Alison M. Behie

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 cortisols 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. Am. J. Primatol. 72:600–606, 2010.

Population Reduction and Social Disorganization in Alouatta pigra Following a Hurricane

The opportunity to study the effects of a powerful hurricane on monkey populations, diet, and behavior via pre- and post-hurricane data was presented when hurricane Iris virtually destroyed the forest along Monkey River in southern Belize on October 8, 2001, including a 52-ha area where black howlers have been subjects since 1999. Before the hurricane, 8 social groups, averaging 6.37 members, had been stable in both group composition and range for ≥q 2 years. The hurricane, which levelled much of the forest, resulted in the complete loss of the forest canopy. The trees that remained standing lost most or all branches and were 100% defoliated. The monkey population in the study area was reduced by 42% and survivers experienced a period of extended social disorganization involving transient individuals, high numbers of solitary monkeys, and small fragmentary social groups. The period of disorganization lasted 12 weeks, after which the number of solitaries reduced and stability of the large groups increased. Within the study area, 5 social groups have been more or less stable since ca. week 15; however, home ranges had yet to stabilize at week 35. The social and ranging effects are similar to what has been described for translocated primates. Post-hurricane diet was limited to fruit and leaves remaining in the deadfall for the first 2 weeks and to new leaves and leaf buds for many weeks after that. Normal fruit consumption in April and May was prevented by the failure of surviving trees to produce fruit. With the loss of forest canopy there has been increased use of low foliage and ground travel, and with the reduction in population density there has been a reduction in vocalization frequency.

The Short-Term Effects of a Hurricane on the Diet and Activity of Black Howlers (Alouatta pigra) in Monkey River, Belize

The diet and activity of a population of Alouatta pigra were compared before and immediately after a major hurricane to begin to explore how the monkeys cope with severe habitat destruction. Focal animal data were collected from January to April (dry season) for two seasons before (368 h) and one season after the storm (149 h) on a population of black howlers in Monkey River, Belize. During the first dry season after the storm, the monkeys changed their diet in direct accordance with the availability of food. The absence of fruit and flower production and the increase in new leaf availability forced the monkeys to adopt a completely folivorous diet. The activity budget of the monkeys also changed, and they spent more time inactive, which may be linked to the change in the distribution and type of food available. They also spent less time in social interactions, which may be due to the lower number of juveniles in the population or to the formation of new groups between unfamiliar individuals following the hurricane. The ability to live for long periods of time on leaves alone has allowed the remaining population to survive in the short term.

Food selection in the black howler monkey following habitat disturbance: implications for the importance of mature leaves

Primates commonly consume leaves that are high in protein but low in digestion-inhibiting fibre. Due to the fact that mature leaves do not meet these criteria, they are typically avoided and many leaf-eating primates select for leaves high in protein and low in fibre leading to the theory that food selection is based on protein maximization. However, feeding records for a population of black howler monkey ( Alouatta pigra ) in Monkey River, Belize, collected over a 5-y period, together with synchronous phenological data, indicate that this population does not meet the expectation and actually prefer mature leaves. This study aims to describe the nutritional composition of the food supply and investigate the possibility that, rather than to maximize protein ingestion, mature leaves are eaten to balance nutrient intake. Macronutrient analyses (moisture, lipids, protein, NDF, ADF and simple sugars) were conducted on a sample of 96 plant samples from 18 food species of this population of black howler. Results reported here show that mature leaves eaten by howlers in this forest contain sufficient protein to meet minimum metabolic requirements (range: 11.6–24%; mean: 16.4% ± 3.8%) and have significantly higher concentrations of simple sugars than young leaves (means of 7.2% ± 2.7% vs. 4.4% ± 2.3% respectively). Thus, it appears that mature leaf ingestion is likely serving to balance energy and protein intake. This result may be due to the disruptive effects of a hurricane in 2001 that resulted in a loss of 80% of the howler population, changed forest composition and may have affected plant chemistry. Despite this, the data reported here suggest that the accepted view that mature leaves are simply fallback foods for primates, eaten only in times of preferred food scarcity, may have to be revised.

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. Am. J. Primatol. 74:1054‐1063, 2012.

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.

Fruit as a Key Factor in Howler Monkey Population Density: Conservation Implications

Howler monkeys (Alouatta) are widely regarded as the most folivorous of the neotropical monkeys and the ability of howlers to live in a wide range of environments including highly disturbed forests has been linked to this ability. Generally categorized as energy minimizing folivores leaves comprise at least half and as much as 90 % of annual feeding time. All howler species also consume fruit; however, this amount is quite variable both within and between species, and across different months of the year. Seasonality in fruit consumption in Alouatta appears to be directly tied to its availability, suggesting that for all species fruit is a preferred food item. A study of population density and diet in A. pigra following a severe hurricane suggests that frugivory may be more crucial to population stability and growth than previously thought. This chapter considers the effects of this hurricane on A. pigra in relation to what is known about frugivory in the Mesoamerican clade of Alouatta (A. palliata and A. pigra), focusing on relationships between diet, population density, group size, behavior, ranging, and reproduction. These data suggest that frugivory is an important part of the feeding ecology of these species and that periods of prolonged fruit shortage may have significant impacts on their population dynamics and survival. Given that both natural and anthropogenic habitat disturbance generally have a negative effect on fruit production, this could have important conservation implications for this primate genus.

Interacting Roles of Diet, Cortisol Levels, and Parasites in Determining Population Density of Belizean Howler Monkeys in a Hurricane Damaged Forest Fragment

Primates in fragments, because of their increased vulnerability to stochasticity, are in double jeopardy with the expected increases in severe weather patterns due to global climate change. It is thus increasingly important to have a better understanding of how severe weather events affect primate populations, especially those in fragments. This study explores the interacting effects of diet, cortisol levels, and parasites on the density of a black howler (Alouatta pigra) population following a major hurricane. In October 2001, Hurricane Iris made landfall in Southern Belize resulting in substantial damage to the 96-km2 Monkey River watershed forest fragment and a loss of nearly 80 % of the population by 3 years after the storm. Late in 2004 the population stabilized and began to recover. From 2001 to 2006, demographic, behavioral, and dietary data along with fecal samples were collected from six monkey groups in an 86-ha study site in the Monkey River forest. Changes in population density over the 5-year period were explained primarily by fruit consumption both directly through inadequate fruit intake leading to energy malnutrition and indirectly through physiological stress (measured through fecal cortisol). Cortisol levels had a lesser direct effect on population density and were affected not only by low fruit consumption, but by multispecies parasite infections. This study highlights the importance of taking a multifactorial approach to understanding population density and shows how diet, stress, and parasites can have interacting effects in influencing primate population dynamics.

Seasonal Variation in the Activity and Dietary Budgets of Cat Ba Langurs (Trachypithecus poliocephalus)

Primate activity budgets are dictated by food availability and distribution; thus primates living in seasonal environments must adapt their behaviors to accommodate fluctuations in resources. Cat Ba langurs (Trachypithecus poliocephalus), a Critically Endangered Asian colobine and a member of the limestone langur group (francoisi superspecies group within genus Trachypithecus), live only in fragmented and disturbed habitats on Cat Ba Island, northeastern Vietnam. This study aimed to assess the behaviors and diet of Cat Ba langurs by group, age, sex, and season. We predicted they would have high rates of inactivity and foraging, low rates of social behaviors, with seasonal variation that reflects an energy-maximizing strategy. We conducted behavioral observations through scan sampling over an 11-month period and found that Cat Ba langurs spent a significant portion of their day inactive (57 %) followed by foraging (18 %), socializing (13 %), locomoting (10 %), and engaging in “other” behaviors (2 %). Their diet was made up primarily of leaves (83 %) followed by flowers (8 %), fruit (6 %), and stems (3 %). We found groups to differ in diet and activity, which is likely owing to differences in demographics and home range between groups. Seasonally, the animals ate more leaves and spent more time foraging in the dry season than the wet season, suggesting that they are energy maximizers. Cat Ba langurs have activity and dietary budgets similar to those of other limestone langurs, and respond to a presumed seasonal fluctuation in food availability similarly.

HIGHER PARENTAL PERCEPTIONS OF WEALTH ASSOCIATED WITH THE BIRTH OF MORE SONS IN AN AUSTRALIAN POPULATION

Many industrialized nations are currently experiencing a decline in average secondary sex ratio (SSR) resulting in fewer boys being born relative to girls. While many potential factors may explain the decline in the birth of males relative to females, it seems most studies support the idea that male offspring are produced less often when environmental conditions are poor owing to males being more susceptible to loss in harsh environments. This study investigates the maternal factors that are associated with the sex of offspring in a cohort of the Australian population. It found that greater parental perceptions of wealth were significantly associated with an increase in the number of sons produced. These results suggest that male offspring are born at increased numbers to women with higher available resources, which may reflect the fact that male offspring are more vulnerable in poor environments.