monkey (Alouatta seniculus), blue‐throated piping guan (Pipile cumanensis), red brocket deer (Mazama americana), collared peccary (Pecari tajacu), and tapir (Tapirus terrestris). Lunar trends in visitation occurred for the paca (Cuniculus paca), Brazilian porcupine (Coendou prehensilis), and red brocket deer. The probability of recording groups (>1 individual) at mineral licks was seasonal and related to lunar brightness for tapir. Overall, our results provide important context for how elusive species of birds and mammals interact with these key ecological resources on a landscape scale. The ecological importance of mineral licks for these species can provide context to seasonal changes in species occupancy and movement.

The occurrence of the red-handed howler monkey (Alouatta belzebul) in amazonian savannas is related to forest patch area and density of flooded area palms.

All Neotropical primates are arboreal and thus depend on forests for their survival. Arboreality puts many Neotropical primates at risk of extinction due to the high rates of deforestation in the tropics. We assessed the influence of vegetation structure and forest patch attributes on the occurrence of the threatened red-handed howler monkey (Alouatta belzebul) in an Amazonian savanna. Using a sample of 38 forest patches in a region of approximately 2000 km2 in the state of Amapá, northern Brazil, we used logistic regression to find the best predictors of the occurrence of A. belzebul. We assessed patch area, patch isolation, the proportion of seasonally flooded forest in the patch, the density of flooded area palms, forest height, canopy cover, and diameter at breast height of trees. Patch area and palm density were the best predictors of the occurrence of A. belzebul in forest patches, both having a positive effect on the probability of occurrence. Our results indicate that areas of flooded forest in forest patches may be keystone habitats for A. belzebul living in Amazonian savannas. The observed effect of palm density on A. belzebul suggests that this variable is useful for planning conservation actions, including the selection of areas for protection and management strategies for areas inhabited by this primate.

Primate life history, social dynamics, ecology, and conservation: Contributions from long‐term research in Área de Conservación Guanacaste, Costa Rica

AbstractResearch on non‐human primates in the endangered tropical dry forest of Sector Santa Rosa (SSR), Área de Conservación Guanacaste (ACG), was launched in 1983 and is now one of the longest running studies of primates globally. Such continuous study provides a rare opportunity to ask questions that are only answerable through decades‐long monitoring of these long‐lived monkeys. In turn, the mounting data generated by long‐term study, including knowledge of lifetime reproductive success, familial relatedness, comprehensive behavioral and dietary repertoires, and patterns of inter‐ and intra‐annual variation in forest productivity, provide diverse opportunities to researchers, and facilitate studies that are of shorter duration. Here, we review some of the contributions of our longitudinal research on white‐faced capuchins and Geoffroy's spider monkeys, together with newer studies on mantled howler monkeys. We begin by synthesizing findings from our research on demography, dispersal, social relationships, and reproduction. These life history and social traits interact with their foraging and sensory ecology, which we review next. We end by highlighting how the longitudinal study of primates in Sector Santa Rosa has made direct and indirect contributions to the conservation of the critically endangered dry forest biome and its inhabitants, as well as to education, community, and forest restoration initiatives. In particular, we focus our review on how long‐term research is uniquely positioned to make key contributions spanning different topical areas.Abstract in Spanish is available with online material.

Fibular and metatarsal osteosynthesis in a southern brown howler monkey (Alouatta guariba clamitans)

Here we describe a successful surgical management of a distal fibular fracture combined with a tarsocrural luxation and multiple metatarsal fractures in the left foot of a southern brown howler monkey (Alouatta guariba clamitans). We achieved satisfactory outcome by applying intramedullary pinning for each of the bone fractures and closed reduction of joint luxation-kept in place only by bone alignment, without further ligament reconstruction. Bone healing occurred uneventfully within eight weeks and the monkey's foot regained its normal function. Therefore, we could properly release the patient back into the wild.

Environmental factors associated With Toxoplasma gondii Exposure in Neotropical Primates of Costa Rica.

The apicomplexan parasite Toxoplasma gondii (T. gondii) has been found in more than 350 species of homoeothermic vertebrates in diverse climates and geographic areas. In most animals, T. gondii produces mild or asymptomatic infection. However, acute and hyperacute toxoplasmosis is associated with high mortality rates observed in Neotropical primates (NP) in captivity. These primates are distributed in 20 countries across the Americas, and although infection has been reported in certain countries and species, toxoplasmosis in the wild and its impact on NP population survival is unknown. Differences among species in exposure rates and disease susceptibility may be due in part to differences in host behavior and ecology. Four species of NP are found in Costa Rica, i.e., howler (Alouatta palliata), spider (Ateles geoffroyi), capuchin (Cebus imitator), and squirrel monkeys (Saimiri oerstedii). This study reports NP exposure to T. gondii using the modified agglutination test in 245 serum samples of NP (198 wild and 47 from captivity) from Costa Rica. Associations of serostatus with environmental (forest cover, annual mean temperature), anthropogenic (human population density), and biological (sex) variables in howler and capuchin monkeys were evaluated. The seroprevalence among wild NP was 11.6% (95% CI = 7.7–17.34), compared with 60% in captive monkeys (95% CI = 44.27–73.63), with significant differences between species (X2 = 20.072; df = 3, p = 0.000164), suggesting an effect of behavior and ecology. In general, antibody titers were low for wild NP (<1:128) and high for captive NP (>1:8192), suggesting higher exposure due to management factors and increased life span in captivity. Seropositivity in howler monkeys was positively related to forest cover and inversely related to annual rainfall. For capuchins, annual rainfall was inversely related to seropositivity. Surveillance of T. gondii exposure in NP in captivity and in the wild is required to understand drivers of the infection and develop novel strategies to protect them.

Morfologia do tubo digestório de Alouatta belzebul

O Alouatta belzebul é uma espécie classificada como “Vulnerável” e isso se justifica principalmente pela caça, fragmentação e perda do hábitat nas florestas tropicais. A anatomia deste gênero apresenta características peculiares em todas as espécies estudadas, assim este trabalho objetivou descrever a morfologia do tubo digestório de Alouatta belzebul a fim de fornecer subsídios para avaliação de dietas, realização de procedimentos clínicos e cirúrgicos nestes animais. Foram utilizados 10 espécimes de Alouatta belzebul, adultos, machos, de diferentes idade. O trabalho foi realizado na Universidade Federal de Goiás e aprovado no comitê de ética N.083∕17. Os animais previamente criopreservados, foram descongelados e fixados por meio da infusão intramuscular e intracavitária de solução aquosa de folmol a 10%. Existem diversas variações na anatomia macroscópica do tubo digestório entre os primatas e estas variações ocorrem de acordo com os hábitos alimentares. Em Alouatta belzebul, que são folívoros-frugívoros, o tubo digestório abrange a maior parte da cavidade abdominal. Estes animais possuem números variáveis de rugas palatinas, de 10 a 17 pares de rugas, independente do sexo e idade, valores estes diferentes dos relatados para Sapajus libidinosus, de 18 a 21 pares de rugas. O estômago pseudo-compartimentalizado com uma região glandular e duas aglandulares, assemelhando com os achados de Nasalis larvatus. O intestino grosso apresenta o ceco aumentado em formato de L, corroborando com os achados em Callithrix penicillata. Os resultados demonstram que as variações estruturais do tubo digestório ocorrem de acordo com o hábito alimentar das diferentes espécies.

Lone males: Solitary and group-living male howler monkey (Alouatta palliata) behavioral ecology in a Costa Rican rainforest.

Many group-living primate species have evolved the capacity for some individuals to live alone for part of their lives, but this solitary life stage has rarely been the subject of focused research. The mantled howler monkey (Alouatta palliata) is a social primate species with bisexual dispersal that lives in mixed-sex groups with low male-to-female sex ratios. Consequently, males often spend a long period of their lives as solitary individuals. This study compares the tree use, feeding, and long-distance vocalization behavior of solitary and group-living mantled howler monkey males living within a fragmented rainforest in Costa Rica, La Suerte Biological Research Station. Based on differences in competitive ability between solitary and group-living males, we predicted that lone males would be found in significantly smaller feeding and resting trees, consume more low-quality foods, and produce shorter howling bouts made at lower rates than group-living males. We collected data on tree use and feeding during 30-min focal samples on male focal animals, recording data at 2-min intervals. We measured the trees in which the monkeys fed and rested for two or more intervals, and recorded the plant parts consumed. We recorded howling behavior using all-occurrences sampling. Lone males used significantly smaller feeding and resting trees, consumed more low-quality foods, and howled at lower rates but had longer howling bouts triggered by anthropogenic noise more than group-living males. Our results demonstrate that lone males differ in their behavioral ecology compared to group-living males, thus improving understanding of the solitary male life stage in primates.

Evaluating extinction debt in fragmented forests: the rapid recovery of a critically endangered primate

AbstractFragmented tropical forests can be highly dynamic, with the spatial configuration of forest patches changing through time. Yet, the lack of longitudinal studies limits our understanding of how patch dynamics affect biodiversity, especially when there is a time lag in species extinctions (extinction debt). We assessed how temporal changes in patch size, shape complexity and isolation affect populations of the Mexican howler monkey (Alouatta palliata mexicana), hypothesizing that we would find an extinction debt in this relatively long‐lived species. We assessed patch occupancy, subpopulation size and immature‐to‐female ratio in 39 forest patches from Los Tuxtlas, Mexico, in both 2001 and 2013. To identify time‐lag responses to habitat disturbance, we related demographic attributes in 2013 to patch metrics in 2001 and 2013 and tested whether primate subpopulations were better predicted by current or historical patch characteristics. We also assessed how changes in patch metrics affected each demographic attribute between 2001 and 2013. Patch size and shape complexity increased over time, whereas isolation decreased. These positive spatial changes were accompanied by a 1.6‐fold increase in mean subpopulation size over the same period. In addition, occupancy and immature‐to‐female ratio were similarly related to patch attributes in both years, suggesting that there is no extinction debt. Our findings are ‘good news’, suggesting that forest recovery over a relatively short period can promote the recovery of this Critically Endangered taxon. They also highlight the importance of preventing forest loss and promoting forest regeneration in human‐modified tropical landscapes.