Can cyclone exposure explain behavioural and demographic variation among lemur species?

Madagascar has a harsh and stochastic climate because of regular natural disturbances. This history of regular cyclones has been hypothesised to have directed evolutionary changes to lemur behaviour and morphology that make them more resilient to sudden environmental change. These adaptations may include: small group sizes, high degrees of energy-conserving behaviours, generalist habitat use, small home ranges, small body size, and a limited number of frugivorous species. To date, however, no one has tested how variation in cyclone exposure across Madagascar is associated with variation in these resilience traits. In this study, we created a detailed cyclone impact map for Madagascar using Koppen-Geiger climate class, historical cyclone tracks, the Saffir Class of cyclone and hurricane intensity, and precipitation data. We also used existing literature to calculate a resilience score for 26 lemur species for which data existed on resilience traits. Our cyclone impact map was then overlaid on known geographic ranges of these species and compared to resilience score while controlling for phylogenetic non-independence and spatial autocorrelation. We found no association between cyclone impact in a lemur range and their resilience score. When assessing traits individually, however, we found that cyclone impact was positively associated with body size, suggesting that the more impacted a species is by cyclones the smaller they are. We also found cyclone impact to be negatively associated with frugivory, with species in higher impact zones eating more fruit. While unexpected, this could reflect an increased production in fruit in tree fall gaps following cyclones. While we did not find a pattern between cyclone impact and behavioural resilience in lemurs, we suggest a similar study at a global scale across all primates would allow for more taxonomic variation and reveal larger patterns key to understanding past and future vulnerability to natural disturbances in primates.

Density and population size estimates of the endangered northern yellow-cheeked crested gibbon Nomascus annamensis in selectively logged Veun Sai-Siem Pang National Park in Cambodia using acoustic spatial capture-recapture methods.

Many gibbon species are threatened with extinction, including the endangered northern yellow-cheeked crested gibbon, Nomascus annamensis. Assessing gibbon populations and understanding how human disturbances and environmental factors impact these populations is vital for effective conservation planning. In 2010, auditory surveys revealed that Veun Sai-Siem Pang National Park (VSSP) in Cambodia contains one of the largest known N. annamensis populations in the world, with an estimated 456 (95% CI 421-490) gibbon groups. Illegal selective logging is common in the park, but the impact of continued logging on the gibbon population has not been investigated. To determine any change in the N. annamensis population since 2010, between January and April 2019 we conducted auditory surveys at 13 sites that were at least 4 km apart. We surveyed each site for three days, each day recording the gibbon calls heard over 3.25 hours from three listening posts located 500 m apart. At the same sites, we assessed the logging intensity using transects and ecological plots. Gibbon densities can be influenced by various environmental factors such as canopy height and forest type. Therefore, in addition to investigating the relationship between the density of N. annamensis groups and logging, we included five additional environmental variables in our acoustic spatial capture-recapture models. Our best fit model with the lowest AIC value included canopy height, forest type, distance to villages, and logging. We estimate that there are 389 (95% CI 284-542) N. annamensis groups currently in VSSP. Selective logging is widespread in the park, primarily targeting four tree species. The estimated felling time of these logged trees, together with previous reports, indicate that the species most targeted in VSSP varies over time. To conserve the N. annamensis population in VSSP, it is crucial that action is taken to reduce illegal logging.

Opportunities for primary health care: a qualitative study of perinatal health and wellbeing during bushfire crises.

BACKGROUND: During the summer of 2019/2020, Australia experienced a catastrophic wildfire season that affected nearly 80% of Australians either directly or indirectly. The impacts of climate crisis on perinatal health have only recently begun to receive attention. The objective of this study was to understand experiences of perinatal women during the bushfire and smoke events of 2019-2020 regarding health, health care, and public health messaging. METHODS: Semistructured interviews were conducted by phone or web conferencing platforms with 43 participants living in the south-east of Australia who were either pregnant or who had recently had a baby during the 2019/2020 fires. RESULTS: The health impacts on participants of the fires, associated smoke, and evacuations for some, were both physical and psychological. Many participants sought information regarding how to protect their own health and that of their unborn/recently born children, but reported this difficult to find. CONCLUSIONS: Pregnant women and new mothers exposed to bushfire events are a risk group for adverse physical and psychological outcomes. At the time of the 2019/2020 Australian bushfires, exposed women could not easily access evidence-based information to mitigate this risk. Family practitioners are well placed to provide pregnant women and new mothers with this sought-after information, but they need to be prepared well in advance of future similar events.

Severe cyclones and sex-specific birth outcomes in Queensland, Australia: An interrupted time-series analysis.

OBJECTIVES: A male is less adaptable to biological stressors than a female fetus with consequent higher morbidity and mortality. Adverse birth outcomes increase and male livebirths decrease after environmental disasters, economic crises, and terrorist events. We hypothesized the ratio of male to female livebirths would decrease in areas affected by severe tropical cyclones (TCs) in Queensland, Australia. Additionally, in male livebirths, there would be an increase in preterm and low birthweight births. Lastly, we hypothesized that the pregnancy stage at which exposure occurred would modify the association between TC exposure and observed outcomes. METHODS: Interrupted time series analysis was used to analyze Queensland administrative birth records from July 2007 to June 2018 for significant changes in the sex ratio at birth, measured as the proportion of male livebirths. Adjusted generalized linear models were fitted to births in areas affected by two category five TCs: cyclones Yasi (February 2011) and Marcia (February 2015). To explore male mortality and morbidity risk, additional analysis was conducted on the proportion of male stillborn, low birthweight, and preterm births. The association between estimated pregnancy stage during the TC and the proportion of male births was also analyzed. RESULTS: Contrary to our hypothesis, increases in the proportion of male livebirths were observed following early-pregnancy exposure to cyclone Yasi and mid-pregnancy exposure to Marcia, although the latter was not statistically significant. No significant changes were observed in proportions of male stillborn, low birthweight, and preterm births. CONCLUSIONS: This study found a significant association between severe TCs and sex ratio at birth. The stage of pregnancy at which maternal stressors were experienced modified this association. Among people exposed in early to mid-pregnancy, the proportion of male births was higher. This may be because of differential loss of females in utero. Studying sex differences in birth outcomes provides insight into in utero vulnerabilities associated with environmental stressors. Climate change is increasing the intensity and frequency of natural disasters. Understanding fetal vulnerability to environmental stressors will provide crucial information supporting early life health interventions that mitigate the immediate and long-term effects.

"The influence of olfactory enrichment on the behavior of two captive New World primates: Black-capped capuchin (Sapajus apella) and common marmoset (Callithrix jacchus)".

Environmental enrichment is an animal husbandry principle that seeks to provide the stimuli necessary for the optimal physiological and psychological well-being of animals. Due to primates having highly developed visual systems, there have been limited attempts to quantify the benefit of olfactory enrichment on captive primate populations. We aim to investigate how a range of odors may influence the behaviors of two captive New World primate species that have varying reliance on olfactory pathways, black-capped capuchin (Sapajus apella) and common marmoset (Callithrix jacchus), at the National Zoo and Aquarium, Canberra, Australia. We presented three odors (rosemary oil, Salvia rosmarinus, banana essence and white-tailed deer urine, Odocoileus virginianus) four different times to the two species following a 12-week randomized schedule. Using instantaneous scan sampling we collected behavioral and direct cloth interaction (DCI) data on 40 days. We then calculated activity budgets. Results show both species significantly respond to different olfactory conditions. S. apella responded to banana by decreasing inactivity (df = 4, F = 6.600, p = .007), and increasing DCI frequencies (df = 3, F = 116.196, p < .0001) whereas C. jacchus was influenced by rosemary and deer urine-also reducing inactivity levels (df= 4, F = 15.938, p < .0001), but not changing DCI frequencies. We also tested habituation however it is not significant for either species over the course of the study. This comparative investigation is one of the first of its kind and uncovers the possibility for olfactory stimulus to be successfully used as a type of beneficial environmental enrichment for captive primates, supporting the constructive and ongoing development of enrichment programs at captive facilities.

Positional behavior and canopy use of black snub-nosed monkeys Rhinopithecus strykeri in the Gaoligong Mountains, Yunnan, China.

Studies on positional behavior and canopy use are essential for understanding how arboreal animals adapt their morphological characteristics and behaviors to the challenges of their environment. This study explores canopy and substrate use along with positional behavior in adult black snub-nosed monkeys Rhinopithecus strykeri, an endemic, critically endangered primate species in Gaoligong Mountains, southwest China. Using continuous focal animal sampling, we collected data over a 52-month period and found that R. strykeri is highly arboreal primarily using the high layers of the forest canopy (15-30 m), along with the terminal zone of tree crowns (52.9%), medium substrates (41.5%), and oblique substrates (56.8%). We also found sex differences in canopy and substrate use. Females use the terminal zones (56.7% versus 40.4%), small/medium (77.7% versus 60.1%), and oblique (59.9% versus 46.5%) substrates significantly more than males. On the other hand, males spend more time on large/very large (39.9% versus 22.3%) and horizontal (49.7% versus 35.2%) substrates. Whereas both sexes mainly sit (84.7%), and stand quadrupedally (9.1%), males stand quadrupedally (11.5% versus 8.3%), and bipedally (2.9% versus 0.8%) more often than females. Clamber, quadrupedalism, and leap/drop are the main locomotor modes for both sexes. Rhinopithecus strykeri populations never enter canopies of degenerated secondary forest and mainly use terminal branches in the middle and upper layers of canopies in intact mid-montane moist evergreen broadleaf forest and hemlock coniferous broadleaf mixed forests across their habitat.

Association between severe cyclone events and birth outcomes in Queensland, Australia, 2008-2018: a population based retrospective cohort study.

OBJECTIVE: Investigate an association between severe tropical cyclones (TCs) and birth outcomes in an Australian population. METHODS: We analysed over 600,000 singleton livebirths collected through the Queensland Perinatal Data Collection between 2008 and 2018. We estimated the odds ratios (ORs) of adverse birth outcomes using logistic multi-level modelling. RESULTS: Exposure to TCs in early pregnancy was associated with significantly higher odds of preterm births in affected compared to unaffected areas during the TC year [OR=1.28, 95%CI=1.11, 1.49, p=0.001] and slightly significant higher odds in affected areas during TC years compared to non-TC years. Significantly higher odds of low birthweight births were associated with mid-pregnancy exposure to cyclone Marcia [OR=1.62, 95%CI=1.00, 2.40, p=0.016] . CONCLUSIONS: Findings aligned with studies demonstrating an association between exposure to environmental stressors in early to mid-pregnancy and adverse birth outcomes. IMPLICATIONS FOR PUBLIC HEALTH: There is limited research into TCs and perinatal health in Australia despite most of the population residing along coastlines and TCs presenting one of the nation's most devastating weather events. This study will inform public health practice and contribute to further research into mitigating environmental risks faced by pregnant women.

The 10th anniversary of the scientific description of the black snub-nosed monkey (Rhinopithecus strykeri): It is time to initiate a set of new management strategies to save this critically endangered primate from extinction.

Traditionally, the genus Rhinopithecus (Milne-Edwards, 1872, Primates, Colobinae) included four allopatric species, restricted in their distributions to China and Vietnam. In 2010, a fifth species, the black snub-nosed monkey (Rhinopithecus strykeri) was discovered in the Gaoligong Mountains located on the border between China and Myanmar. Despite the remoteness, complex mountainous terrain, dense fog, and armed conflict that characterizes this region, over this past decade Chinese and Myanmar scientists have begun to collect quantitative data on the ecology, behavior and conservation requirements of R. strykeri. In this article, we review the existing data and present new information on the life history, ecology, and population size of R. strykeri. We discuss these data in the context of past and current conservation challenges faced by R. strykeri, and propose a series of both short-term and long-term management actions to ensure the survival of this Critically Endangered primate species. Specifically, we recommend that the governments and stakeholders in China and Myanmar formulate a transboundary conservation agreement that includes a consensus on bilateral exchange mechanisms, scientific research and monitoring goals, local community development, cooperation to prevent the hunting of endangered species and cross-border forest fires. These actions will contribute to the long-term conservation and survival of this Critically Endangered species.

Pregnancy outcomes among evacuees of the Sinabung volcano, 2010-2018 (North Sumatra, Indonesia): A matched cohort study.

OBJECTIVES: Exposure to natural disasters during pregnancy is associated with adverse birth outcomes and increased probability of female births. Nonetheless, relatively little work has been done on evacuations of women living in close vicinity to volcanic eruptions. We conducted a retrospective cohort study among women from villages near the Sinabung volcano in North Sumatra, Indonesia, which has been active since 2010. METHODS: We compared an "exposed" sample of women (n = 97) who were pregnant when forced to evacuate their villages due to the volcanic eruptions and an "unexposed" sample of non-evacuees (n = 97) matched for age and year of child's birth. We collected anthropometric data (height and weight of each woman) and conducted structured interviews about pregnancy outcomes and evacuation-related stress. RESULTS: Evacuation led to an almost five-fold increase in the adjusted odds of having an early or preterm birth in non-imputed (OR = 4.84, 95% CI: 1.31-17.92) and multiply imputed (OR = 4.84, 95% CI: 1.29-19.19) analyses. It also led to approximately a 1 cm decrease in birth length in the non-imputed (ß = -1.10, 95% CI: -1.96-0.24) and multiply imputed (ß = -1.17, 95% CI: -1.20-0.36) analyses, both including controls for confounders. We found decreasing birth length with increasing stress among evacuees. There was no discernible effect of evacuation or stress on the other outcomes. CONCLUSIONS: Both adverse effects we documented can exert negative influences on later-in-life outcomes for children of women pregnant during evacuation. This should be considered when developing protocols for supporting women and connecting them with clinical resources when evacuated from natural disasters.

Growth of Neanderthal infants from Krapina (120-130 ka), Croatia.

Modern humans have a slow and extended period of childhood growth, but to what extent this ontogenetic pathway was present in Neanderthals is debated. Dental development, linked to the duration of somatic growth across modern primates, is the main source for information about growth and development in a variety of fossil primates, including humans. Studies of Neanderthal permanent teeth report a pace of development either similar to recent humans or relatively accelerated. Neanderthal milk teeth, which form and emerge before permanent teeth, provide an opportunity to determine which pattern was present at birth. Here we present a comparative study of the prenatal and early postnatal growth of five milk teeth from three Neanderthals (120 000-130 000 years ago) using virtual histology. Results reveal regions of their milk teeth formed quickly before birth and over a relatively short period of time after birth. Tooth emergence commenced towards the earliest end of the eruption schedules displayed by extant human children. Advanced dental development is consistent with expectations for Neanderthal infant feeding.

Cafeteria-style feeding trials provide new insights into the diet and nutritional strategies of the black snub-nosed monkey (Rhinopithecus strykeri): Implications for conservation.

Anthropogenic changes and fragmentation of natural habitats often exert a negative effect on resource availability and distribution, and the nutritional ecology and feeding behavior of nonhuman primates. The goals of this study are to examine food choice and to identify the nutritional profile of foods consumed by the Critically Endangered black snub-nosed monkey (Rhinopithecus strykeri). To accomplish our study goals, we presented cafeteria-style feeding trials of fresh food items collected in the home range of wild black snub-nosed monkeys to the only two captive R. strykeri, and compared the nutritional profiles of the leafy foods (buds, young, and mature leaves, 100 i23tems from 70 plant species) selected with those avoided (54 items from 48 plant species). Overall, the results indicate that captive R. strykeri selected foods that were higher in moisture (Mo; 77.7%), crude protein (CP; 21.2%), total nonstructural carbohydrates (TNC; 34.9%), and phosphorus (P; 0.37%) while tending to avoid foods with a neutral detergent fiber (NDF) content of greater than 46.8%. Leaves collected in autumn and selected by the monkeys were characterized by a slightly higher amount of metabolizable energy (ME) than those rejected (1,350 kJ/100 g vs. 1,268 kJ/100 g). In contrast, the protein content of foods collected and consumed during the spring was greater (22.9%) than in autumn (16.4%). Random Forests modeling, an ensemble learning method, indicated that the proportion of Mo, NDF, ME, CP, P, and TNC were among the most important factors in predicting which items were consumed by the captive R. strykeri during spring and autumn. On the basis of the nutritional profile of foods consumed across the two seasons, we identified 18 nutrient-rich native plant species that we recommend for use in ex- and in-situ conservation management and reforestation programs to provide long-term access to a nutritionally adequate diet.

Enamel neonatal line thickness in deciduous teeth of Australian children from known maternal health and pregnancy conditions.

BACKGROUND: Physiological disruptions to early human development have implications for health and disease in later life. Limited research has explored how prenatal factors influence dental development in children of mothers with known pregnancy conditions. Enamel in human deciduous teeth begins forming in utero and is highly susceptible to physiological upsets experienced perinatally. The moment of birth itself is marked in deciduous enamel by the Neonatal Line (NNL) as a baby transitions from the uterine to external environment. This study evaluates the effect of maternal health factors that include stress and alcohol consumption on NNL in teeth from Australian children. STUDY DESIGN AND SUBJECTS: Mothers (n = 53) were interviewed about their health during pregnancy and experience of birth. Sixty-five deciduous teeth (incisors, molars, one canine) from their children were donated for histological examination. Neonatal line thickness was measured from thin sections and evaluated against maternal and neonatal factors using statistical analyses, controlling for tooth type and birth number. RESULTS AND CONCLUSIONS: The only maternal factor of a statistically significant effect on NNL thickness was alcohol consumption. Children of mothers who drank occasionally during pregnancy had a thicker NNL when compared to children of mothers who abstained. These results suggest that maternal lifestyle factors influence NNL formation possibly due to physiological changes that disrupt calcium homeostasis during enamel deposition. We highlight large intra-specific variation in human NNL expression. The potential of dental sampling in identifying children with prenatal exposure to alcohol is suggested.

First insights into the feeding habits of the Critically Endangered black snub-nosed monkey, Rhinopithecus strykeri (Colobinae, Primates).

Since its initial discovery in 2010 in the Gaoligong Mountains on the Sino-Myanmar border, there remains no direct information on the feeding habits of the black snub-nosed monkey (Rhinopithecus strykeri). This species is on the verge of extinction, with an estimated remaining population of < 400 individuals. Due to difficulties in following these monkeys across steep mountainous terrain, during 203 observation days (September 2015-January 2017) we recorded 80 h of behavioral records of a wild population (Luoma group). Our preliminary results identified 14 plant species and four lichen species consumed by the monkeys. In addition, we provided the only two captive individuals of this species with a cafeteria diet composed of > 600 wild-collected plant species that were gathered from known R. strykeri habitats to determine which plant species and food items were considered palatable. Our results indicate that the captive monkeys freely consumed young and mature leaves, fruits/seeds, buds, flowers, twigs, and bark from 170 different species of trees, bushes, and herbs representing 76 genera and 41 plant families, as well as 15 species of lichen. All foods consumed by the wild monkeys were also consumed by the captive individuals. Food plants consumed by R. strykeri were found principally in intact subtropical evergreen broadleaf forests and hemlock-broadleaf mixed forests at an altitude of 2200-3000 m. Strict enforcement of habitat protection and access to resources across this elevation zone appear to be essential for the conservation and survivorship of this critically endangered primate.

Nutritional composition of the diet of the northern yellow-cheeked crested gibbon (Nomascus annamensis) in northeastern Cambodia.

This study measured the nutritional composition of foods consumed by the northern yellow-cheeked crested gibbon (Nomascus annamensis) in northeastern Cambodia. One group of N. annamensis was studied, and focal animal sampling was used to observe their feeding behavior. The study was conducted for 4 months (January-April 2015) in the dry season and 69 foods were collected for nutritional analyses. N. annamensis fed on 37 plant species, but only seven species made up more than 80% of feeding time. N. annamensis spent the majority of their time feeding on fruit (60.36%), followed by young leaves (22.60%), flowers (13.74%), and mature leaves (3.30%). Fruit had the highest concentrations of total non-structural carbohydrates, while young leaves had the highest concentration of crude protein compared to other food items. All food items had similar concentrations of lipids, except young leaves, which had lower levels than fruit and flowers. All plant parts consumed by N. annamensis had similar amounts of neutral detergent fiber, acid detergent fiber, and acid detergent lignin. Thirty-two percent of all food items contained condensed tannins, and they had a similar level of it. All foods also had similar energy contents. This study adds to our knowledge of the feeding ecology of N. annamensis by providing baseline data on the make-up of the foods they eat and may contribute to captive feeding programs, ultimately assisting the conservation of this species.

The role of minerals in food selection in a black howler monkey (Alouatta pigra) population in Belize following a major hurricane.

As plants may contain low levels of some minerals including sodium, copper, and phosphorous, herbivores may become deficient in these nutrients. In 2001, Hurricane Iris hit the Monkey River Forest in Belize causing substantial damage to the food supply of the black howler monkey population (Alouatta pigra) living there. This included an 18-month absence in fruit production and a complete loss of figs that are high in calcium. In this article, we describe the post-hurricane diet of this monkey population and compare the mineral content of food items to each other and to recommendations for non-human primates [NRC 2003]. We also investigate food selection in relation to potentially limiting minerals. Behavioral data from four groups of howlers (2002-2006) and samples of all ingested food items were collected and a sample of 99 plant from 18 food species was analyzed for mineral content. Unexpectedly, the post-hurricane diet contained more mature leaves than new leaves despite the availability of new leaves. Leaves contained higher amounts of minerals than reproductive parts and with the exception of Cecropia peltata stems, plant parts were low in sodium. Cecropia peltata is a pioneer species that grows following habitat disturbance thus the ingestion of these stems may be a potential mechanism to avoid sodium deficiency in this damaged forest. Calcium and zinc were found above recommended values in most food items; however, both positively predicted food selection, which may reflect a difference between their abundance and their bioavailability. However, as mature leaves contained more calcium than other plant parts, their high post-hurricane consumption may also be a response to the absence of figs and the need to find an alternate calcium source. This study highlights how habitat disturbance may affect mineral abundance and the dietary choices of primates.

Parasites, primates, and ant-plants: clues to the life cycle of Controrchis spp. in black howler monkeys (Alouatta pigra) in southern Belize.

The purpose of this study was to investigate the prevalence, intensity, and possible transmission routes of the trematode, Controrchis spp. (Dicrocoeliidae), in a population of black howler monkeys (Alouatta pigra) near Monkey River, Belize. Alouatta pigra are arboreal primates that are typically folivorous and frugivorous. Controrchis is a dicrocoeliid trematode and, as such, should require a gastropod and an ant (Formicidae) intermediate host for transmission. From January to July 2005 and February 2006 to June 2007, we collected fecal samples and focal animal data from 18 individual primates in four social groups. Feces were stored in either 10% buffered formalin or 95% ethanol and examined using a double-centrifugation sugar-flotation technique. The prevalence of Controrchis spp. was 89%, and the mean intensity was 2.29 eggs per gram (epg), with a range of 1.00-6.57 epg. A general linear mixed model to examine the effect of sex, rainfall, and time spent feeding on various plant species, while controlling for individual and group identity, revealed that both group and the amount of time spent feeding on trumpet trees (Cecropia peltata) by individuals predicted the prevalence and intensity of Controrchis spp. infestation. Cecropia peltata has a mutualistic relationship with Azteca spp. ants and constitutes an important food source for A. pigra. Our findings provide strong, circumstantial evidence that A. pigra are infected with Controrchis spp. through the ingestion of metacercariae in Azteca spp. when feeding on C. peltata. Because C. peltata is a pioneer tree species and typically occurs in disturbed forests, results from this study suggest an important link between habitat disturbance and parasitism in a wild mammal.

Sources of variation in fecal cortisol levels in howler monkeys in Belize.

High cortisol levels are known to cause low fecundity and increased mortality; thus, the prospect of using cortisol as a measure of population health is an exciting one. However, because so many factors can interact to influence cortisol release, it can be difficult to interpret what exactly is creating changes to cortisol levels. This study investigates variation in fecal cortisol levels in a population of black howlers (Alouatta pigra) from 350 fecal samples collected from 33 individuals in more than 4 years. A general linear mixed model revealed that cortisol varied significantly with fruit availability and contact with tourists. When fruit availability was low, cortisol increased, likely because when fruit availability is low monkeys eat less fruit, thus obtaining less sugar. This result may simply reflect cortisol's metabolic function of mobilizing glucose. It also indicates that these monkeys may be experiencing periods of food stress throughout the year, which was earlier thought to be minimal for a primarily folivorous species. Presence of tourists was the only other factor found to lead to high cortisol; with exposure to tourists increasing stress levels. These results highlight the importance of understanding how physiological factors can influence cortisol, making it easier to interpret results and determine the external social or ecological stressors that may increase cortisol.