Flower consumption, ambient temperature and rainfall modulate drinking behavior in a folivorous-frugivorous arboreal mammal

Water is vital for the survival of any species because of its key role in most physiological processes. However, little is known about the non-food-related water sources exploited by arboreal mammals, the seasonality of their drinking behavior and its potential drivers, including diet composition, temperature, and rainfall. We investigated this subject in 14 wild groups of brown howler monkeys (Alouatta guariba clamitans) inhabiting small, medium, and large Atlantic Forest fragments in southern Brazil. We found a wide variation in the mean rate of drinking among groups (range = 0–16 records/day). Streams (44% of 1,258 records) and treeholes (26%) were the major types of water sources, followed by bromeliads in the canopy (16%), pools (11%), and rivers (3%). The type of source influenced whether howlers used a hand to access the water or not. Drinking tended to be evenly distributed throughout the year, except for a slightly lower number of records in the spring than in the other seasons, but it was unevenly distributed during the day. It increased in the afternoon in all groups, particularly during temperature peaks around 15:00 and 17:00. We found via generalized linear mixed modelling that the daily frequency of drinking was mainly influenced negatively by flower consumption and positively by weekly rainfall and ambient temperature, whereas fragment size and the consumption of fruit and leaves played negligible roles. Overall, we confirm the importance of preformed water in flowers to satisfy the howler’s water needs, whereas the influence of the climatic variables is compatible with the ‘thermoregulation/dehydration-avoiding hypothesis’. In sum, we found that irrespective of habitat characteristics, brown howlers seem to seek a positive water balance by complementing the water present in the diet with drinking water, even when it is associated with a high predation risk in terrestrial sources.Coordinación de la formación del personal de nivel superior/[2755/2010]/CAPES/BrasilNational Council for scientific and Technological Development/[303306/2013-0]/CNPq/BrasilNational Council for scientific and Technological Development/[304475/2018-1]/CNPq/BrasilNational Council for scientific and Technological Development/[140641/2016-5]/CNPq/BrasilUCR::Vicerrectoría de Docencia::Ciencias Básicas::Facultad de Ciencias::Escuela de Biologí

Efecto de la variación estacional en la cantidad de luz y de las interacciones planta-herbívoro sobre la fenología inversa de Jacquinia nervosa (Theophrastaceae)

Tesis (magister scientiae en biología)--Universidad de Costa Rica. Sistema de Estudios de Posgrado, 2002.UCR::Vicerrectoría de Investigación::Sistema de Estudios de Posgrado::Ciencias Básicas::Maestría Académica en Biologí

¿Qué tipo de árboles prefiere consumir Nasutitermes?

Las termitas son uno de los grupos de insectos más importantes en el mundo, tanto por el papel que juegan en la degradación de materia vegetal, como por los daños económicos que le causan al ser humano. En las zonas tropicales, Nasutitermes sp. es uno de los géneros de termitas más abundantes. No obstante, hasta la fecha se desconocen muchos aspectos básicos de su ecología. Durante los meses de enero y febrero de 1999, se evaluó la preferencia de Nasutitermes sp. por algunas características de los árboles en un Bosque Tropical Lluvioso y en un manglar en Costa Rica. Tanto en el bosque como en el manglar se trazaron 20 transectos lineales de 50 m de longitud y se determinó la especie, el tamaño, el diámetro a la altura del pecho (DAP) y el estado de salud de todos los árboles y arbustos con un diámetro basal = 3 cm. En el bosque se muestrearon 134 árboles de los cuales el 40,3% presentaron termiteros o caminos de forrajeo; mientras que en el manglar este porcentaje fue del 53,7%. En el bosque, las termitas mostraron un patrón de distribución aleatorio, mientras que en el manglar estuvieron agrupadas. La especie de árbol no afectó la presencia de termitas en ninguno de los dos ecosistemas. En el bosque y el manglar, Nasutitermes mostró una preferencia por los árboles con ramas secas y por árboles con fuste rugoso. El DAP y la altura estuvieron directamente relacionados con la presencia de termitas en el bosque, pero no en el manglar. Estos resultados sugieren que a pesar de que Nasutitermes es muy generalista en cuanto a las especies de árboles que consume, muestra cierta preferencia por algunas características estructurales de los árboles como lo son el tamaño, el grosor y la presencia de ramas secas

Retraso del enverdecimiento en las hojas nuevas de Pernettya prostrata (ericaceae): posibles funciones adaptativas

El retraso del enverdecimiento de las hojas nuevas es un fenómeno común en muchas especies de plantas tropicales. Así, en diferentes bosques lluviosos y de páramo de Costa Rica es frecuente observar una coloración rojiza en las hojas nuevas de diferentes especies de árboles y arbustos; sin embargo, hasta la fecha no se conoce con certeza la función que desempeña este carácter. Con el fin de evaluar el posible significado adaptativo de la coloración rojiza en las hojas nuevas del arbusto rastrero P. prostrata en un ecosistema de páramo del Cerro de la Muerte, sometí a prueba dos hipótesis principales: (1) la coloración rojiza de las hojas nuevas reduce los daños por herbivoría, y (2) esta coloración representa un mecanismo de fotoprotección. Para esto, establecí 20 parcelas de 15 x 15 m en un bosque de páramo del Cerro de la Muerte, en Costa Rica. En cada parcela diferencié tres diferentes microhábitas lumínicos (sombra, sombra intermedia y sol). En cada uno de estos microhábitas determiné la proporción de hojas rojizas y hojas verdes que presentaban daños por herbivoría, así como la proporción de hojas rojizas asociada a cada microhábitat lumínico. La herbivoría en hojas nuevas rojizas y verdes fue semejante. Sin embargo, la proporción hojas rojizas por rama se incrementó con la exposición a la luz. Estos resultados sugieren que la pigmentación rojiza de las hojas nuevas de P. prostrata podría representar una adaptación fisiológica contra el exceso de radiación solar que reciben las plantas de ambientes de páramo

Do seasonal changes in light availability influence the inverse leafing phenology of the neotropical dry forest understory shrub Bonellia nervosa (Theophrastaceae)?

In tropical dry forests most plants are deciduous during the dry season and flush leaves with the onset of the rains. In Costa Rica, the only species displaying the opposite pattern is Bonellia nervosa. To determine if seasonal changes in light availability are associated with the leaf and reproductive phenology of this species, we monitored leaf production, survival, and life span, as well as flower and fruit production from April 2000 to October 2001 in Santa Rosa National Park. Leaf flushing and flower bud production took place shortly after the autumnal equinox when day length starts to decrease. Leaves began expansion at the end of the wet season, and plants reached 70 % of their maximum leaf area at the beginning of the dry season, maintaining their foliage throughout the entire dry period. Leaf shedding occurred gradually during the first three months of the wet season. Leaf flushing and shedding showed high synchrony, with leaf numbers being related to light availability. Maximum leaf production coincided with peaks in radiation during the middle of the dry season. Decreasing day length induces highly synchronous flower bud emergence in dry forest species, but this is the first study indicating induction of leaf flushing by declining day length

Is the inverse leafing phenology of the dry forest understory shrub Jacquinia nervosa (Theophrastaceae) a strategy to escape herbivory?

In the dry forest of Santa Rosa National Park, Costa Rica, the understory shrub Jacquinia nervosa presents an inverse pattern of phenology that concentrates vegetative growth and reproduction during the dry season. In this study, we tested the “escape from herbivory” hypothesis as a potential explanation for the inverse phenological pattern of J. nervosa. We monitored leaf, flower and fruit production in 36 adult plants from October 2000 to August 2001. Leaves of six randomly selected branches per plant were marked and monitored every two weeks to measure the cumulative loss in leaf area. To analyze pre-dispersal seed predation we collected 15 fruits per plant and counted the total number of healthy and damaged seeds, as well as the number and type of seed predators found within the fruits. Leaf, flower, and fruit production occurred during the first part of the dry season (end of November to February). The cumulative herbivory levels were similar to those observed in other tropical dry forest tree species that concentrate leaf production during the wet season, and were concentrated on young leaves, which lost an average of 36.77 % of their area (SD= 34.35 %, N= 195). Chewing beetles of the genus Epicauta (Meloidae) were the most important herbivores. In mature leaves, most of the damage was caused by the beetle Coptocycla rufonotata (Chrysomelidae). Fruits took 4 months to develop during the dry season (January-March 2001) but continue increasing in size well into the first 3 months of the wet season (May-July). Average seed number per ripe fruit was 9 (SD = 5, N = 500). Seed predation in mature fruits was 42 % (SD = 47 %, N = 122). Most seeds were damaged by moth larvae of the family Tortricidae. Only 3 % of the flowers became fruits. This was influenced by the low level of flower synchrony (0.38±0.26, N = 36 plants), but neither leaf synchrony (0.88±0.06, N = 36 plants) nor plant size influenced fruit numbers. The significant damaged produced by insect herbivores in young leaves, fruits, and seeds, as well as the low reproductive index observed in J. nervosa, shows that the inverse leafing phenology of this species is not consistent with the “escape hypothesis” since J. nervosa was considerably attacked during the dry season. Considering the strong seasonality of the tropical dry forest and the heliophyte character of J. nervosa, it is more likely that this phenological strategy evolved in response to seasonal fluctuations in light availability, light quality, and daylength.Analizamos la hipótesis de “escape de la herbivoría” como explicación para la fenología foliar inversa del arbusto de sotobosque del bosque seco Jacquinia nervosa, el cual produce sus hojas durante la estación seca y se mantiene sin ellas durante la estación lluviosa. Medimos la producción de hojas, flores y frutos, el daño por herbivoría en hojas y semillas, y la fauna de herbívoros en 36 plantas adultas de octubre del 2000 a agosto del 2001 en Santa Rosa, Costa Rica. La herbivoría foliar acumulada durante la estación seca fue similar a la herbivoría de otras especies que concentran la producción foliar en la estación lluviosa. En las hojas maduras la mayor parte del daño fue causado por el escarabajo Coptocycla rufonotata (Chrysomelidae). La depredación de semillas predispersión fue de 42% (DE= 47 %, N= 122) y es causada por larvas de polilla de la familia Tortricidae. Los niveles de daño indican que la fenología foliar de J. nervosa no coincide con la hipótesis de “escape”. Considerando la fuerte estacionalidad del bosque seco y el carácter heliófito de J. nervosa, es probable que esta estrategia fenológica evolucionara en respuesta a cambios estacionales en la disponibilidad y calidad de la luz, y duración del fotoperíodo

Análisis comparativo de la folivoría en helechos y angiospermas en un Bosque Tropical Húmedo de Costa Rica

Comparamos la magnitud de la folivoría causada por insectos en helechos y angiospermas en tres diferentes tipos de bosque de la Estación Biológica La Selva: Bosque Tropical Húmedo de Altura (BTH1), Bosque Tropical Húmedo Basal (BTH2) y Bosque Secundario (BS). En términos generales, los helechos presentaron mayor folivoría que las angiospermas. Sin embargo, se presentaron diferencias entre ecosistemas. En BTH2 los daños fueron mayores para helechos que para las angiospermas, pero en BTH1 y en BS no hubo diferencias. Los helechos presentaron mayores daños en hojas jóvenes y en hojas maduras en comparación con las angiospermas. Para las angiospermas, la folivoría en ambos tipos de hoja fue similar entre ecosistemas. Sin embargo, en helechos las hojas jóvenes presentaron mayor daño en BTH2 que en los demás sitios. Nuestros resultados sugieren que los helechos no están tan bien protegidos como se creía y, al igual que en las angiospermas, en este grupo los herbívoros también representan una importante presión selectiva

Assessing the influence of biotic, abiotic, and social factors on the physiological stress of a large Neotropical primate in Atlantic Forest fragments

Wildlife physiological responses to environmental and human-related stressors provide useful clues on animal welfare. Non-invasive biomarkers, such as fecal glucocorticoid metabolites (fGCM), allow researchers to assess whether variations in habitat quality, behavior, and climate influence the animals' physiological stress. We examined the role of fragment size, ambient temperature, ripe fruit availability and consumption, percentage of records moving, sex, female reproductive state, and group composition as predictors of the level of fGCM in adult brown howler monkeys (Alouatta guariba clamitans) inhabiting three small (90 ha) Atlantic Forest fragments in southern Brazil. We collected bimonthly behavioral data and fecal samples from adult individuals over three years, and used a multimodel inference framework to identify the main predictors of fGCM. We found that the mean (±SD) fGCM in the study groups ranged from 57 ± 49 ng/g to 93 ± 58 ng/g, which were within the known range for howler monkeys. We found 10 best models including five of the 17 tested variables. Sex and reproductive state were the only variables included in all these models. We found that fGCM was higher in nursing females (mean ± SD = 104 ± 73 ng/g) than in non-nursing females (64 ± 55 ng/g) and males (53 ± 40 ng/g, P  0.05). We conclude that factors related to the energetic balance of individuals play major roles in modulating the physiological stress of brown howler monkeys. Future studies should investigate the consequences of higher levels of stress hormones on howler monkey health and demography.Coordenação de Aperfeiçoamento de Pessoal de Nível Superior/[Finance Code 001; PNPD grant # 2755/2010]/CAPES/BrasilUCR::Vicerrectoría de Docencia::Ciencias Básicas::Facultad de Ciencias::Escuela de Biologí

Plant diversity in the diet of Costa Rican primates in contrasting habitats: a meta-analysis

In human-modified tropical landscapes, the survival of arboreal vertebrates, particularly primates, depends on their plant dietary diversity. Here, we assessed diversity of plants included in the diet of Costa Rican non-human primates, CR-NHP (i.e. Alouatta palliata palliata, Ateles geoffroyi, Cebus imitator, and Saimiri oerstedii) inhabiting different habitat types across the country. Specifically, we assessed by analyzing 37 published and unpublished datasets: (i) richness and dietary -plant diversity, (ii) the β-diversity of dietary plant species and the relative importance of plant species turnover and nestedness contributing to these patterns, and (iii) the main ecological drivers of the observed patterns in dietary plant . Diet data were available for 33 Alouatta, 15 Cebus, 8 Ateles, and 5 Saimiri groups. Overall dietary plant species richness was higher in Alouatta (454 spp.), followed by Ateles (329 spp.), Cebus (237 spp.), and Saimiri (183 spp.). However, rarefaction curves showed that -diversity of plant species was higher in Ateles than in the other three primate species. The γ-diversity of plants was 868 species (range=1664-2041 species). The three most frequently reported food species for all CR-NHP were Spondias mombin, Bursera simaruba, and Samanea saman. In general, plant species turnover, rather than nestedness, explainedthe dissimilarity in plant diet diversity (βsim = 0.76) of CR_NHP. Finally, primate species, habitat type (life zone and disturbance level) and, to a lesser degree, sampling effort were the best predictors of the dietary plant assemblages. Our findings suggest that CR-NHPdiets were diverse, even in severely-disturbed habitats.Universidad de Costa RicaUCR::Vicerrectoría de Investigación::Unidades de Investigación::Ciencias de la Salud::Laboratorio de Ensayos Biológicos (LEBI)UCR::Vicerrectoría de Docencia::Ciencias Básicas::Facultad de Ciencias::Escuela de BiologíaUCR::Vicerrectoría de Investigación::Unidades de Investigación::Ciencias Básicas::Centro de Investigación en Biodiversidad y Ecología Tropical (CIBET)UCR::Sedes Regionales::Sede de Occidente::Recinto San RamónUCR::Vicerrectoría de Docencia::Ciencias Sociales::Facultad de Ciencias Sociales::Escuela de Antropologí

Fermented food consumption in wild nonhuman primates and its ecological drivers

Objectives: Although fermented food use is ubiquitous in humans, the ecological and evolutionary factors contributing to its emergence are unclear. Here we investigated the ecological contexts surrounding the consumption of fruits in the late stages of fermentation by wild primates to provide insight into its adaptive function. We hypothesized that climate, socioecological traits, and habitat patch size would influence the occurrence of this behavior due to effects on the environmental prevalence of late-stage fermented foods, the ability of primates to detect them, and potential nutritional benefits. Materials and methods: We compiled data from field studies lasting at least 9 months to describe the contexts in which primates were observed consuming fruits in the late stages of fermentation. Using generalized linear mixed-effects models, we assessed the effects of 18 predictor variables on the occurrence of fermented food use in primates. Results: Late-stage fermented foods were consumed by a wide taxonomic breadth of primates. However, they generally made up 0.01%–3% of the annual diet and were limited to a subset of fruit species, many of which are reported to have mechanical and chemical defenses against herbivores when not fermented. Additionally, latestage fermented food consumption was best predicted by climate and habitat patch size. It was more likely to occur in larger habitat patches with lower annual mean rainfall and higher annual mean maximum temperatures. Discussion: We posit that primates capitalize on the natural fermentation of some fruits as part of a nutritional strategy to maximize periods of fruit exploitation and/or access a wider range of plant species. We speculate that these factors contributed to the evolutionary emergence of the human propensity for fermented foods.Canadian Institute for Advanced Research/[]/CIFAR/CanadáUCR::Vicerrectoría de Docencia::Ciencias Básicas::Facultad de Ciencias::Escuela de Biologí