Howler monkey ( Alouatta palliata ) thermal behavioral strategies and resting time are temperature-dependent

Mantled howler monkeys Alouatta palliata display a daily behavior pattern, but the time they rest can vary with the use of thermal behaviors to prevent endogenous heat production, maintain body temperature, and reduce the need to consume water or energy. The primary objective of this exploratory study was to determine the effects of fluctuations in temperature and relative humidity and behavioral thermoregula¬tion (body postures and tree stratum selection) on the resting time of A. palliata introduced in Agaltepec Island, Veracruz, Mexico. Focal animal sampling was carried out between October 2018 and August 2019, collecting 384 hours of fieldwork (observation/data recording) with 628 thermal behavioral records. We used a generalized linear mixed-effects model (GLMM) to observe the possible influence of the weather variables and behavioral thermoregulation on the rest time. The results showed differences in the temperature recorded in each posture and tree strata but according to the statistical models, the adoption of postures better explained (percentage of variance: 48.21 %) the time A. palliata rests. At higher ambient temperatures and lower humidities, the monkeys adopted an ex¬tended posture in the lower tree stratum and increased their resting time. These warm conditions likely pose a significant thermoregulatory challenge for howler monkeys, promoting the use of specific thermal behaviors that may affect resting times and potentially time allocated to other behaviors, such as locomotion and feeding. These changes in their behavior could compromise their survival if the temperature continues to rise and the relative humidity decreases due to the effect of climate change. Key words: Temperature, Thermoregulation, Body postures, Arboreal stratum, Daily behavior

Variation in tropical forest management directly affects biodiversity and provisioning of ecosystem services on a global scale, thus it is necessary to compare forests under different conservation approaches such as protected areas, payments for ecosystem services programs (PES), and ecotourism, as well as forests lacking any formal conservation plan. To examine the effectiveness of specific conservation approaches, we examined differences in forest structure and tree recruitment, including canopy cover; canopy height; seedling, sapling, and adult tree density; and average and total diameter at breast height (DBH) across 78 plots in 18 forests across Costa Rica representing protected areas, private forests utilizing PES and/or ecotourism, and private forests not utilizing these economic incentives. The effectiveness of conservation approaches in providing suitable primate habitat was assessed by conducting broad primate census surveys across a subset of eight forests to determine species richness and group encounter rate of three primate species: mantled howler monkey (Alouatta palliata), Central American spider monkey (Ateles geoffroyi), and the white-faced capuchin monkey (Cebus imitator). Only canopy height was significantly different across the three approaches, with protected areas conserving the tallest and likely oldest forests. Canopy height was also significantly associated with the group encounter rate for both mantled howler and spider monkeys, but not for capuchins. Total group encounter rate for all three monkey species combined was higher in incentivized forests than in protected areas, with capuchin and howler monkey group encounter rates driving the trend. Group encounter rate for spider monkeys was higher in protected areas than in incentivized forests. Incentivized conservation (PES and ecotourism) and protected areas are paragons of land management practices that can lead to variation in forest structure across a landscape, which not only protect primate communities, but support the dietary ecologies of sympatric primate species.

Hand preference is the preferential use of one hand for a single task. Its study provides insight into the neural mechanisms underlying motor skills, perception, and cognitive functions. From a comparative perspective, it also offers a window into evolutionary history, shedding light on whether manual preferences stem from genetics, environmental influences, or a combination of both. However, there is a paucity of information on preferential hand use for several primate taxa. Here we examine hand preference for the first time in mantled howler monkeys (Alouatta palliata) to determine if there is preferential hand use at the individual and population level as well as sex differences in hand use. We followed 17 wild adult individuals for 10months and used focal animal sampling (506 focal samples) to record hand use in two types of self-directed behaviors, touching (1246 events) and scratching (1115 events). According to the binomial tests, four individuals were right-hand-preferent, two were left-hand-preferent, and 11 were ambilateral during touching, whereas for scratching seven individuals were right-hand-preferent, two were left-hand-preferent, and eight were ambilateral. At the population level, there was ambilaterality in both behaviors. At the individual level, according to the HI index, hand preference in touching and scratching were not associated and did not vary between sexes. These findings concur with previous studies with howler monkeys and other taxa suggesting that population-level hand preference is not a universal trait across primates.

The circadian rhythm of the body core temperature (T(c)) and the effects of changes in ambient temperatures on the homeostasis of T(c) in Otsuka Long Evans Tokushima Fatty (OLETF) rats, which are naturally occurring cholecystokinin (CCK)-A receptor (CCK-AR) gene knockout (-/-) rats, were examined. In addition, the peripheral responses to warming or cooling of the preoptic and anterior hypothalamic region (PO/AH) were determined. The circadian rhythm of T(c) in OLETF rats was similar to that in Long-Evans Tokushima (LETO) rats; this rhythm was characterized by a higher T(c) during the dark period and a lower T(c) during the light period. When the ambient temperature was changed within the limits of 0 degrees C to 30 degrees C, the changes in T(c) of LETO rats were associated with the changes in ambient temperature, whereas those in OLETF rats were dissociated from the temperature changes. The OLETF rats showed a large hysteresis. The peripheral responses to warming or cooling of PO/AH, including shivering of the neck muscle and changes in skin temperature of the tail and footpad, were similar in OLETF and LETO rats. To confirm the role of CCK-AR in the regulation of body temperature, the values of T(c) in the CCK-AR(-/-) mice were compared with those in CCK-B receptor (CCK-BR) (-/-), CCK-AR(-/-)BR(-/-), and wild-type mice. In the mice, the circadian rhythms of T(c) were the same, regardless of the genotype. Mice without CCK-AR showed larger hysteresis than mice with CCK-AR. From these results, we conclude that the lack of CCK-AR causes homeostasis of T(c) in rats and mice to deteriorate.

In 1960 Adolph Schultz described several cases of plagiocephaly in a collection of mantled howler monkeys (Alouatta palliata) from the forests of Central America. Since then several more specimens have been described. These individuals make up one of the largest samples of nonhuman primates that are affected by craniosynostosis. In this study, we used finite element scaling analysis (FESA) to quantify morphologic differences between adult normal (N = 19) and plagiocephalic female howler monkeys (N = 4). FESA utilizes three dimensional coordinate data to provide detailed information on size and shape differences local to biologic landmarks. The relatively large number of plagiocephalic howler monkeys provides a natural means for examining hypotheses concerning patterns of dysmorphology associated with plagiocephaly. Comparison of our results to observations from the clinical literature reveals similarities in neurocranial and facial morphology among plagiocephalic humans and howler monkeys, but the direction and magnitude of local form differences between howler monkeys and humans indicate species-specific responses to sutural constraint. Few cases of craniosynostosis in nonhuman primates are known. The number of plagiocephalic howler monkeys suggests these monkeys may be particularly susceptible to some defect that leads to premature suture closure. If this is the case, then howler monkeys may be a good model to study the cause(s) of craniosynostosis.

In 1960 Adolph Schultz described several cases of plagiocephaly in a collection of mantled howler monkeys (Alouatta palliata) from the forests of Central America. Since then several more specimens have been described. These individuals make up one of the largest samples of nonhuman primates that are affected by craniosynostosis. In this study, we used finite element scaling analysis (FESA) to quantify morphologic differences between adult normal (N = 19) and plagiocephalic female howler monkeys (N = 4). FESA utilizes three dimensional coordinate data to provide detailed information on size and shape differences local to biologic landmarks. The relatively large number of plagiocephalic howler monkeys provides a natural means for examining hypotheses concerning patterns of dysmorphology associated with plagiocephaly. Comparison of our results to observations from the clinical literature reveals similarities in neurocranial and facial morphology among plagiocephalic humans and howler monkeys, but the direction and magnitude of local form differences between howler monkeys and humans indicate species-specific responses to sutural constraint. Few cases of craniosynostosis in nonhuman primates are known. The number of plagiocephalic howler monkeys suggests these monkeys may be particularly susceptible to some defect that leads to premature suture closure. If this is the case, then howler monkeys may be a good model to study the cause(s) of craniosynostosis.

Context For dairy cows housed indoors, ambient temperature and relative humidity are key drivers of heat stress, whereas for cows kept outdoors, solar radiation and wind speed are also important. Solar radiation directly increases the heat load on cows, whereas wind speed affects their ability to dissipate heat through convection and evaporation. Aim We aimed to determine whether climate-driven changes in these variables affect heat stress risk where cows are outdoors during summer and shoulder seasons, particularly in pasture-based farming systems such as in New Zealand. Understanding outdoor-specific factors is crucial for accurately assessing and mitigating heat stress in grazing dairy cattle, because their management needs differ substantially from those in housed systems. Methods Using daily climate projection data from 2006 to 2098, peak daily values of the temperature–humidity index (THI) of Thom and the grazing heat-load index (GHLI) of Bryant were calculated and used to map predicted changes in both the annual (June–May) number of days with heat stress risk and also the annual accumulated heat stress exposure (the sum of effective degrees Celsius above the threshold) for dairy production regions of New Zealand. Key results The results illustrated the limitations of using THI in the context of outdoor use, where solar radiation and wind speed are shown to be more important than relative humidity. The GHLI predicted that the risk of heat stress is already high in the Waikato (69 days), Bay of Plenty (69 days) and Canterbury (80 days) regions in the 2020s. Canterbury was also notable for having high heat stress exposure within day compared with other regions (i.e. heat stress days were particularly intense), attributable to the combined effect of high air temperatures, high solar radiation and low wind speeds. Conclusions According to climate projections, regions already experiencing high numbers of heat stress risk days and heat stress exposure in the 2020s will experience the greatest increases in heat stress risk to the 2050s. However, dramatic increases in the number of heat stress days are not anticipated. Implications This allows research and development to focus on mitigation practices in these regions where dairy farming systems must adapt to a changing climate. Mitigation strategies may include provision of shade, access to sprinklers, genetic selection for heat stress resilience, modifying feeding regimes to reduce heat load, or development of new solutions and technologies.

Space use patterns are the result of complex interactions between individuals and their environment. Although competition with conspecifics, the distribution and availability of food resources and climatic conditions may all influence space use by primates, these factors are usually addressed separately. Studies that integrate social, ecological, and physical factors have the potential to improve our understanding of variation in the spatial behavior of primates. We studied two groups of mantled howler monkeys (Alouatta palliata) in Los Tuxtlas, Mexico, to explore how intergroup competition, food availability, and ambient temperature influenced their use of space over 15 months. Loud calls produced by neighboring groups were a determining factor in the variation in the area used per month, daily ranging distance, and travel rate. Food availability did not influence any aspect of spatial behavior, but the distribution of feeding trees affected travel rate. Ambient temperature influenced the frequency and speed of travel. These results suggest that the spatial behavior of howler monkeys is influenced by social (intergroup competition), ecological (food distribution), and physical (ambient temperature) factors, and that the specific effects of these factors vary among measures of space use.


 
 
 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).
 
 

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.

Heat Stress: A Hazardous Occupational Risk for Vulnerable Workers

Long-term field studies are critical for our understanding of animal life history and the processes driving changes in demography. Here, we present long-term demographic data for the northernmost population of mantled howler monkeys (Alouatta palliata) residing in a highly anthropogenically fragmented landscape in Los Tuxtlas, Mexico. We carried out 454 monthly group visits to 10 groups of mantled howler monkeys between 2000 and 2011. The population remained relatively stable over the 11-year study period, with an overall increase in the total number of individuals. Birth rates and inter-birth intervals were comparable to those of howler monkeys at non-fragmented sites, suggesting that living in a fragmented landscape did not affect the reproductive output of our study population. Moreover, despite the landscape, dispersal events were commonplace, including many secondary dispersals (individuals emigrating from groups that they had previously immigrated into). Finally, we found a marked effect of seasonality on the dynamics of our study population. In particular, the period of lowest temperatures and resource scarcity between November and March was associated with higher mortality and reproductive inhibition, while the period of resource abundance between April and May was associated with the majority of conceptions and weaning of offspring. This, in turn, could be influencing dispersal patterns in our study area, as male howler monkeys seem to time some of their immigrations into new groups to coincide with the start of the period of higher fertility, while females preferentially joined new groups several months before the onset of this period. These data have important implications for the conservation and management of howler monkeys in fragmented landscapes, as well as for our understanding of the effect of seasonality over howler monkey dispersal, reproduction and survival.

We studied the geographic distribution of the endangered black howler monkey, Alouatta pigra, in its southeastern range in eastern Guatemala along its putative contact zone with the mantled howler monkey, A. palliata. A distributional survey of both species was conducted through direct observations and interviews, and the data analyzed with GIS to detect potentially limiting geographic and ecological factors. Alouatta pigra was not associated with any specific vegetation type or altitudinal range, as it occurred in many forest types from the lowlands up to elevations of 2705 m a.s.l., in contrast to prior reports of it being restricted to elevations below 400 m a.s.l. and having a strong affinity for riverine forests. Alouatta palliata did not occur at the higher elevations. Distribution of both howler monkey species was unaffected by the presence of Ateles, by protection status of the survey site, or by hunting activities. Deforestation appears to have restricted both species in some areas. Throughout the southeastern range of A. pigra, we found no evidence for current sympatry with A. palliata, as their distributions are separated by a river barrier and unsuitable dry shrubland. Ecological preferences also seem to reinforce allopatry, with only A. pigra occurring in wet and cold montane forests of the Sierra de las Minas. Our data indicate that highland habitats in Mexico and Guatemala, previously considered unsuitable for A. pigra, may need to be evaluated for distribution assessments and management plans. Populations of A. pigra in the diverse protected ecosystems in eastern Guatemala may be an important component for conservation of the species.

Four groups of mantled howling monkeys (Alouatta palliata) were observed at El Zota Biological Field Station in northeastern Costa Rica to assess whether resource scarcity caused by anthropogenic disturbance and hypothesized increased competition for limited resources would result in more frequent and more aggressive interactions between neighboring howling monkey groups and between howling monkeys and other, sympatric primate species, namely white-faced capuchins (Cebus capucinus) and black-handed spider monkeys (Ateles geoffroyi). Using a comparison between the primary forest, as a control, and anthropogenically-altered secondary forest, I examined whether a behavioral difference existed between groups with hypothesized varying degrees of resource competition. Intergroup encounters were broken down into long distance howling bouts, with 46 observed, and close proximity interactions, with 11 observed. Results showed an increased frequency of howling in the primary forest as compared with the secondary forest, but no difference between the frequency, duration, or type of close-proximity intergroup encounters. Forty-five interspecies interactions were observed between howling monkeys and sympatric primate species. These interactions showed no difference between forest type for frequency, duration, or type of interaction. These results suggest that the composition and resource availability of the secondary forest at this site that does not align with current assumptions of habitat degradation. Alternatively results may be a reflection of social pressures such as infanticide, intragroup competition, and genetic relatedness as factors shaping howling monkey behaviors in both primary and secondary forests.

The current Chilean population originated from admixture between aboriginal populations (Amerindians) and Spanish conquerors of European origin. Consequently, the unions that gave rise to the Chilean population were chiefly between Spanish males and aboriginal females, and not the converse. To test the hypothesis that the Y chromosome of the Chilean population is mainly of Spanish origin, while the other chromosomes are from mixed (European and aboriginal) origin, we studied the DYS19 and DYS199 loci in two samples. One sample was obtained from a high socioeconomic stratum, while a second sample was from a low stratum. We studied male blood donors (N = 187) from Santiago, the capital of the country. Subjects were typed for the autosomal ABO and Rh (locus D) blood groups, and for the Y-linked DYS19 and the DYS199 loci, reported as Y-chromosome haplotypes. The aboriginal admixture was estimated for each genetic marker. The percentage of aboriginal admixture was 38.17% for the ABO system and 31.28% for the Rh system in the low socioeconomic stratum and 19.22% and 22.5%, respectively, in the high stratum. Y-chromosome haplotype frequencies constructed from the DYS19 and DYS199 loci demonstrated that the main haplotypes were DYS19*14/DYS199 C, as is often the case with many European populations, and DYS19*13/DYS199 C. The aboriginal admixture from Y-haplotype frequencies was estimated to be 15.83% in the low socioeconomic stratum and 6.91% in the high stratum. These values are lower than the values found using autosomal genetic markers, and are consistent with the historical background of the population studied. This study highlights the population genetic consequences of the asymmetric pattern of genome admixture between two ancestral populations (European and Amerindian).