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.

Dominance style is a key predictor of vocal use and evolution across nonhuman primates.

Animal communication has long been thought to be subject to pressures and constraints associated with social relationships. However, our understanding of how the nature and quality of social relationships relates to the use and evolution of communication is limited by a lack of directly comparable methods across multiple levels of analysis. Here, we analysed observational data from 111 wild groups belonging to 26 non-human primate species, to test how vocal communication relates to dominance style (the strictness with which a dominance hierarchy is enforced, ranging from 'despotic' to 'tolerant'). At the individual-level, we found that dominant individuals who were more tolerant vocalized at a higher rate than their despotic counterparts. This indicates that tolerance within a relationship may place pressure on the dominant partner to communicate more during social interactions. At the species-level, however, despotic species exhibited a larger repertoire of hierarchy-related vocalizations than their tolerant counterparts. Findings suggest primate signals are used and evolve in tandem with the nature of interactions that characterize individuals' social relationships.

Seasonal and sex differences in the fission-fusion dynamics of spider monkeys (Ateles geoffroyi yucatanensis) in Belize.

Spider monkeys (Ateles sp.) are characterized by high fission-fusion dynamics, meaning their social grouping pattern is fluid and consists of subgroups that vary in size, composition, and spatial cohesion over time. In this study, we quantify the fission-fusion dynamics of a group of spider monkeys at Runaway Creek Nature Reserve in Belize by measuring subgroup size, spatial cohesion, and stability using data spanning 5 years. We then test whether variation in these three subgroup measures differ according to season, subgroup sex composition, and the reproductive status of female subgroup members. Our results show that subgroups were larger in size and less stable in membership during the wet season compared to the dry season. All-female subgroups were less spatially cohesive but more stable in membership than all-male subgroups. Finally, we report that subgroups with one or more non-lactating females (i.e., without nursing young) were smaller on average than subgroups containing lactating females with nursing young. These data contribute to a growing body of research documenting the ecological and social dimensions along which grouping patterns might vary.

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.

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.

Group size in folivorous primates: ecological constraints and the possible influence of social factors.

The ecological-constraints model assumes that food items occur in depletable patches and proposes that an increase in group size leads to increased day range due to more rapid patch depletion. Smaller groups become advantageous when an increase in travel costs is not repaid by an increase in energy gained or some other fitness advantage. On the other hand, we also know that group size can be influenced by social factors. Here we contrast the diet and group size of red colobus (Procolobus badius) and black-and-white colobus (Colobus guereza) in Kibale National Park, Uganda to consider how ecological and social factors are affecting their group sizes. Subsequently, we examine whether the insights gained from this detailed comparison can provide an understanding of why the social organization and group size of mantled howlers (Alouatta palliata) and black howlers (A. pigra) differ. Two groups of red colobus and two groups of black-and-white colobus were studied over 10 months. Red colobus groups were larger (48 and 24) than black-and-white colobus groups (9 and 6). The two groups of red colobus overlap home ranges with the two groups of black-and-white colobus; 75% and 95% of their home ranges were within red colobus's home range. There was a great deal of similarity in the plant parts eaten by the two species and both species fed primarily on young leaves (red colobus 70%, black-and-white colobus 76%). In terms of the actual species consumed, again there was a great deal of similarity between species. The average dietary overlap among months for the two neighboring groups of red colobus was 37.3%, while the dietary overlap between the red colobus and the black-and-white colobus group that had its home range almost entirely within the home range of the red colobus groups averaged 43.2% among months. If ecological conditions were responsible for the difference in group size between the two colobine species, one would expect the density of food trees to be lower in the home ranges of the black-and-white colobus monkeys, since they have the smaller group size. We found the opposite to be true. Both black-and-white colobus groups had more food trees and the cumulative size of those trees was greater than those in the red colobus's home ranges. We quantify how these differences parallel differences in mantled and black howlers. The average group size for mantled howlers was 12.9 individuals, and for black howlers it was 5.3 individuals. We explore possible social constraints, such as infanticide, that prevent black-and-white colobus and black howlers from living in large groups.

Observed case of infanticide committed by a resident male central American black howler monkey (Alouatta pigra).

Although infanticide has been witnessed in other species of howler monkey, and has been inferred for Alouatta pigra, an observed case of infanticide has not previously been recorded for this species. Here we describe the killing of a 2-week-old infant by the resident male of a small social group in southern Belize. The infanticide was witnessed as part of an intensive observational study that began in January 2003. The male was known to have resided in the group for at least 4 months, but it is not known whether he was the father of the infant. The literature proposes three main explanations for infanticide: two adaptive hypotheses (sexual selection and resource competition), and one nonadaptive hypothesis (social pathology). Individual cases of infanticide such as this one are important for comparative purposes, but when examined on their own they are difficult to interpret in relation to established theoretical frameworks. The data presented here show some consistency with the sexual-selection and resource-competition hypotheses, but the lack of critical information (i.e., as to paternity) makes it impossible to draw firm conclusions.

Diet and activity in black howler monkeys ( Alouatta pigra) in southern Belize: does degree of frugivory influence activity level?

This study reports on the diet and activity budgets of Central American black howling monkeys ( Alouatta pigra) at Monkey River, Belize. This is a previously unstudied population, close to the southern boundary of the species range, and it provides comparative data on A. pigra from a new study site. Both diet and activity are within the ranges reported for other A.pigra sites and for mantled howlers ( A. palliata). No age-sex differences could be discerned in either diet or activity, though monthly variation was apparent. The monkeys switch from consuming leaves 86% of the time in January to March to consuming 67% fruit in April to July. This difference was statistically significant, and provided the opportunity to compare activity levels of the monkeys over two dietary periods, one characterized primarily by folivory, the other by frugivory. Howlers are often seen as a relatively inactive species, something that is associated with a low quality, folivorous diet. However, A. pigra have been described as being as frugivorous as possible and as folivorous as necessary. Yet, despite the opportunistic consumption of large quantities of high-energy foods, A. pigra has been observed as conforming to the howler lifestyle, resting as much as 80% of the day. The data in this paper support both of these reports. Black howlers at Monkey River Belize are typically inactive, maintaining high levels of inactivity even during months characterized by frugivory, suggesting that diet is more flexible and varied than is behavior and calling into question the assumption that howler inactivity is due to the digestion of large quantities of leaves.