Kenneth E. Glander

Background: Hematologic and blood biochemical values are key tools for assessing primate health. A long‐term behavioral study of howler monkeys at a single site (La Pacífica, Guanacaste, Costa Rica), afforded the opportunity to develop baseline values for a large group of animals, evaluating differences between adult males and females and comparing to a report in the same population two decades later.Methods: In 1998, 64 free‐ranging mantled howler monkeys were anesthetized and sampled for hematologic and biochemical analysis.Results: Blood analysis is reported for 29 adult females, 9 juvenile females, 19 adult males and 3 juvenile males. Four adults were excluded due to external injury or disease. There were few significant differences between adult females, juvenile females, and adult males.Conclusions: Baseline blood parameters are useful for determining normal values for howler monkey populations. The values for total protein, blood urea nitrogen, glucose, liver enzymes and potassium differed from a later study in 2019 may indicate changes that are influencing howler monkey health.

Objectives: Alouatta palliatapatterns of growth and sexual dimorphism are evaluated using 20 plus years of field data. Comparisons are made to other species ofAlouattaand other New World primates.Materials and methods: Records of 92A. palliatafrom Guanacaste Province, Costa Rica, were used to generate growth curves for body mass and linear measurements. Timing of growth for the properties was compared, and males and females were contrasted. Slopes and elevations for periods of rapid growth were evaluated. Growth allometry and proportion ratios were also explored.Results: Body mass growth is rapid during the first 2 years. Males and females begin to diverge around a year of age as male growth increases and female growth slows. Adult mass for both is reached about 4 years of age. Linear measurements show rapid growth the first 18 months for both sexes. Differences develop as males continue the same rate of linear growth while female growth slows. Adult size is reached for head and body length around 3 years, and for hind‐foot and tail lengths around 2 years.Discussion: A. palliatamales grow in mass more rapidly than females, while both grow similarly in linear dimensions, so that dimorphism is more pronounced in mass. This pattern is seen in other dimorphic New World primates. MaleA. palliatamay grow more rapidly thanA. seniculus, reflecting earlier emigration forA. palliatamales. Linear dimensions reach adult proportions earlier than body mass. For hind‐foot and tail, this is probably an adaptation for gripping.

Wild primates face grave conservation challenges, with habitat loss and climate change projected to cause mass extinctions in the coming decades. As large-bodied Neotropical primates, mantled howling monkeys (Alouatta palliata) are predicted to fare poorly under climate change, yet are also known for their resilience in a variety of environments, including highly disturbed habitats. We utilized ecophysiology research on this species to determine the morphological, physiological, and behavioral mechanisms howlers employ to overcome ecological challenges. Our data show that howlers at La Pacifica, Costa Rica are capable of modifying body size. Howlers displayed reduced mass in warmer, drier habitats, seasonal weight changes, frequent within-lifetime weight fluctuations, and gradual increases in body mass over the past four decades. These within-lifetime changes indicate a capacity to modify morphology in a way that can impact animals’ energetics and thermodynamics. Howlers are also able to consume foods with a wide variety of food material properties by altering oral processing during feeding. While this capability suggests some capacity to cope with the phenological shifts expected from climate change and increased habitat fragmentation, data on rates of dental microwear warns that these acclimations may also cost dental longevity. Lastly, we found that howlers are able to acclimate to changing thermal pressures. On shorter-term daily scales, howlers use behavioral mechanisms to thermoregulate, including timing activities to avoid heat stress and utilizing cool microhabitats. At the seasonal scale, animals employ hormonal pathways to influence heat production. These lines of evidence cumulatively indicate that howlers possess morphological, physiological, and behavioral mechanisms to acclimate to environmental challenges. As such, howlers’ plasticity may facilitate their resilience to climate change and habitat loss. While habitat loss in the tropics is unlikely to abate, our results point to a potential benefit of active management and selective cultivation to yield large, interconnected forest fragments with targeted phenology that provides both a complex physical structure and a diversity of food sources. These steps could assist howlers in using their natural acclimation potential to survive future conservation threats.

Anthropogenic habitat change can have varied impacts on primates, including both negative and positive outcomes. Even when behavioural shifts are seen, they may reflect decreased health, or simply behavioural flexibility; understanding this distinction is important for conservation efforts. This study examines habitat-related variation in adult and immature morphometrics among diademed sifakas (Propithecus diadema). We collected morphometric data from sifakas at Tsinjoarivo, Madagascar (19 years, 188 captures, 113 individuals). Captures spanned 12 groups, five within continuous forest (“CONT”), and seven in degraded fragments (“FRAG”) where sifakas have lower nutritional intakes. Few consistent differences were found between CONT and FRAG groups. However, using home range quality as a covariate rather than a CONT/FRAG dichotomy revealed a threshold: the two FRAG groups in the lowest-quality habitat showed low adult mass and condition (wasting), and low immature mass and length (stunting). Though less-disturbed fragments apparently provide viable habitat, we suggest the sifakas in the most challenging habitats cannot evolve fast enough to keep up with such rapid habitat change. We suggest other long-lived organisms will show similar morphometric “warning signs” (wasting in adults, stunting in immatures); selected morphometric variables can thus be useful at gauging vulnerability of populations in the face of anthropogenic change.

The eponymous vocalizations of howling monkeys (genusAlouatta) are associated with territorial defense and male-male competition, yet the extreme loudness of howls, which are among the loudest vocalizations of any terrestrial mammal, have yet to be fully explained. Loudness facilitates long-distance sound propagation but the effectiveness of any vocal signal depends in part on the auditory capabilities of the intended receiver, and the auditory sensitivities of howling monkeys are unknown. To better understand the evolution of loud calls, we used the auditory brainstem response (ABR) method to estimate the auditory sensitivities ofAlouatta palliata. The mean estimated audiogram of four wild-caught adults displayed a w-shaped pattern with two regions of enhanced sensitivity centered at 0.7-1.0 and 11.3 kHz. The lower-frequency region of auditory sensitivity is pitched moderately higher than the fundamental frequencies of howling, whereas the higher-frequency region corresponds well with harmonics in an infant distress call, thewrah-ha. Fitness advantages from detecting infants amid low-frequency background noise, including howling, could explain the incongruity between our ABR thresholds and the fundamental frequencies of howling. Attending to infant calls is expected to enhance reproductive success within an infanticidal genus, and we suggest that the extraordinary loudness of male howling is an indirect (runaway) result of positive feedback between the selective pressures of hearing infant distress calls and deterring infanticide.

Red-shanked doucs (Pygathrix nemaeus) are endangered, foregut-fermenting colobine primates which are difficult to maintain in captivity. There are critical gaps in our understanding of their natural lifestyle, including dietary habits such as consumption of leaves, unripe fruit, flowers, seeds, and other plant parts. There is also a lack of understanding of enteric adaptations, including their unique microflora. To address these knowledge gaps, we used the douc as a model to study relationships between gastrointestinal microbial community structure and lifestyle. We analyzed published fecal samples as well as detailed dietary history from doucs with four distinct lifestyles (wild, semi-wild, semi-captive, and captive) and determined gastrointestinal bacterial microbiome composition using 16S rRNA sequencing. A clear gradient of microbiome composition was revealed along an axis of natural lifestyle disruption, including significant associations with diet, biodiversity, and microbial function. We also identified potential microbial biomarkers of douc dysbiosis, includingBacteroidesandPrevotella, which may be related to health. Our results suggest a gradient-like shift in captivity causes an attendant shift to severe gut dysbiosis, thereby resulting in gastrointestinal issues.

The mammalian gastrointestinal (GI) tract is home to trillions of bacteria that play a substantial role in host metabolism and immunity. While progress has been made in understanding the role that microbial communities play in human health and disease, much less attention has been given to host‐associated microbiomes in nonhuman primates (NHPs). Here we review past and current research exploring the gut microbiome of NHPs. First, we summarize methods for characterization of the NHP gut microbiome. Then we discuss variation in gut microbiome composition and function across different NHP taxa. Finally, we highlight how studying the gut microbiome offers new insights into primate nutrition, physiology, and immune system function, as well as enhances our understanding of primate ecology and evolution. Microbiome approaches are useful tools for studying relevant issues in primate ecology. Further study of the gut microbiome of NHPs will offer new insight into primate ecology and evolution as well as human health.

Thyroid hormones boost animals’ basal metabolic rate and represent an important thermoregulatory pathway for mammals that face cold temperatures. Whereas the cold thermal pressures experienced by primates in seasonal habitats at high latitudes and elevations are often apparent, tropical habitats also display distinct wet and dry seasons with modest changes in thermal environment. We assessed seasonal and temperature‐related changes in thyroid hormone levels for two primate species in disparate thermal environments, tropical mantled howlers (Alouatta palliata), and seasonally cold‐habitat Japanese macaques (Macaca fuscata). We collected urine and feces from animals and used ELISA to quantify levels of the thyroid hormone triiodothyronine (fT₃). For both species, fT₃ levels were significantly higher during the cooler season (wet/winter), consistent with a thermoregulatory role. Likewise, both species displayed greater temperature deficits (i.e., the degree to which animals warm their body temperature relative to ambient) during the cooler season, indicating greater thermoregulatory pressures during this time. Independently of season, Japanese macaques displayed increasing fT₃ levels with decreasing recently experienced maximum temperatures, but no relationship between fT₃ and recently experienced minimum temperatures. Howlers increased fT₃ levels as recently experienced minimum temperatures decreased, although demonstrated the opposite relationship with maximum temperatures. This may reflect natural thermal variation in howlers’ habitat: wet seasons had cooler minimum and mean temperatures than the dry season, but similar maximum temperatures. Overall, our findings support the hypothesis that both tropical howlers and seasonally cold‐habitat Japanese macaques utilize thyroid hormones as a mechanism to boost metabolism in response to thermoregulatory pressures. This implies that cool thermal pressures faced by tropical primates are sufficient to invoke an energetically costly and relatively longer‐term thermoregulatory pathway. The well‐established relationship between thyroid hormones and energetics suggests that the seasonal hormonal changes we observed could influence many commonly studied behaviors including food choice, range use, and activity patterns.