Edge effects and social behavior in three platyrrhines.

Social behavior is a key adaptation for group-living primates. It is important to assess changes to social behavior in human-impacted landscape zones to better understand the impact of anthropogenic disturbance on primate species. We investigated social behavior rate and type in three species of platyrrhines across 100 m anthropogenic edge and interior zones of a fragmented forest in Costa Rica, La Suerte Biological Research Station (LSBRS). Following results from other sites, we predicted that spider monkeys (Ateles geoffroyi), capuchin monkeys (Cebus imitator) and howler monkeys (Alouatta palliata) would show lower rates and fewer types of social behavior in forest edge compared to interior. We collected 1341 h of instantaneous focal data from 2017 to 2023 across the three monkey species. We found mixed support for our predictions, with spider and capuchin monkeys modifying some but not all aspects of social behavior across forest zones at LSBRS. Spider monkeys had lower rates of social behavior and capuchin monkeys performed different types of social behaviors in forest edge compared to interior at LSBRS. In contrast, howler monkeys did not modify social behavior. Two out of three platyrrhine species altered their social behavior when in anthropogenic edges, indicating behavioral adjustment when in human-altered habitat areas at LSBRS.

Nighttime behavior and the length of social relationships in male Asian elephants.

To evaluate elephant welfare, it is important to understand their use of time both during day and night. The length of social relationships can influence how much time they spend in different activities. We assessed daytime and nighttime activity budgets of male Asian elephants at Denver Zoo and examined how length of relationships influenced nighttime behavior. Using scan sampling we investigated activity budget and proximity to a conspecific, and used General Estimating Equations to compare them across day and night and across new and established dyads at night. During daytime, elephants spent significantly more time exhibiting affiliative and agonistic behaviors, and in proximity to a conspecific, and less time resting, compared to night. Overnight, the odds of resting were significantly lower in new social dyads compared to established dyads, and new dyads spent more time exhibiting agonistic behavior and in proximity to a conspecific compared to established dyads. Our study suggests that male elephants at Denver Zoo have developed strong relationships and highlights the importance of systematically observing elephants overnight so that managers make decisions that improve animal welfare.

Social Dynamics of a Newly Integrated Bachelor Group of Asian Elephants (Elephas maximus): Welfare implications.

Male associations are a typical component of elephant society, allowing bulls to practice appropriate social behavior. To improve zoo elephant welfare, it is important to provide bulls with social opportunities. In fall 2018, Denver Zoo added two bull Asian elephants to its existing all-male group of three bulls, offering the opportunity to conduct a systematic behavioral study of the integration of the new bulls into the resident group. We recorded aggressive and affiliative behaviors before, during, and after the introduction of the new males. The proportion of aggressive behavior was significantly higher during the five-month introduction period compared to before their introduction. By the end of the study period, the elephants engaged in significantly more affiliative behavior and less aggressive behavior than during the introduction period, suggesting they had formed a new stable social dynamic. These results suggest group compatibility and positive elephant welfare resulting from housing male elephants together and can be used to inform management plans for bull elephants that prioritize their welfare.

Student research collaboration as conservation education: A case study from the primate field school at Maderas Rainforest Conservancy.

Maderas Rainforest Conservancy (MRC) is a conservation-focused non-profit organization that is devoted to protecting the tropical forests they manage in Costa Rica and Nicaragua and to providing conservation education for international university students through biological field schools. The MRC Primate Behavior and Ecology course is their most frequent course offering and is aimed at developing students to be independent field researchers. This course involves classroom lectures, training in primate identification and field methods, and the execution of independent research projects that students design, collect data for, and write up as scientific papers. Student development as conservationists is facilitated through the research experience provided by this field course as well as through co- and extracurricular research opportunities available to students at the sites that MRC manages: La Suerte Biological Research Station in Costa Rica, and Ometepe Biological Research Station in Nicaragua. In tandem with their participation in the MRC primate field course, we (Laura M. Bolt and Amy L. Schreier) consistently offer students research opportunities in our ongoing project examining the impact of forest fragmentation on primate behavioral ecology. MRC student course evaluations indicate that this co- and extracurricular research participation substantially contributes to student academic development and conservation awareness. Student research collaboration, therefore, greatly benefits students as well as furthers MRC's conservation goals as a non-profit organization. In future MRC primate field school sessions, we will continue to offer research collaboration opportunities to students and will also endeavor to improve conservation education at MRC by involving more local community members in MRC's academic programs.

Behavioral responses to riparian and anthropogenic edge effects in mantled howler monkeys (Alouatta palliata) in a disturbed riverine forest.

Fragmented forests contain natural edges, including riparian zones, and anthropogenic edges. Edges generally have lower plant density and fewer large trees than forest interior. Riparian edges, however, contain gap-specialist trees yielding leaves with high protein content, providing primates with important resources. We examined mantled howler monkeys' behavioral responses to riparian and anthropogenic edges at La Suerte Biological Research Station (LSBRS), Costa Rica. We predicted the monkeys would spend more time resting and feeding and less time traveling, and be less spatially cohesive, in both anthropogenic and riparian edges compared to forest interior due to lower resource abundance in edges, and in anthropogenic compared to riparian edge due to higher leaf quality in riparian zones. From 2017 to 2020, we collected data across forest zones on activity and spatial cohesion patterns via focal sampling, recording data every 2 min. Howler monkeys were significantly more likely to rest and significantly less likely to travel in both anthropogenic and riparian edges compared to forest interior; however, there were no differences between these edge types. There were significantly more monkeys within a 5-m radius of focal subjects in both anthropogenic and riparian edges compared to forest interior, but no differences between these edge types. While prior research found no differences across zones when only anthropogenic edge and forest interior were compared, results of this study demonstrate that howler monkeys at LSBRS modify their activity patterns in anthropogenic and riparian edge zones compared to forest interior, highlighting the importance of focusing on both natural and anthropogenic edge zones to fully understand primates' behavioral responses in fragmented landscapes.

The effects of Zoo Lights on animal welfare: A case study of great Indian hornbills at Denver Zoo.

Popular evening events, such as Zoo Lights, increase the exposure of animals in managed care to stressors such as artificial light and noise, which may alter their behavior and negatively affect animal well-being. The pair of great Indian hornbills (Buceros bicornis) at Denver Zoo provided an opportunity to study the impacts of these stressors because their exhibit was open every evening during Zoo Lights 2017. We expected the hornbills to display increased aggressive behaviors during Zoo Lights due to more exposure to stressors compared to the periods before and after the holiday event. Alternatively, if behavioral changes were associated with hornbills' breeding season which runs from December-March, we expected the hornbills to engage in more affiliative behaviors, and to increase conspecific and nest proximity, during and after Zoo Lights compared to before it due to the onset and progression of the breeding season. The hornbills did not engage in significantly more aggressive behavior during Zoo Lights than before or after it. By contrast, the hornbills engaged in significantly more affiliative behaviors and increased conspecific proximity during and after Zoo Lights compared to before the event. These results are consistent with the timing of the hornbills' breeding season and not with the increased exposure to stressors during Zoo Lights. This case study provides an early step in assessing the impact of Zoo Lights on animals whose exhibits are part of these holiday events. Studies like this will help inform best practices for Zoo Lights events such that they are positive experiences for the zoo, visitors, and animals.

Maderas Rainforest Conservancy: A One Health approach to conservation.

Maderas Rainforest Conservancy (MRC) was incorporated as a conservation nonprofit organization in 2008, and manages two sites where biological field courses have been offered since the 1990s: La Suerte Biological Research Station in Costa Rica, and Ometepe Biological Research Station in Nicaragua. MRC employs a One Health approach to conservation education, and can serve as a model for other biological field sites. The Nicaraguan Molina family, who owns the sites, partnered with primatologist Paul Garber in 1994 to develop a primate field course aimed at introducing university students to field research. Through using their land to further conservation education and research, the Molina family has preserved the forest and engaged the local communities near their sites. Eight graduate theses and 46 refereed publications have been completed since 2010 based on research undertaken at MRC sites. While primate field courses have been offered at least once annually since 1994 and remain popular, a range of other ecological courses are now additionally offered. MRC operates from a One Health perspective, engaging in forest restoration and ecological monitoring projects, and has gradually expanded community outreach initiatives. MRC now conducts regular medical and veterinary missions in the communities surrounding the research stations which provide health care to local people and limit the population growth of domestic animals, thereby increasing the survival of wild animals. MRC is also active in ESL-teaching and conservation education, and funds Proyecto Jade, which empowers local women to make and sell organic jewelry. Through these programs, MRC works to help the local communities live more sustainably with the environment around them. MRC's support of research, commitment to education, medical and veterinary missions, and outreach initiatives to the local community all work together for the well-being of both the people and the environment, thus exemplifying the One Health perspective.

Anthropogenic edges impact howler monkey (Alouatta palliata) feeding behaviour in a Costa Rican rainforest.

Anthropogenic forest fragmentation impacts many aspects of animal behaviour, including feeding ecology. With forests increasingly fragmented in tropical regions due to human development, the proportion of forest edge (≤ 100 m from clear-cut regions) is higher relative to forest interior. Forest edges differ in vegetation from interior, making it important to better understand how anthropogenic edges impact the feeding behaviour of primates such as mantled howler monkeys (Alouatta palliata). We predicted that howler monkeys would feed on higher-quality plant resources, from a larger number of tree families, and from larger trees in forest interior compared to anthropogenic forest edge. We surveyed howler monkey feeding behaviour across forest zones in a fragmented rainforest in Costa Rica, La Suerte Biological Research Station. We observed individual monkeys for 30-minute periods, collecting data on their feeding behaviour and tree use at 2-minute intervals. We measured feeding trees and recorded the plant parts and taxonomy of resources consumed. Monkeys consumed more leaves and fewer stems and fed from a smaller number of tree families in the forest interior, while they consumed fewer leaves and more stems and fed from a larger number of tree families in the forest edge. Monkeys also fed from larger, taller trees in the forest interior than the edge. The differences in howler monkey feeding behaviour between forest zones attest to the impact of human disturbance on howler monkey feeding ecology.

Lone males: Solitary and group-living male howler monkey (Alouatta palliata) behavioral ecology in a Costa Rican rainforest.

OBJECTIVES: Many group-living primate species have evolved the capacity for some individuals to live alone for part of their lives, but this solitary life stage has rarely been the subject of focused research. The mantled howler monkey (Alouatta palliata) is a social primate species with bisexual dispersal that lives in mixed-sex groups with low male-to-female sex ratios. Consequently, males often spend a long period of their lives as solitary individuals. This study compares the tree use, feeding, and long-distance vocalization behavior of solitary and group-living mantled howler monkey males living within a fragmented rainforest in Costa Rica, La Suerte Biological Research Station. Based on differences in competitive ability between solitary and group-living males, we predicted that lone males would be found in significantly smaller feeding and resting trees, consume more low-quality foods, and produce shorter howling bouts made at lower rates than group-living males. MATERIALS AND METHODS: We collected data on tree use and feeding during 30-min focal samples on male focal animals, recording data at 2-min intervals. We measured the trees in which the monkeys fed and rested for two or more intervals, and recorded the plant parts consumed. We recorded howling behavior using all-occurrences sampling. RESULTS: Lone males used significantly smaller feeding and resting trees, consumed more low-quality foods, and howled at lower rates but had longer howling bouts triggered by anthropogenic noise more than group-living males. DISCUSSION: Our results demonstrate that lone males differ in their behavioral ecology compared to group-living males, thus improving understanding of the solitary male life stage in primates.

Mantled Howler Monkeys (Alouatta palliata) in a Costa Rican Forest Fragment Do Not Modify Activity Budgets or Spatial Cohesion in Response to Anthropogenic Edges.

Forest fragmentation increases forest edge relative to forest interior, with lower vegetation quality common for primates in edge zones. Because most primates live in human-modified tropical forests within 1 km of their edges, it is critical to understand how primates cope with edge effects. Few studies have investigated how primates inhabiting a fragment alter their behaviour across forest edge and interior zones. Here we investigate how anthropogenic edges affect the activity and spatial cohesion of mantled howler monkeys (Alouatta palliata) at the La Suerte Biological Research Station (LSBRS), a Costa Rican forest fragment. We predicted the monkeys would spend greater proportions of their activity budget feeding and resting and a lower proportion travelling in edge compared to forest interior to compensate for lower resource availability in the edge. We also predicted that spatial cohesion would be lower in the edge to mitigate feeding competition. We collected data on activity and spatial cohesion (nearest neighbour distance; number of individuals within 5 m) in forest edge and interior zones via instantaneous sampling of focal animals. Contrary to predictions, the monkeys spent equal proportions of time feeding, resting and travelling in forest edge and interior. Similarly, there were no biologically meaningful differences in the number of individuals or the distance between nearest neighbours in the edge (1.0 individuals; 1.56 m) versus the interior (0.8 individuals; 1.73 m). Our results indicate that A. palliata at LSBRS do not adjust their activity or spatial cohesion patterns in response to anthropogenic edge effects, suggesting that the monkeys here exhibit less behavioural flexibility than A. palliata at some other sites. To develop effective primate conservation plans, it is therefore crucial to study primate species' responses to fragmentation across their geographic range.

Meat eating in wild hamadryas baboons: Opportunistic trade-offs between insects and vertebrates.

The consumption of meat may provide herbivorous animals with important nutrients that are scarce in their plant-based diet. Seasonal variation in plant food availability has been suggested to motivate dietary flexibility in a range of species and thus primates may seek more prey when key plant resources are unavailable. Alternatively, prey encounter rate may drive meat eating. Here we investigate patterns of meat eating in hamadryas baboons (Papio hamadryas) at Filoha, Awash National Park, Ethiopia. The Filoha baboons rely largely on doum palm fruit (Hyphaene thebaica), which are available most months of the year, and the young leaves of Acacia senegal, which are more abundant during the wet season. We hypothesized that the baboons would consume more meat when H. thebaica and A. senegal were less available, which we tested by comparing meat eating and consumption of these plant food species from March 2005 through February 2006. Our results reveal a high rate of vertebrate meat eating at Filoha (0.028/hour of observation) compared with other hamadryas sites. We found no relationship, however, between meat eating (either insect or vertebrate) and either rainfall or consumption of H. thebaica or A. senegal, indicating that availability of preferred plant resources does not drive meat consumption. Vertebrate consumption and time spent feeding were significantly negatively associated; there was no relationship, however, between the consumption of animal matter and either home range size or daily path length. Vertebrate and insect consumption alternated throughout the year such that the baboons maintained a small amount of animal matter in their diet year-round. Our results suggest that the baboons do not often actively seek animal matter, but consume it opportunistically, with the presence of locust and dragonfly swarms driving insect consumption, and both prey availability and the availability of feeding time shaping vertebrate predation.

The influence of anthropogenic edge effects on primate populations and their habitat in a fragmented rainforest in Costa Rica.

When a forest is fragmented, this increases the amount of forest edge relative to the interior. Edge effects can lead to loss of animal and plant species and decreased plant biomass near forest edges. We examined the influence of an anthropogenic forest edge comprising cattle pasture, coconut plantations, and human settlement on the mantled howler (Alouatta palliata), white-faced capuchin (Cebus capucinus), Central American spider monkey (Ateles geoffroyi), and plant populations at La Suerte Biological Research Station (LSBRS), Costa Rica. We predicted that there would be lower monkey encounter rate, mean tree species richness, and diameter at breast height (DBH) in forest edge versus interior, and that monkeys would show species-specific responses to edge based on diet, body size, and canopy height preferences. Specifically, we predicted that howler monkeys would show positive or neutral edge effects due to their flexible folivorous diet, large body size, and preference for high canopy, capuchins would show positive edge effects due to their diverse diet, small body size, and preference for low to middle canopy, and spider monkeys would show negative edge effects due their reliance on ripe fruit, large body size, and preference for high upper canopy. We conducted population and vegetation surveys along edge and interior transects at LSBRS. Contrary to predictions, total monkey encounter rate did not vary between the forest edge and forest interior. Furthermore, all three species showed neutral edge effects with no significant differences in encounter rate between forest edge and interior. Interior transects had significantly higher mean tree species richness than edge transects, and interior trees had greater DBH than edge trees, although this difference was not significant. These results suggest that forest edges negatively impact plant populations at La Suerte but that the monkeys are able to withstand these differences in vegetation.

Testing parallel laser image scaling for remotely measuring body dimensions on mantled howling monkeys (Alouatta palliata).

Body size is a fundamental variable for many studies in primate biology. However, obtaining body dimensions of wild primates through live capture is difficult and costly, so developing an alternative inexpensive and non-invasive method is crucial. Parallel laser image scaling for remotely measuring body size has been used with some success in marine and terrestrial animals, but only one arboreal primate. We further tested the efficacy of this method on the arboreal mantled howling monkey (Alouatta palliata) in La Pacifica, Costa Rica. We calculated interobserver error, as well as the method's repeatability when measuring the same animal on different occasions. We also compared measurements obtained physically through live capture with measurements obtained remotely using parallel laser image scaling. Our results show that the different types of error for the remote technique are minimal and comparable with the error rates observed in physical methods, with the exception of some dimensions that vary depending on the animals' posture. We conclude that parallel laser image scaling can be used to remotely obtain body dimensions if careful consideration is given to factors such as species-specific morphology and postural habits.

Recurrent patterning in the daily foraging routes of hamadryas baboons (Papio hamadryas): spatial memory in large-scale versus small-scale space.

The benefits of spatial memory for foraging animals can be assessed on two distinct spatial scales: small-scale space (travel within patches) and large-scale space (travel between patches). While the patches themselves may be distributed at low density, within patches resources are likely densely distributed. We propose, therefore, that spatial memory for recalling the particular locations of previously visited feeding sites will be more advantageous during between-patch movement, where it may reduce the distances traveled by animals that possess this ability compared to those that must rely on random search. We address this hypothesis by employing descriptive statistics and spectral analyses to characterize the daily foraging routes of a band of wild hamadryas baboons in Filoha, Ethiopia. The baboons slept on two main cliffs--the Filoha cliff and the Wasaro cliff--and daily travel began and ended on a cliff; thus four daily travel routes exist: Filoha-Filoha, Filoha-Wasaro, Wasaro-Wasaro, Wasaro-Filoha. We use newly developed partial sum methods and distribution-fitting analyses to distinguish periods of area-restricted search from more extensive movements. The results indicate a single peak in travel activity in the Filoha-Filoha and Wasaro-Filoha routes, three peaks of travel activity in the Filoha-Wasaro routes, and two peaks in the Wasaro-Wasaro routes; and are consistent with on-the-ground observations of foraging and ranging behavior of the baboons. In each of the four daily travel routes the "tipping points" identified by the partial sum analyses indicate transitions between travel in small- versus large-scale space. The correspondence between the quantitative analyses and the field observations suggest great utility for using these types of analyses to examine primate travel patterns and especially in distinguishing between movement in small versus large-scale space. Only the distribution-fitting analyses are inconsistent with the field observations, which may be due to the scale at which these analyses were conducted.

Ecology and sociality in a multilevel society: ecological determinants of spatial cohesion in hamadryas baboons.

The multilevel society of hamadryas baboons, consisting of troops, bands, clans, and one-male units (OMUs), is commonly perceived to be an effective means of adapting to variable food availability while allowing spatial cohesion in response to predator pressure. The relationship between these variables, however, has never been tested quantitatively. The Filoha site in Awash National Park, Ethiopia is ideally suited to such an investigation as it contains nutrient-dense palm forests in addition to the Acacia scrublands typical of hamadryas distribution elsewhere, allowing comparisons of spatial cohesion across habitat types. Here, we use observations over a 1-year period to examine the relationship between resource availability, perceived predator pressure, and spatial cohesion in a band of wild hamadryas baboons at Filoha. Our results demonstrate that the band was more likely to break into OMUs when foraging in habitats with lower food availability, and that the band fissioned into independent clans more often when preferred resources were not available. Furthermore, the baboons remained in larger aggregations for longer periods of time (i.e., prior to embarking on their daily foraging route) on mornings after predators were heard in the vicinity, and increased cohesion in response to encounters with people who may have been perceived as predators. These results support the notion that hamadryas baboons change their social groupings in response to both food availability and predation risk and that the ability of hamadryas bands to cleave and coalesce in response to changes in these factors underlies the evolution of the hamadryas modular social structure.

Feeding ecology, food availability and ranging patterns of wild hamadryas baboons at Filoha.

Most hamadryas baboons rely on Acacia species for subsistence in their semidesert habitats. Unlike other hamadryas sites, palm forests at Filoha in Awash National Park, Ethiopia, provide the baboons with a preferred food resource close to a commonly used sleeping site. The baboons are expected to feed on doum palm trees when fruit is available, and this resource use should play a role in ranging patterns. This paper describes the feeding ecology, food availability and ranging patterns of a band of wild hamadryas baboons at Filoha from March 2005 to February 2006. Data on feeding and ranging behavior derive from band scans during all-day follows of baboons, and data on food availability derive from monthly phenological monitoring of frequently consumed food species. The baboons fed predominantly on palms when fruit was available, and preferred the flowers of Acacia senegal to its leaves. There was no relationship between daily path length and the proportion of palm fruit in the baboons' diet, but changes in the availability of fruit across the Filoha region appear to mirror the baboons' shifting use of its home range. The large band sizes at Filoha may obscure the effects doum palm fruit might have on ranging patterns.

The fourth level of social structure in a multi-level society: ecological and social functions of clans in hamadryas baboons.

Hamadryas baboons are known for their complex, multi-level social structure consisting of troops, bands, and one-male units (OMUs) [Kummer, 1968. Social organization of hamadryas baboons. Chicago: The University of Chicago Press. 189p]. Abegglen [1984. On socialization in hamadryas baboons: a field study. Lewisburg, PA: Bucknell University Press. 207p.] observed a fourth level of social structure comprising several OMUs that rested near one another on sleeping cliffs, traveled most closely together during daily foraging, and sometimes traveled as subgroups independently from the rest of the band. Abegglen called these associations "clans" and suggested that they consisted of related males. Here we confirm the existence of clans in a second wild hamadryas population, a band of about 200 baboons at the Filoha site in lowland Ethiopia. During all-day follows from December 1997 through September 1998 and March 2005 through February 2006, data were collected on activity patterns, social interactions, nearest neighbors, band fissions, and takeovers. Association indices were computed for each dyad of leader males, and results of cluster analyses indicated that in each of the two observation periods this band comprised two large clans ranging in size from 7 to 13 OMUs. All band fissions occurred along clan lines, and most takeovers involved the transfer of females within the same clan. Our results support the notion that clans provide an additional level of flexibility to deal with the sparse distribution of resources in hamadryas habitats. The large clan sizes at Filoha may simply be the largest size that the band can split into and still obtain enough food during periods of food scarcity. Our results also suggest that both male and female relationships play a role in the social cohesion of clans and that males exchange females within clans but not between them.