Activity budget and gut microbiota stability and flexibility across reproductive states in wild capuchin monkeys in a seasonal tropical dry forest.

BACKGROUND: Energy demands associated with pregnancy and lactation are significant forces in mammalian evolution. To mitigate increased energy costs associated with reproduction, female mammals have evolved behavioural and physiological responses. Some species alter activity to conserve energy during pregnancy and lactation, while others experience changes in metabolism and fat deposition. Restructuring of gut microbiota with shifting reproductive states may also help females increase the energy gained from foods, especially during pregnancy. The goal of this study was to examine the relationships among behaviour, gut microbiota composition, and reproductive state in a wild, non-human primate to better understand reproductive ecology. We combined life history data with > 13,000 behavioural scans and 298 fecal samples collected longitudinally across multiple years from 33 white-faced capuchin monkey (Cebus imitator) females. We sequenced the V4 region of the 16S rRNA gene and used the DADA2 pipeline to analyze microbial diversity. We used PICRUSt2 to assess putative functions. RESULTS: Reproductive state explained some variation in activity, but overall resting behaviours were relatively stable across pregnancy and lactation. Foraging was less frequent among females in the early stage of nursing compared to the cycling stage, though otherwise remained at comparable levels. Maximum temperature was a strong, significantly positive predictor of resting, while social dominance had a small but significantly negative effect on resting. Ecological variables such as available fruit biomass and rainfall had a small but significantly positive effects on measures of foraging time. Gut microbial community structure, including richness, alpha diversity, and beta diversity remained stable across the reproductive cycle. In pairwise comparisons, pregnant females exhibited increased relative abundances of multiple microbial ASVs, suggesting small changes in relation to reproductive state. Reproductive state was not linked to differential abundance of putative metabolic pathways. CONCLUSIONS: Previous data suggest that activity budget and the gut microbiome shifts considerably during reproduction. The present study finds that both activity and gut microbial communities are less associated with reproduction compared to other predictors, including ecological contexts. This suggests that behavioural flexibility and gut microbial community plasticity is contrained by ecological factors in this population. These data contribute to a broader understanding of plasticity and stability in response to physiological shifts associated with mammalian reproduction.

Anatomy and dietary specialization influence sensory behaviour among sympatric primates.

Senses form the interface between animals and environments, and provide a window into the ecology of past and present species. However, research on sensory behaviours by wild frugivores is sparse. Here, we examine fruit assessment by three sympatric primates (Alouatta palliata, Ateles geoffroyi and Cebus imitator) to test the hypothesis that dietary and sensory specialization shape foraging behaviours. Ateles and Cebus groups are comprised of dichromats and trichromats, while all Alouatta are trichomats. We use anatomical proxies to examine smell, taste and manual touch, and opsin genotyping to assess colour vision. We find that the frugivorous spider monkeys (Ateles geoffroyi) sniff fruits most often, omnivorous capuchins (Cebus imitator), the species with the highest manual dexterity, use manual touch most often, and that main olfactory bulb volume is a better predictor of sniffing behaviour than nasal turbinate surface area. We also identify an interaction between colour vision phenotype and use of other senses. Controlling for species, dichromats sniff and bite fruits more often than trichromats, and trichromats use manual touch to evaluate cryptic fruits more often than dichromats. Our findings reveal new relationships among dietary specialization, anatomical variation and foraging behaviour, and promote understanding of sensory system evolution.

Ecotourism and primate habituation: Behavioral variation in two groups of white-faced capuchins (Cebus capucinus) from Costa Rica.

The increase of ecotourism operations within Costa Rica during the last 20 yrs has brought more and more humans into close, direct contact with several wildlife species. One of these species is the white-faced capuchin (Cebus capucinos), highly gregarious, and with exposure over time, willing to come into close vicinity of humans and their developments. Such contact has its advantages and disadvantages for the ecotourism industry. We observed white-faced monkeys in order to assess the impact of human presence and development on monkey behavior, with a focus on aggressive, affiliative, and foraging behaviors in Curú Wildlife Refuge (CWR), located in Puntarenas, Costa Rica, and to ascertain the degree of over-habituation of capuchin popula- tions at CWR. Though there exists no discrete behavioral parameters that measure over-habituation, it can be defined as an extreme state of habituation in which non-human primates not only lose fear of humans, but also actively include humans in social interactions or treat them as a food resource. We used instantaneous focal animal and group scan sampling during 8 wks in March and April 2012. Two groups (approximately 20-30 individuals each) of capuchins were observed; the first near the tourist development at the Southwestern area of CWR, representing a habituated population that regularly foraged, rested, and groomed in the presence of humans. The second, was observed in the Northeastern area of CWR, did not visit the center of human activity and exhibited fear of humans. The habituated group exhibited significantly fewer instances of threatened behavior in response to human presence (p < 0.0001) than the non-habituated group, and spent significantly more time eating and foraging (p < 0.0001). While the habituated monkeys at CWR may not be over-habituated, they could become that way as development, especially ecotourism, increases. Over-habituation is a problem that affects capuchins in certain ecotourism sites in Costa Rica. It is critical that the consequences of habituation be studied more carefully, primarily in areas where ecotourism operations draw visitors to wildlife habitats.

Ecotourism and primate habituation: Behavioral variation in two groups of white-faced capuchins (Cebus capucinus) from Costa Rica / Ecoturismo y habituación de primates: variación en comportamiento de dos grupos de monos carablanca (Cebus capucinus) en Costa Rica

The increase of ecotourism operations within Costa Rica during the last 20yrs has brought more and more humans into close, direct contact with several wildlife species. One of these species is the white-faced capuchin (Cebus capucinus), highly gregarious, and with exposure over time, willing to come into close vicinity of humans and their developments. Such contact has its advantages and disadvantages for the ecotourism industry. We observed white-faced monkeys in order to assess the impact of human presence and development on monkey behavior, with a focus on aggressive, affiliative, and foraging behaviors in Curú Wildlife Refuge (CWR), located in Puntarenas, Costa Rica, and to ascertain the degree of over-habituation of capuchin populations at CWR. Though there exists no discrete behavioral parameters that measure over-habituation, it can be defined as an extreme state of habituation in which non-human primates not only lose fear of humans, but also actively include humans in social interactions or treat them as a food resource. We used instantaneous focal animal and group scan sampling during 8wks in March and April 2012. Two groups (approximately 20-30 individuals each) of capuchins were observed; the first near the tourist development at the Southwestern area of CWR, representing a habituated population that regularly foraged, rested, and groomed in the presence of humans. The second, was observed in the Northeastern area of CWR, did not visit the center of human activity and exhibited fear of humans. The habituated group exhibited significantly fewer instances of threatened behavior in response to human presence (p<0.0001) than the non-habituated group, and spent significantly more time eating and foraging (p<0.0001). While the habituated monkeys at CWR may not be over-habituated, they could become that way as development, especially ecotourism, increases. Over-habituation is a problem that affects capuchins in certain ecotourism sites in Costa Rica. It is critical that the consequences of habituation be studied more carefully, primarily in areas where ecotourism operations draw visitors to wildlife habitats. Rev. Biol. Trop. 62 (3): 909-918. Epub 2014 September 01.

El aumento de actividades ecoturísticas en Costa Rica durante los últimos 20 años ha ocasionado que más y más personas entren en contacto directo y cercano con varias especies de vida silvestre. Una de estas especies es el mono carablanca (Cebus capucinus), que es muy gregario y, al pasar el tiempo, tiende a acercarse a los humanos y sus instalaciones. Tal contacto tiene ventajas y desventajas para la industria del ecoturismo. Observamos monos carablanca con el fin de evaluar el impacto de la presencia humana y la infraestructura en el comportamiento de estos animales, enfocando los comportamientos de agresión, acicalamiento y forrajeo para determinar el grado de habituación excesiva de las poblaciones de monos capuchinos en el Refugio de Vida Silvestre Curú, Puntarenas, Costa Rica. Aunque no existen parámetros específicos de comportamiento para medir la habituación excesiva, se puede definir esta condición como un estado en que los primates no humanos no solamente pierdan su temor a los humanos, sino que también incluyen a las personas activamente en sus interacciones sociales o las consideran como una fuente de alimentación. Los monos carablanca fueron observados a través del muestreo instantáneo focal y por escaneo grupal durante ocho semanas de marzo y abril de 2012. Dos grupos (aproximadamente 20-30 individuos cada uno) fueron observados; uno cerca del desarrollo turístico en la parte suroeste del refugio, que representó una población habituada que de manera regular comía, descansaba y se acicalaba en presencia de humanos; el segundo grupo, que se observó en el noreste del refugio, no visitaba el centro de actividad humana y mostraba temor hacia los humanos. El grupo habituado mostró significativamente menos ocasiones de comportamiento amenazante ante la presencia humana (p<0.0001) y empleó más tiempo comiendo y buscando alimento (p<0.0001). Aunque el grupo de habituados en Curú probablemente no tenga habituación excesiva, esta condición podría surgir más adelante, especialmente si aumenta el desarrollo, y en particular el ecoturismo. La habituación excesiva es un problema que afecta a los monos carablanca en ciertos sitios secoturísticos de Costa Rica. Es de suma importancia que las consecuencias de la habituación excesiva se estudien más a fondo, principalmente en las áreas donde las actividades ecoturísticas atraen visitantes a los hábitats de la vida silvestre.