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"Howler monkeys."
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Meet the howlers!
These rain forest dwellers are loud and sloppy. This playful poem brings howler monkeys to life in all their growly, barking glory. Extra facts within the text give readers the lowdown on these loudmouths.
Book
Determinants of Daily Path Length in Alouatta guariba in a Continuous Forest
Spatial use patterns in primates result from complex interactions among individual characteristics, physical, and ecological factors, such as temperature, food availability and distribution, and conspecific and heterospecific encounters. Understanding how these factors integrate is essential for interpreting variation in species' movement patterns. In this study, we evaluated how minimum temperature, day length, diet, rest and activity time, and social interactions influence the daily path length (DPL) of a group of brown howler monkeys ( Alouatta guariba ) sharing their habitat with muriquis ( Brachyteles arachnoides ), capuchin monkeys ( Sapajus cucullatus ), and black lion tamarins ( Leontopithecus chrysopygus ) in a continuous Atlantic Forest fragment, Brazil. We hypothesized that DPL is modulated by the integration of physiological constraints, ecological pressures, and dynamic social interactions. We followed the focal group for 22 full days between August 2023 and January 2024, recording GPS locations and behaviors at 5-min intervals, along with encounters with conspecific and heterospecific primates. A structural equation model based on Partial Least Squares Path Modeling explained 70% of the variation in DPL. Environmental variables (minimum temperature and day length) were positively associated with rest time, while both rest time and leaf consumption were negatively associated with path length. Encounters with heterospecifics were positively associated with displacement, while fruit consumption, conspecific encounters, and activity time showed no significant association. Collectively, these findings highlight the importance of simultaneously integrating ecological and social variables to understand the spatial organization of primates in continuous habitats.
Journal Article
Reversing defaunation by trophic rewilding in empty forests
Defaunation has a major driver of biodiversity loss in tropical forests. Here we discuss how to reverse defaunation by re-introducing key species in defaunated or restored forests.
Journal Article
Observed infanticides following a male immigration event in black howler monkeys, Alouatta pigra, at Palenque National Park, Mexico
This study describes two cases of directly observed and one case of nearly observed infanticide after an adult male immigrated into a multimale-multifemale group of black howler monkeys (Alouatta pigra) at Palenque National Park, Mexico. The immigrant male entered the group alone, injured the central adult male, presumably evicted the noncentral adult male, and killed all three young infants present over the course of three consecutive days in February 2010. Three weeks after the infanticide events, the three adult females who lost their infants were observed to sexually solicit and copulate with both the infanticidal male and the injured central male. Multimale mating is an effective reproductive strategy that females employ to confuse paternity and reduce the risk of infanticide, but the extent to which promiscuous mating after infanticide events is part of a counterstrategy in this species is still unknown. More cases of infanticide will need to be observed to assess the degree to which infanticide avoidance shapes the social system of the black howler monkey.
Journal Article
Age-related Changes in Dehydroepiandrosterone-sulfate in Black-and-gold Howler Monkeys (Alouatta caraya)
Dehydroepiandrosterone-sulfate (DHEAS) is the most abundant steroid in humans and some nonhuman primates. This adrenal androgen contributes to immune enhancement, neuroprotection, and reproduction. In humans and apes, DHEAS levels increase before puberty, a phenomenon called adrenarche. However, a postnatal increase in the levels of these hormones is not apparent in cercopithecoids. In marmosets, DHEAS is only synthesized from female adrenal glands, if their ovarian function is compromised. However, DHEAS is poorly investigated among other platyrrhines. Our main objective was to test the influence of sex and age on fecal and serum DHEAS levels in black-and-gold howler monkeys (
Alouatta caraya
) under human care. We measured DHEAS levels in feces from 16 females and 21 males aged between 6 months and 26 years old and in serum from 27 of those animals using a commercial enzyme immunoassay kit. We found high levels of serum DHEAS in adult females, and DHEAS levels in fecal and serum samples were strongly and positively correlated. Fecal DHEAS levels showed a quadratic relationship with age, increasing from infancy to adulthood, then declining in older adults. There was no significant effect of sex, although females had a greater range than males. The postnatal increase in DHEAS levels in howler monkeys is like that of apes and humans, while the large variation in DHEAS levels among adult females suggests that, as in marmosets, DHEAS may be important for female howler monkey reproduction. This pattern highlights the importance of comparative studies to investigate the biological function of DHEAS in evolution.
Graphical Abstract
Journal Article
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.
Journal Article
A comparison of inter- and intraspecific variation in seed dispersal in three South American primates
Primate communities vary in their level of redundancy, or overlap, in seed dispersal function, which could be due to body size, degree of frugivory or intraspecific variation, among other factors. In this study, we quantified redundancy in seed dispersal among three sympatric primate species: Lagothrix lagothricha, Alouatta seniculus and Sapajus apella in gallery forests in Meta, Colombia. We compared the median seed width dispersed and the number and species richness of large (≥5.9 mm wide) and very large (>7.5 mm wide) seeds per faecal sample. The medium-sized, highly folivorous A. seniculus mostly dispersed large seeds, the larger, highly frugivorous L. lagothricha dispersed very large and small seeds, and the smaller, partially frugivorous S. apella dispersed the smallest seeds. However, for L. lagothricha and S. apella, we did not find the expected results that adults disperse larger seeds than juveniles. Across species, there is complementarity in seed dispersal in relation to seed size, with L. lagothricha being unique in its contribution to the dispersal of very large seeds both in terms of quantity and richness.
Journal Article
A comparison of statistical methods for deriving occupancy estimates from machine learning outputs
The combination of autonomous recording units (ARUs) and machine learning enables scalable biodiversity monitoring. These data are often analysed using occupancy models, yet methods for integrating machine learning outputs with these models are rarely compared. Using the Yucatán black howler monkey as a case study, we evaluated four approaches for integrating ARU data and machine learning outputs into occupancy models: (i) standard occupancy models with verified data, and false-positive occupancy models using (ii) presence-absence data, (iii) counts of detections, and (iv) continuous classifier scores. We assessed estimator accuracy and the effects of decision threshold, temporal subsampling, and verification strategies. We found that classifier-guided listening with a standard occupancy model provided an accurate estimate with minimal verification effort. The false-positive models yielded similarly accurate estimates under specific conditions, but were sensitive to subjective choices including decision threshold. The inability to determine stable parameter choices a priori, coupled with the increased computational complexity of several models (i.e. the detection-count and continuous-score models), limits the practical application of false-positive models. In the case of a high-performance classifier and a readily detectable species, classifier-guided listening paired with a standard occupancy model provides a practical and efficient approach for accurately estimating occupancy.
Journal Article
Plasmodium Infections in Wild Mexican Primates, with the Detection of P. falciparum
Primates share several disease agents with humans. Some of these are of high medical concern, impacting both primate conservation and human health. Plasmodium parasites, responsible for malaria disease, have been associated with primate infection, and some species can be transferred between humans and other primates. In Mexico, despite the increasing rates of environmental transformation and human encroachment into the wild, there is no information regarding the occurrence of malaria parasites in wild primates in the country. We employed noninvasive sampling and molecular diagnostic techniques to detect Plasmodium infections in 14 populations of Alouatta pigra and Ateles geoffroyi in southern Mexico. We screened primate fecal samples for Plasmodium DNA through qPCR, and sequenced cytochrome b ( cytb ) and cytochrome c oxidase subunit 3 ( cox3 ) genes to identify parasites at the species level. We used Bayesian inference to assess the phylogenic position of the obtained cytb sequences. Prevalence of Plasmodium infection was 12% in A. pigra and 7% in A. geoffroyi . The highest percentage of Plasmodium infection in these primates coincides with areas of foci of human malaria in the country. We confirmed the presence of P. falciparum in three of 93 samples. Further studies are needed to assess the richness of Plasmodium species in Mexican primates and to understand disease dynamics at the interface between human and our fellow primates, along with its implications for both public health and primate conservation.
Journal Article