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.

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.

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.

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.

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.

Agonistic vocalization behaviour in the male ring-tailed lemur (Lemur catta).

Vocalizations are used by group-living animals as aggressive and submissive signals during agonistic interactions, and are also used to maintain dominance hierarchies in many species. For gregarious strepsirrhines with large vocal repertoires and differentiated dominance ranks like the ring-tailed lemur (Lemur catta), agonistic vocalization use is important to study to better understand their social adaptations.To determine whether ring-tailed lemur vocalizations such as the yip, cackle, twitter, chutter, and plosive bark were used as aggressive or submissive signals during agonism and uttered at different rates by males of differing dominance ranks and ages, 565 h of focal data were collected on 31 individual males aged ≥ 1 year from Beza Mahafaly Special Reserve, Madagascar. Yip, cackle, and twitter vocalizations were consistently used during agonistic submissive interactions with both males and females, chutter vocalizations were used during aggressive agonistic interactions with males and submissive agonistic interactions with males and females, and plosive bark vocalizations were used across behavioural contexts but not particularly during agonism. Males of all ages employed all vocalizations, and while low-ranking males uttered yip calls at higher rates, males of all dominance ranks uttered cackle, twitter, chutter, and plosive bark vocalizations. These results advance our knowledge of how male lemurs utilize agonistic vocalizations to maintain inter-individual relationships with males and females, and improve our overall understanding of the function of different agonistic vocalizations in wild lemurs.

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.

Affiliative Contact Calls during Group Travel: Chirp and Wail Vocalization Use in the Male Ring-Tailed Lemur (Lemur catta).

Affiliative vocalizations occur across primate taxa and may be used to maintain spatial cohesion and/or to regulate social interactions in group-living species. For gregarious strepsirhines like the ring-tailed lemur (Lemur catta), with large vocal repertoires and several distinct affiliative vocalizations including the chirp and wail, it is important to understand behavioural usage of these vocalizations to gain insight into their social interactions. To determine whether chirp and wail vocalizations facilitate group cohesion, regulate interactions to achieve socially positive outcomes, and are correlated with differences in individual characteristics such as dominance rank and age, I collected 565 h of focal data on 31 males aged ≥1 year at Beza Mahafaly Special Reserve, Madagascar, from March to July 2010. I found that chirp and wail vocalizations occurred at the highest rates during group-wide travel compared to other behaviours. Although nearest neighbour distance did not influence calling rate, focal animals maintained the same distance or were located closer to nearest neighbours after calling. Both chirp and wail calls were heard in behavioural contexts without agonism rather than agonistic contexts. No relationship was found between male calling rate and dominance rank or age, although the chirp showed a non-significant tendency to be produced at higher rates by younger males. Overall, my results indicated that ring-tailed lemur males of all ages and dominance ranks used both chirp and wail vocalizations as contact calls during group-wide travel events, helping individuals maintain proximity to other group members during movement. Chirp and wail vocalizations may additionally help regulate the caller's social interactions and promote increased tolerance from conspecifics. These findings add to our understanding of the breadth of communication behaviour in wild lemurs, thus furthering our knowledge of the social lives and cognitive abilities of strepsirhines. Through examining the complexity of vocalization use by a living lemur species with a communication system much like early social primates, we gain broad insight into the evolution of primate sociality.

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.

Antipredator Vocalization Usage in the Male Ring-Tailed Lemur (Lemur catta).

The ring-tailed lemur (Lemur catta) is a group-living strepsirrhine primate endemic to Madagascar that faces considerable predation pressure from aerial and terrestrial predators. This species engages in mobbing and vigilance behavior in response to predators, and has referential alarm vocalizations. Because L. catta is female dominant, less is known about the alarm calls of males. We tested 3 hypotheses for male antipredator vocalization behavior on L. catta at the Bezà Mahafaly Special Reserve in Madagascar: the predator confusion, group maintenance, and predation risk allocation hypotheses. We found support for 2 hypotheses. When a male L. catta made an antipredator call, other group members vocalized in response. Dominant males did not make alarm calls at higher rates than subordinate males. Predators were more abundant on the western side of Parcel 1, but an even greater number of antipredator vocalizations occurred in this area than predator abundance warranted. We show that male L. catta consistently participated in group-level antipredator vocalization usage in high-risk locations. Although female L. catta are known to hold the primary role in group defense, male L. catta are also key participants in group-wide behaviors that may confuse or drive away predators.

Male-specific use of the purr in the ring-tailed lemur (Lemur catta).

In mammals, purring has been described in mostly affiliative contexts. In the ring-tailed lemur (Lemur catta), both males and females purr, but only males were observed purring in agonistic contexts. In order to determine whether male ring-tailed lemurs purr as aggressive displays during intrasexual agonistic encounters, 480 h of focal data were collected on 25 adult males from Beza Mahafaly Special Reserve, Madagascar, from March to July 2010. The male purring rate increased during periods of male-male agonism when compared to times without intrasexual agonism, and the purring rate was positively correlated with male dominance rank. However, the purring rate was not significantly higher during winning agonistic interactions when compared with losing encounters. My results indicate that the male ring-tailed lemur purr is used most frequently as an agonistic vocalization in male-male encounters, in addition to being used less frequently in other social contexts, including during tail-waving at females, resting, scent-marking, feeding and copulation. Dominant males have higher purring rates across social situations, suggesting that the purring rate may be driven by intrinsic male qualities rather than functioning as a meaningful signal in each disparate social context. Male purring in intrasexual agonistic encounters can be added to previously described social contexts for ring-tailed lemur purring.

Squealing rate indicates dominance rank in the male ring-tailed lemur (Lemur catta).

Squeals are sharp and forceful short-range vocalizations used as aggressive and submissive agonistic signals by many mammalian species. The ring-tailed lemur (Lemur catta), a female-dominant strepsirhine primate, has a male-specific squeal call with proposed male-male agonistic functions and male-female courtship functions that have never been empirically tested. The goal of my study is to clarify why ring-tailed lemur males squeal at other males and females by applying the handicap hypothesis to this male-specific vocalization. This hypothesis has rarely been tested in primates, and this study elucidates how the rate of a male-specific call relates to male-male and male-female behavior in a Malagasy strepsirhine. To test whether males squeal towards other males to assert dominance, I predict that male squealing rate is positively correlated with dominance rank. I further predict that male ring-tailed lemurs squeal at other males while engaged in agonistic interactions, and that squealing during an interaction is positively correlated with winning that encounter. To test whether males squeal towards females as a mate attraction signal, I predict that male squealing rate is higher on estrus days, and that estrous females indicate attraction by approaching squealing males. From March to July 2010, 480 hr of focal data were collected on 25 males aged three and older at Beza Mahafaly Special Reserve, Madagascar. I continuously observed each male for 30 min at a time and recorded all agonistic interactions and squeal vocalizations using 1-0 sampling at 2.5-min intervals. Squealing rate was higher during times of male-male agonism when compared to times without male-male agonism, and males with higher dominance ranks had higher squealing rates. In contrast, the mate attraction hypothesis was not supported. My results suggest that the male squeal is an agonistic signal when used in male-male interaction in ring-tailed lemurs, but does not specifically indicate aggression or submission.