Measuring mantled howler monkey (Alouatta palliata) testes via parallel laser photogrammetry: Expanding the use of noninvasive methods.

Parallel laser photogrammetry (PLP), which consists of attaching two or three parallel laser beams at a known inter-beam distance to a camera, can be used to collect morphological measurements of organisms noninvasively. The lasers project onto the photo being taken, and because the inter-beam distance is known, they act as a scale for image analysis programs like ImageJ. Traditionally, this method has been used to measure larger morphological traits (e.g., limb length, crown-rump length) to serve as proxies for overall body size, whereas applications to smaller anatomical features remain limited. To that end, we used PLP to measure the testes of 18 free-living mantled howler monkeys (Alouatta palliata) at La Selva Biological Station, Costa Rica. We tested whether this method could reliably measure this relatively small and globular morphology, and whether it could detect differences among individuals. We tested reliability in three ways: within-photo (coefficient of variation [CV] = 4.7%), between-photo (CV = 5.5%), and interobserver (intraclass correlation = 0.92). We found an average volume of 36.2 cm3 and a range of 16.4-54.4 cm3, indicating variation in testes size between individuals. Furthermore, these sizes are consistent with a previous study that collected measurements by hand, suggesting that PLP is a useful method for making noninvasive measurements of testes.

Reconstruction of large scalp defect in a brown howler monkey (Alouatta guariba clamitans): A case report.

This case report describes different repair techniques used to reconstruct a large scalp defect in a brown howler monkey (Alouatta guariba clamitans) hit by a vehicle. Three reconstructive procedures were performed in two surgical stages. The repair techniques had successful outcomes on the patient's rehabilitation.

Predicting future climate change impacts on the potential distribution of the black howler monkey (Alouatta pigra): an endangered arboreal primate.

Climate change is one of the main factors affecting biodiversity worldwide at an alarming rate. In addition to increases in global extreme weather events, melting of polar ice caps, and subsequent sea level rise, climate change might shift the geographic distribution of species. In recent years, interest in understanding the effects of climate change on species distribution has increased, including species which depend greatly on forest cover for survival, such as strictly arboreal primates. Here, we generate a series of species distribution models (SDMs) to evaluate future projections under different climate change scenarios on the distribution of the black howler monkey (Alouatta pigra), an endemic endangered primate species. Using SDMs, we assessed current and future projections of their potential distribution for three Social Economic Paths (SSPs) for the years 2030, 2050, 2070, and 2090. Specifically, we found that precipitation seasonality (BIO15, 30.8%), isothermality (BIO3, 25.4%), and mean diurnal range (BIO2, 19.7.%) are the main factors affecting A. pigra distribution. The future climate change models suggested a decrease in the potential distribution of A. pigra by projected scenarios (from - 1.23 to - 12.66%). The highly suitable area was the most affected above all in the more pessimist scenario most likely related to habitat fragmentation. Our study provides new insights into the potential future distribution and suitable habitats of Alouatta pigra. Such information could be used by local communities, governments, and non-governmental organizations for conservation planning of this primate species.

Mantled howler monkey males assess their rivals through formant spacing of long-distance calls.

Formant frequency spacing of long-distance vocalizations is allometrically related to body size and could represent an honest signal of fighting potential. There is, however, only limited evidence that primates use formant spacing to assess the competitive potential of rivals during interactions with extragroup males, a risky context. We hypothesized that if formant spacing of long-distance calls is inversely related to the fighting potential of male mantled howler monkeys (Alouatta palliata), then males should: (1) be more likely and (2) faster to display vocal responses to calling rivals; (3) be more likely and (4) faster to approach calling rivals; and have higher fecal (5) glucocorticoid and (6) testosterone metabolite concentrations in response to rivals calling at intermediate and high formant spacing than to those with low formant spacing. We studied the behavioral responses of 11 adult males to playback experiments of long-distance calls from unknown individuals with low (i.e., emulating large individuals), intermediate, and high (i.e., small individuals) formant spacing (n = 36 experiments). We assayed fecal glucocorticoid and testosterone metabolite concentrations (n = 174). Playbacks always elicited vocal responses, but males responded quicker to intermediate than to low formant spacing playbacks. Low formant spacing calls were less likely to elicit approaches whereas high formant spacing calls resulted in quicker approaches. Males showed stronger hormonal responses to low than to both intermediate and high formant spacing calls. It is possible that males do not escalate conflicts with rivals with low formant spacing calls if these are perceived as large, and against whom winning probabilities should decrease and confrontation costs increase; but are willing to escalate conflicts with rivals of high formant spacing. Formant spacing may therefore be an important signal for rival assessment in this species.

Radiographically guided femoral neck osteosynthesis with cannulated compressive titanium screw and anti-rotational component in a Brown Howler Monkey (Alouatta guariba clamitans).

A Brown Howler Monkey presented with a femoral neck fracture was successfully treated with a cannulated compressive screw and an anti-rotational component inserted with radiographically guided technique. Complete bone consolidation and functional recovery were observed 9 weeks after the surgery, and the monkey was released to his place of origin.

Lead exposure and its relationship with fecal cortisol levels in black howler monkeys (Alouatta pigra).

Efficiently detecting early environmental threats to wildlife is vital for conservation. Beyond obvious dangers like habitat loss or deforestation, our study focuses on one of the most hazardous toxic metals for wildlife: lead (Pb). Pb is a widespread, cumulative, and insidious environmental pollutant that can trigger a wide range of physiological, biochemical, and behavioral disorders. In fact, Pb can cause permanent dysfunction of the major stress system, the hypothalamic pituitary adrenal (HPA) axis. We analyzed Pb and cortisol concentrations in fecal samples from Alouatta pigra in southern Mexico. Fecal samples were collected across six sites categorized as free-ranging (n = 65; conserved and disturbed) and from captive animals (n = 58). Additionally, we collected soil samples (n = 35). We found that Pb was present in 28% of fecal samples and 83% of soil samples. There was a positive relation between fecal and soil Pb levels, and fecal Pb concentration was negatively associated with cortisol levels. However, the claim of Pb being a direct interference with HPA axis requires further investigation. Given our findings, assessing wildlife exposure can be a valuable tool for understanding potential Pb exposure levels in the environment and its possible implications for human health. It can also serve as an early warning system of these consequences.

Food preferences and nutrient composition in captive Southern brown howler monkeys, Alouatta guariba clamitans.

Studies of food preferences in captive primates have so far mainly been restricted to frugivorous species. It was therefore the aim of the present study to assess the occurrence of spontaneous food preferences in a mainly folivorous primate, the captive Southern brown howler monkey, and to analyze whether these preferences correlate with nutrient composition. Using a two-alternative choice test, we presented ten male and five female adult Alouatta guariba clamitans with all possible binary combinations of ten types of food that are part of their diet in captivity and recorded their choice behavior. We found the howler monkeys to display the following rank order of preference: banana > mango > watermelon > papaya > beetroot > apple > pear > orange > cucumber > tomato. This preference ranking significantly and positively correlated with the total carbohydrate content and with the sucrose content of the food items. We also found significant positive correlations between the food preference ranking and the content of the minerals copper and magnesium. Male and female howler monkeys did not differ significantly in their food preference rankings. These results suggest this howler monkeys under human care are not opportunistic, but selective feeders with regard to maximizing their net gain of energy as only the content of carbohydrates, but not the contents of total energy, proteins, or lipids significantly correlated with the displayed food preferences. Thus, the food preferences of this primate are similar to those reported in several species of frugivorous primates tested with cultivated fruits and vegetables.

CAMPYLOBACTER HYOINTESTINALIS ISOLATION FROM HOWLER (ALOUATTA CARAYA) AND SPIDER MONKEYS (ATELES FUSCICEPS ROBUSTUS) AT A ZOOLOGIC FACILITY IN CENTRAL ILLINOIS.

Campylobacter hyointestinalis was initially isolated from an asymptomatic black howler monkey (Alouatta caraya) in a routine fecal culture examination. Fecal cultures from other individuals in this group and an adjacently housed black-headed spider monkey (Ateles fusciceps robustus) group recovered C. hyointestinalis from all but one of the individuals sampled (1.1 spider monkeys and 2.1 howler monkeys). Concurrently, one spider monkey presented with acute onset severe rectal prolapse and diarrhea. Whole-genome sequencing results of C. hyointestinalis isolates from all individuals were homologous and closely related to Campylobacter hyointestinalis subsp. hyointestinalis TTU_618, a strain typically associated with environmental samples. In addition, two cytolethal distending toxin (CDT) expressing gene clusters, cdt-I and cdt-II, were identified in all isolates. These results suggest C. hyointestinalis is transmissible to both howler monkeys and spider monkeys, though the origin of infection and whether it is transmissible between these species is undetermined.

Noise intensity modulates the responses of mantled howler monkeys to anthropophony.

Anthropogenic noise is a major global pollutant but its effects on primates are poorly understood, limiting our ability to develop mitigation actions that favor their welfare and conservation. In this study, we used an experimental approach to determine the impact of variation in noise intensity on mantled howler monkeys (Alouatta palliata). We conducted the study at Los Tuxtlas (México), where we studied the physiological stress (proxied via fecal glucocorticoid metabolites, fGCM) and behavioral responses of 16 males. We played back chainsaw noise at two intensities (40 and 80 dB) and used days in which groups were not exposed to noise as matched controls. With increased noise intensity fGCM increased, vigilance and vocalizations were longer, and vigilance, vocalizations, and flight occurred quicker. Physiological and behavioral responses occurred even after low-intensity noise playbacks (i.e., 40 dB). Therefore, noise intensity is a significant factor explaining the responses of mantled howler monkeys to anthropogenic noise. These results imply that management actions aimed at eradicating anthropogenic noise are required for the conservation and welfare of mantled howler monkeys at Los Tuxtlas.

Evaluation of Dental Enamel Thickness in Maxillary Teeth of Alouatta guariba clamitans, Alouatta caraya, and Sapajus nigritus by Cone Beam Computed Tomography.

Tooth enamel thickness is widely studied in primates and is important in differentiating taxa and in interpreting diet and feeding behavior. The objective of this study was to measure enamel thickness and discuss whether the results can be associated with different feeding patterns. Thirty-four syncraniums of Alouatta guariba clamitans, Alouatta caraya, and Sapajus nigritus were subjected to cone beam computed tomographic (CBCT) scans, and the dental enamel was measured in different regions of the crown using the multiplanar reconstruction tool. The differences observed indicate that for many variables and teeth, A. guariba clamitans showed significantly higher values compared to the other 2 species, with the exception of the cuspid region. Although the A. guariba clamitans is a folivorous species, it showed thicker enamel for most of the variables. CBCT was efficient in performing the measurements, allowing analysis of the syncraniums.

Mediastinal T-cell lymphoma in a free-ranging brown howler monkey (Alouatta guariba clamitans).

A free-ranging brown howler monkey (Atelidae: Alouatta guariba clamitans) was necropsied and a mediastinal T-cell lymphoma and esophageal dilation were diagnosed. The case report may contribute to the differential diagnosis of neoplastic and esophageal lesions in non-human primates and highlighted the importance of surveillance of cancer in wildlife.

Opportunistic meat-eating by urban folivorous-frugivorous monkeys.

The consumption of vertebrate tissues and eggs (hereinafter "meat") is relatively common among some primates that are highly frugivorous or eclectic omnivores, but rare or absent in those that are highly folivorous. The Neotropical howler monkeys (Alouatta spp.) belong in the latter group. Here we report the consumption of meat by free-ranging urban black and gold howler monkeys (Alouatta caraya) and discuss the potential role of the consumed meat as a source of energy, protein, or micronutrients. We studied three groups of howler monkeys (comprising four to seven individuals), living in city squares (0.6, 1.5, and 1.9 ha) in south Brazil, from July 2022 to May 2023 (65 days; 797 h of observations). All of the study groups were spontaneously supplemented daily by people with variable amounts and types of food provided. Meat was only offered in the two larger squares. The groups' diets included leaves (42-49% scan sampling feeding records), fruit (3-20%), and flowers (2-5%) from 13 to 20 plant species, and considerable amounts of supplemented food (27-50%). We recorded 33 individual events of ingestion of supplemented cooked meat, three individual events of dove egg predation, and three bird nest inspections without egg consumption. All members of the two groups in the larger squares, except an infant male, ingested meat at least once. Meat accounted for 1% of total scan feeding records of both groups with access to this supplement. We conclude that whereas the opportunistic consumption of meat probably contributed only minor amounts of energy and protein to the study subjects, it may have benefitted them with micronutrients that are scarce in plant foods.

Detection of herpesviruses in neotropical primates from São Paulo, Brazil.

Transmission of herpesvirus between humans and non-human primates represents a serious potential threat to human health and endangered species conservation. This study aimed to identify herpesvirus genomes in samples of neotropical primates (NTPs) in the state of São Paulo, Brazil. A total of 242 NTPs, including Callithrix sp., Alouatta sp., Sapajus sp., and Callicebus sp., were evaluated by pan-herpesvirus polymerase chain reaction (PCR) and sequencing. Sixty-two (25.6%) samples containing genome segments representative of members of the family Herpesviridae, including 16.1% for Callitrichine gammaherpesvirus 3, 6.1% for Human alphaherpesvirus 1, 2.1% for Alouatta macconnelli cytomegalovirus, and 0.83% for Cebus albifrons lymphocryptovirus 1. No co-infections were detected. The detection of herpesvirus genomes was significantly higher among adult animals (p = 0.033) and those kept under human care (p = 0.008671). These findings confirm the importance of monitoring the occurrence of herpesviruses in NTP populations in epizootic events.

Hematology and blood biochemistry in a declining population of mantled howler monkeys (Alouatta palliata palliata) at La Pacifica, Costa Rica.

BACKGROUND: Alouatta palliata palliata are an ecologically flexible howler monkey subspecies that has recently been relisted as Endangered. Populations are declining through much of the subspecies' range, including at our study site at La Pacifica, Costa Rica. Our objectives were to screen blood hematology and biochemistry samples collected from this wild population to elucidate their baseline health. METHODS: We collected blood samples from 38 adult individuals from across the study site and analyzed 13 hematology and 14 biochemistry parameters. RESULTS: Most hematology and blood biochemistry parameter values were similar between males and females. However, mean hemoglobin was significantly lower, and mean white blood cell count was significantly higher in females; and mean calcium and mean creatinine were significantly lower in females compared to males. CONCLUSIONS: Overall, the La Pacifica population appeared healthy based on the blood parameters analyzed from sampled individuals. Our results were also largely consistent with published data available from other populations of A. p. palliata, and with reference values for captive Alouatta caraya.

Fatal Simplexvirus humanalpha1 infection in howler-monkeys (Alouatta sp.) under human care: Clinical, molecular, and pathological findings.

BACKGROUND: Simplexvirus humanalpha1 (HuAHV-1) are common anthropozoonosis reported in marmosets but rare in howler monkeys (Alouatta sp.). METHODS: Necropsy of two brown-howler monkeys (A. caraya) and one red-howler monkey (A. guariba clamitans) from different zoo collections were performed. Fragments of all organs were examined through microscopy. Samples were submitted to IHC for Simplexvirus humanalpha 2 (HuAHV-2) [sin. Herpesvirus simplex type 2] and PCR. RESULTS: Grossly, only the A. guariba showed liver lesions characterized by multifocal, pinpoint white areas corresponding microscopically as random necrotizing herpetic hepatitis and ulcerative glossitis. Both A. caraya showed necrotizing meningoencephalitis with Cowdry A-type body inclusions within neurons and astrocytes. Immunolabeling for HuAHV-1/2 was observed in the tongue, liver, and brain. HuAHV-1 was confirmed in all samples by PCR, Sanger sequencing, and phylogenetic analyses. CONCLUSION: Necrotizing meningoencephalitis was appreciated in 2/3 of animals, and it is associated with neurologic signs. Along with ulcerative glossitis, a hallmark lesion in marmosets, it was present in one animal. Regarding herpetic hepatitis, it is not frequent in monkeys and occurs mainly in immunocompromised animals. HuAHV-1 infection was confirmed corroborating with a human source. This is the second report on captive black-howler monkeys and the first gross, histologic, immunohistochemical, and molecular description of herpetic hepatitis and ulcerative glossitis in red-howler monkeys (A. guariba).

Differences in sperm morphology between Alouatta palliata and Alouatta pigra are consistent with the intensity of sperm competition in each species.

The intensity of sperm competition, in which sperm compete within the female reproductive tract to reach and fertilize her eggs, varies in species with different mating systems. Sperm competition is more intense in species where males cannot monopolize access to reproductive females and females mate with multiple males. In this scenario, a morphological change that increases the ability of sperm to reach and fertilize eggs should rapidly spread in the population, leading to sperm morphological differences between closely related species. Differences in sperm morphology have been reported among primate species with different mating systems. However, due to the inherent logistical and ethical difficulties to sample sperm from wild primates, the extent of variation in sperm morphology within species and among closely related species remains understudied. Here, we compared sperm morphological traits from two sister howler monkey species (Alouatta palliata and Alouatta pigra) that have different mating systems to investigate the effect of sperm competition on sperm morphological traits. We predicted that sperm from A. palliata, where females have more opportunities to mate with multiple males, would show differences in traits associated with increase sperm competitiveness compared to A. pigra where females mostly mate with the central male. We used linear mixed models to determine species differences in sperm morphology, controlling for individual variation. We found that midpieces and heads in A. palliata sperm were on average 26.2% and 11.0% longer, respectively, than those of A. pigra. Differences in these traits are important for sperm speed and hydrodynamic movement in other species and can affect fertilization success. This study provides empirical evidence of sperm morphological traits that evolved through sexual selection in sister primate species with different mating systems.

Behavioral responses of mantled howler monkeys to neighbor long-distance vocalizations.

OBJECTIVES: Long-distance vocalizations are used by primates in a variety of contexts and may have different functions. The long-distance vocalizations of howler monkeys (Alouatta spp.) underlie the spatial regulation of neighboring groups and could be associated with the defense of food resources. Here, we test the hypothesis that the behavioral responses of mantled howler monkeys (A. palliata) to neighbor long-distance vocalizations are influenced by the potential for range defensibility while accounting for location within the home range and food availability. METHODS: We studied two groups for 13 months and a total of 888 h at La Flor de Catemaco (Mexico). Group 1 had a 92-ha home range and Group 2 had a 24-ha home range. We recorded vocalizations (N = 178 calls) and movements (N = 74 movements) of focal groups following long-distance vocalizations produced by their neighbors. RESULTS: Movement responses, but not vocal responses, were predicted by range defensibility, location, and food availability. As predicted, the group living in the smaller and more defendable range showed stronger movement responses than the group in the larger home range. These movement responses had a shorter latency and longer duration in more valuable spatial and temporal contexts (i.e., the core area and during periods of low food availability). CONCLUSIONS: These results suggest that the tradeoff between the costs and benefits of range defense varies according to the interactions between home range size and both the spatial (core areas) and temporal (food availability) abundance of resources. Thus, the responses of mantled howler monkeys to neighbor long-distance vocalizations could be related to home range defensibility.

Comparative gastrointestinal organ lengths among Amazonian primates (Primates: Platyrrhini).

OBJECTIVES: The morphological features of the gastrointestinal tract (GIT) in mammals reflect a species' food niche breadth and dietary adaptations. For many wild mammals, the relationship between the structure of the GIT and diet is still poorly understood, for example, the GIT for frugivorous primates is usually classified as unspecialized and homogeneous. Here, we compare the GIT structure of 13 primate species from the three families of extant platyrrhines (Atelidae, Pitheciidae, and Cebidae) in Amazonia, and discuss possible evolutionary adaptations to different diets and trophic niches. METHODS: We measured the length of the esophagus, stomach, small intestine, large intestine, cecum, colon, and rectum of the digestive tracts of 289 primate specimens. We determined the allometric relationships of the different tubular organs with the total length of the GIT as a proxy of specimen body size. Allometric parameters were used to establish the quotients of differentiation of every organ for each primate specimen. RESULTS: There was a high differentiation in structure of the digestive organs among genera. Alouatta specimens clearly separated from the other genera based on dissimilarities in gastric, colonic, and rectal quotients, likely linked to the fermentation of plant contents. In contrast, all cebines (Sapajus, Cebus, and Saimiri) and Cacajao species had similar small intestine quotients, which is expected due to their high rates of animal matter consumed. CONCLUSIONS: We show that diverse adaptations in digestive structure exist among frugivorous primates, which in turn reflect different dietary patterns within this group that may enable the geographic coexistence of different primate species.

Hematological and serum biochemistry evaluation in howler monkeys (Alouatta caraya) and capuchin monkeys (Sapajus apella): A comparative study.

BACKGROUND: Evaluation of blood parameters in captive non-human primates (NHPs) is crucial for monitoring their health and ensuring that their environment meets their physiological requirements. METHODS: We performed hemogram, serum biochemistry, and parasitological exams in 20 howler monkeys and 21 capuchin monkeys. RESULTS: In both species, over 50% of the individuals presented at least one parasite. There was a negative effect of age on red blood cell (RBC), white blood cell, platelets, total protein, globulin, and alkaline phosphatase, and a positive effect on the A:G ratio, gamma-glutamyl transferase, and mean platelet volume (MPV). Capuchin monkeys presented the highest platelets and alanine aminotransferase (ALT) values and howler monkeys presented the highest MPV, aspartate aminotransferase, ALT, amylase, glucose, bilirubin, and triglycerides values. We observed an interaction between species and sex on RBC, Htc, mean corpuscular hemoglobin concentration, and cholesterol. CONCLUSIONS: Species differences found in blood parameters may reflect differences in physiological adaptations associated with ecological and morphological traits and are clinically relevant for evaluating animal health and the suitability of breeding programs.

Dog barks influence the physiological stress and behavior of a wild primate.

Non-lethal impacts of dogs on primates have seldom been assessed. We used an experimental approach to determine if mantled howler monkeys (Alouatta palliata) perceive dog barks as an aversive stimulus and thus display physiological and behavioral responses toward simulated barks. For one year (1754 h of observations) we studied 16 adult males belonging to five groups in Los Tuxtlas (Mexico), and recorded the occurrence of naturally occurring dog barks, their sound pressure level (SPL), and the behavioral responses of howler monkeys to barks. We then exposed males to bark playbacks at two SPL treatments, 40 and 80 dB in a total of 50 experiments. We assayed glucocorticoid metabolite concentrations in fecal samples (fGCM) as a marker of the physiological stress response of males. We also recorded the duration of vigilance, vocalizations, and flight in relation to playbacks. Naturally occurring barks were frequent and usually elicited behavioral responses by males. fGCM concentrations increased after bark playbacks and with stimuli intensity. Time spent vigilant increased following playbacks independently of stimuli intensity but both vocalizations and flight were linked to stimuli intensity: vocalizations were the longest after barks played-back at 80 dB, but males spent more time fleeing in response to 40 dB bark playbacks. These results provide evidence that dog barks are pervasive in the habitat of mantled howler monkeys living at Los Tuxtlas and disturb males, both physiologically and behaviorally. Although the potential costs of physiological and behavioral responses could not be determined, there is sufficient evidence to assume that they do have negative impacts on individuals. Therefore, our study provides avenues for future research on dog-wildlife interactions and valuable information for the design of conservation actions aimed at mitigating the impact of dogs on mantled howler monkeys.