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.

DHEA Induces Sex-Associated Differential Patterns in Cytokine and Antibody Levels in Mice Infected with Plasmodium berghei ANKA.

Malaria is the most lethal parasitic disease worldwide; the severity of symptoms and mortality are higher in men than in women, exhibiting an evident sexual dimorphism in the immune response; therefore, the contribution of 17ß-estradiol and testosterone to this phenomenon has been studied. Both hormones differentially affect several aspects of innate and adaptive immunity. Dehydroepiandrosterone (DHEA) is the precursor of both hormones and is the sexual steroid in higher concentrations in humans, with immunomodulatory properties in different parasitic diseases; however, the involvement of DHEA in this sexual dimorphism has not been studied. In the case of malaria, the only information is that higher levels of DHEA are associated with reduced Plasmodium falciparum parasitemia. Therefore, this work aims to analyze the DHEA contribution to the sexual dimorphism of the immune response in malaria. We assessed the effect of modifying the concentration of DHEA on parasitemia, the number of immune cells in the spleen, cytokines, and antibody levels in plasma of CBA/Ca mice infected with Plasmodium berghei ANKA (P. berghei ANKA). DHEA differentially affected the immune response in males and females: it decreased IFN-γ, IL-2 and IL-4 concentrations only in females, whereas in gonadectomized males, it increased IgG2a and IgG3 antibodies. The results presented here show that DHEA modulates the immune response against Plasmodium differently in each sex, which helps to explain the sexual dimorphism present in malaria.

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.

Testosterone induces sexual dimorphism during infection with Plasmodium berghei ANKA.

Malaria is the most lethal parasitic disease worldwide; men exhibit higher mortality and more severe symptomatology than women; however, in most studies of immune response in malaria, sex is not considered a variable. Sex hormones 17ß-oestradiol and testosterone are responsible for the main physiological differences between sexes. When interacting with their receptors on different immune cells, they modify the expression of genes that modulate cell proliferation, differentiation, and synthesis of cytokines. The immunosuppressive activity of testosterone is well accepted; however, its participation in the sexual dimorphism of the immune response to malaria has not been studied. In this work, we analysed whether altering the concentration of testosterone, through increasing the concentration of this hormone for exogenous administration for three weeks, or gonadectomy before infection with Plasmodium berghei ANKA affects different cells of the immune response necessary for parasite clearance. We also assessed the concentration of pro-and anti-inflammatory cytokines in male and female CBA/Ca mice infected or not with the parasite. Our results show that testosterone changes affect females more than males, resulting in sex-associated patterns. Testosterone administration increased parasitaemia in intact males while reducing it in intact females leading to a dimorphic pattern. In addition, gonadectomy increased parasitaemia in both sexes. Moreover, testosterone administration prevented both weight loss caused by the infection in females and hypothermia in gonadectomized mice of both sexes. Boosting testosterone concentration increased CD3+ and CD8+ populations but decreased the B220+ cells exclusively in females. Additionally, testosterone reduced IFN-γ concentration and increased IL-6 levels only in females, while in males, testosterone increased the number of NK cells. Finally, gonadectomy decreased TNF-α concentration in both sexes. Our results demonstrate that testosterone induces different patterns depending on sex and testosterone concentration. The results of this work contribute to understanding the impact of modifying testosterone concentration on the immune response specific against Plasmodium and the participation of this hormone in sexual dimorphism in malaria.

Correlates of hormonal modulation in mantled howler monkey males, Alouatta palliata.

OBJECTIVES: The study of hormone modulation may offer important insight into the responses of individuals to environmental challenges. Here we studied C-peptide, thyroid hormone (T3), glucocorticoid (GC), and testosterone (T) metabolites of mantled howler males to assess: 1) correlations among hormones; 2) individual and temporal variation in hormone concentrations; and 3) the influence of ecological, climatic, behavioral, social, and reproductive factors on hormone variation. METHODS: We studied 10 adult males at La Flor de Catemaco (Mexico) from January 2012 to December 2016. We collected information on food availability; ambient temperature; time budgets; male involvement in mating, agonistic interactions, and interactions with extragroup males. We analyzed C-peptide concentrations in urine samples and T3, GC, and T in fecal samples. RESULTS: C-peptide was negatively correlated with other hormones, whereas T3, GC, and T were positively related. Hormonal variation was unrelated to individual or yearly differences. Food availability was positively related to C-peptide and T3, and negatively related to GC. Involvement in mating was positively related to T3 and T, whereas the rate agonistic interactions was positively related to GC and T. The rate of interactions with extragroup males was positively related to T. When males mated, the increase in C-peptide and the decrease in GC with increasing food availability were less notable. CONCLUSIONS: Hormonal variation in mantled howler monkey males is generally stable, but it is influenced by several factors. Our results offer a broad picture of the hormonal modulation of mantled howler monkey males in response to diverse challenges.

17ß-Estradiol Is Involved in the Sexual Dimorphism of the Immune Response to Malaria.

Malaria is the leading cause of parasitic infection-related death globally. Additionally, malaria-associated mortality is higher in men than in women, and this sexual dimorphism reflects differences in innate and adaptive immune responses that are influenced by sex hormones. Normally, females develop more robust immune responses against parasites than males. However, most clinical and laboratory studies related to the immune response to malaria do not consider sex as a variable, and relatively few studies have compared the sex-dependent role of 17ß-estradiol in this process. In this study, we decreased in vivo the levels of 17ß-estradiol by gonadectomy or administered 17ß-estradiol to intact or gonadectomized male and female CBA/Ca mice infected with Plasmodium berghei ANKA. Subsequently, we assessed the effects of 17ß-estradiol on parasite load; the percentages of different immune cells in the spleen; the plasma levels of antibodies and pro- and anti-inflammatory cytokines; and the mRNA expression levels of cytokine-encoding genes in the brain. The results showed that the administration of 17ß-estradiol increased parasitemia and decreased body weight in intact female mice. Moreover, intact females exhibited higher levels of CD8+ T cells and lower levels of NK1.1+ cells than their male counterparts under the same condition. Gonadectomy increased IFN-γ and decreased TNF-α concentrations only in intact female mice. Additionally, IL-10 levels were higher in intact females than in their male counterparts. Finally, the mRNA expression levels of cytokines coding genes in the brain showed a dimorphic pattern, i.e., gonadectomy upregulated Tnf, Il1b, and Il10 expression in males but not in females. Our findings explain the sexual dimorphism in the immune response to malaria, at least in part, and suggest potential sex-dependent implications for the efficacy of vaccines or drugs targeting malaria.

Maternal condition and maternal investment during lactation in mantled howler monkeys.

OBJECTIVES: Lactation is a costly reproductive state for females, as it may entail decreased body condition, increased morbidity, and increased mortality risk. To offset these costs, mothers should allocate investment in infant care as a function of their physical condition. Here, we assessed the relationship between maternal condition and maternal investment in wild mantled howler monkeys (Alouatta palliata) to determine: (1) whether maternal physical condition varied as a function of food availability, activity levels and feeding effort throughout lactation; (2) whether maternal investment was affected by maternal condition and offspring age. MATERIALS AND METHODS: We studied six adult females while rearing their immature offspring. We determined weekly food availability, C-peptide levels (as a measure of energy balance) in urine samples (306 samples), mothers' time budgets, feeding rates, time spent vigilant, and time spent carrying their offspring (for two years; 600 observation hours). RESULTS: C-peptide levels were positively related to food availability. Maternal care in terms of vigilance and offspring carrying peaked at early lactation and decreased progressively with offspring age. Carrying was positively related to C-peptide levels and was also influenced by variation in maternal condition throughout lactation. DISCUSSION: These results converge with previous theoretical and empirical studies on this topic and contribute to the growing evidence that nonhuman primate mothers allocate maternal care based on their current condition to maximize lifetime reproductive success.

Behavioural and Glucocorticoid Responses of a Captive Group of Spider Monkeys to Short-Term Variation in Food Presentation.

The presentation of food may affect feeding competition and the well-being of captive social species. We hypothesized that feeding competition in a captive group of 5 black-handed spider monkeys (Ateles geoffroyi) should increase in response to certain food presentations in terms of size, distribution and quality of food, and that higher feeding competition should lead to an increase in agonism and physiological stress (measured by faecal glucocorticoid metabolites, FGCM) as well as to a decrease in affiliation, proximity among individuals and feeding activity. We used 5 experimental treatments representing different combinations of size, distribution and quality of food. We observed social interactions for 100 h, collected 6,500 proximity and feeding activity records, and gathered 226 faecal samples. When food was clumped, individuals spent less time feeding, and there was also significant individual variation in feeding activity within treatments. FGCM levels were higher when food was clumped. These results are probably linked to an increase in feeding competition when food is concentrated. At least in small groups of spider monkeys, dispersing food in two feeding stations may be sufficient to decrease differences among individuals in priority of access to food resources, hence reducing physiological stress and interindividual differences in feeding activity.