The ontogeny of feeding is characterized by shifting functional demands concurrent with changes in craniofacial anatomy; relationships between these factors will look different in primates with disparate feeding behaviors during development. This study examines the ontogeny of skull morphology and jaw leverage in tufted (Sapajus) and untufted (Cebus) capuchin monkeys. Unlike Cebus, Sapajus have a mechanically challenging diet and behavioral observations of juvenile Sapajus suggest these foods are exploited early in development. Landmarks were placed on three-dimensional surface models of an ontogenetic series of Sapajus and Cebus skulls (n = 53) and used to generate shape data and jaw-leverage estimates across the tooth row for three jaw-closing muscles (temporalis, masseter, medial pterygoid) as well as a weighted combined estimate. Using geometric morphometric methods, we found that skull shape diverges early and shape is significantly different between Sapajus and Cebus throughout ontogeny. Additionally, jaw leverage varies with age and position on the tooth row and is greater in Sapajus compared to Cebus when calculated at the permanent dentition. We used two-block partial least squares analyses to identify covariance between skull shape and each of our jaw muscle leverage estimates. Sapajus, but not Cebus, has significant covariance between all leverage estimates at the anterior dentition. Our findings show that Sapajus and Cebus exhibit distinct craniofacial morphologies early in ontogeny and strong covariance between leverage estimates and craniofacial shape in Sapajus. These results are consistent with prior behavioral and comparative work suggesting these differences are a function of selection for exploiting mechanically challenging foods in Sapajus, and further emphasize that these differences appear quite early in ontogeny. This research builds on prior work that has highlighted the importance of understanding ontogeny for interpreting adult morphology.
Cebus , Jaw , Skull , Animals , Skull/anatomy & histology , Skull/growth & development , Jaw/anatomy & histology , Cebus/anatomy & histology , Sapajus/anatomy & histology , Sapajus/growth & development , Feeding Behavior/physiology , Male , Female
OBJECTIVES: Studies on oral processing are often snapshots of behaviors that examine feeding through individual bouts. In this study, we expand on our previous work comparing bite/chew variables per feeding bout to summed daily biting, chewing, and food intake to interpret loading that could have potential morphological effects. MATERIALS AND METHODS: We observed sympatric Lemur catta and Propithecus verreauxi over two field seasons in the dry forest of Bezà Mahafaly Special Reserve in southwestern Madagascar. Bite and chew rates determined from videos filmed during observations were multiplied with time spent feeding on specific foods during focal follows to calculate daily values for each feeding bout. Food mechanical properties (FMPs) were tested on dietary items with a portable tester. We contrasted daily bite/chew numbers and intake with FMPs, species, season, and food shape. RESULTS: Daily bite and chew numbers increased with maximum, but not average, food toughness. Daily intake decreased with average and maximum toughness. Season had a strong effect on daily bites and chews, but not on intake. Food shape influenced intake and total bite and chew numbers. The lemur species did not differ in our models. DISCUSSION: Maximum food toughness impacted feeding behaviors and intake, which is consistent with higher loads having a greater effect on morphology. In contrast to feeding per bout, cumulative biting and chewing did not differ between species; taking feeding frequency into consideration affects interpretation of jaw loading. Finally, biting, as much as chewing, may generate strains that impact morphology.
Lemur , Lemuridae , Succinimides , Animals , Lemur/anatomy & histology , Diet , Food
OBJECTIVES: The link between diet and the masticatory apparatus in primates is complex. We investigated how food mechanical properties (FMPs) and food geometry affect feeding behaviors and subsequent jaw loading. We compared oral processing in two sympatric lemur species with distinct diets and mandibular morphologies. MATERIALS AND METHODS: All-day focal follows of Lemur catta (Lc) and Propithecus verreauxi (Pv) were conducted in both the dry and wet seasons at Beza Mahafaly Special Reserve. We collected activity budget data, filmed feeding bouts, and collected food items to measure their mechanical properties with an FLS-1 portable tester. Feeding videos for the top food items they spent the most time consuming were analyzed frame-by-frame to assess bite and chew numbers and rates. RESULTS: Lc bite more and at a slower rate on tougher (maximum) foods, chew more for tougher (average) foods, and chew less for stiffer leaves. Pv initially increase chew number for tougher (average) foods, but their behavior is less affected as food toughness increases. Pv chew less and more slowly but spend more of the day feeding than Lc. Additionally, they have a tougher (maximum) diet than Lc. DISCUSSION: Lc adjust their feeding behaviors depending on the FMPs of their top food items, while Pv feed more consistently. The more robust masticatory apparatus of Pv may not require them to adjust their feeding behaviors for more mechanically challenging foods. Furthermore, the two species show distinct differences in chewing. Exploring chewing on a daily scale could aid in understanding its impact on the loading of the masticatory apparatus.
Lemur , Lemuridae , Animals , Diet , Feeding Behavior
Bite force and gape are two important performance metrics of the feeding system, and these metrics are inversely related for a given muscle size because of fundamental constraints in sarcomere length-tension relationships. How these competing performance metrics change in developing primates is largely unknown. Here, we quantified in vivo bite forces and gapes across ontogeny and examined these data in relation to body mass and cranial measurements in captive tufted capuchins, Sapajus spp. Bite force and gape were also compared across geometric and mechanical properties of mechanically challenging foods to investigate relationships between bite force, gape and food accessibility (defined here as the ability to breach shelled nuts). Bite forces at a range of gapes and feeding behavioral data were collected from a cross-sectional ontogenetic series of 20 captive and semi-wild tufted capuchins at the Núcleo de Procriação de Macacos-Prego Research Center in Araçatuba, Brazil. These data were paired with body mass, photogrammetric measures of jaw length and facial width, and food geometric and material properties. Tufted capuchins with larger body masses had absolutely higher in vivo bite forces and gapes, and animals with wider faces had absolutely higher bite forces. Bite forces and gapes were significantly smaller in juveniles compared with subadults and adults. These are the first primate data to empirically demonstrate the gapes at which maximum active bite force is generated and to demonstrate relationships to food accessibility. These data advance our understanding of how primates meet the changing performance demands of the feeding system during development.
Bite Force , Skull , Animals , Cross-Sectional Studies , Feeding Behavior/physiology , Sarcomeres , Biomechanical Phenomena , Jaw/physiology
Lianas are woody climbers and their stems and leaves deal with different environmental pressures such as resistance to mechanical damage and dehydration. The damage resistance of plants can be biomechanically evaluated by their stiffness, bending and toughness. Despite the well-known relationship between physical resistance and moisture of plant organs in woody plants, this relationship is uncertain and has not been previously evaluated in lianas. Thus, this study investigated experimentally the effect of stems and leaf dehydration on the structural Young's modulus in the stem and fracture toughness in leaves across time in the liana Amphilophium crucigerum (Bignoniaceae). Ten stem and leaf samples were collected and assigned to two distinct conditions: (i) samples kept moist and (ii) samples underwent gradual dehydration with natural moisture loss by air exposition. Successive measures of structural Young's modulus and fracture toughness were taken every 4 hours during a 48-hour period for both conditions. Stem and leaf samples which underwent gradual dehydration showed greater bending stiffness and fracture toughness, respectively, while the samples kept moist presented no changes in any studied biomechanical features during the entire experiment. We concluded that the moisture of both stem and leaf samples are critical factors to estimate the biomechanical properties of lianas stem and leaves.
Lianas são trepadeiras lenhosas e seus caules e folhas lidam com diferentes pressões ambientais, como a resistência aos danos mecânicos e de desidratação. A resistência ao dano das plantas pode ser biomecanicamente avaliada pelas propiedades de dureza, flexão e tenacidade. Apesar da conhecida relação entre resistência física e umidade dos órgãos das plantas em espécies lenhosas, essa relação não foi avaliada anteriormente e é incerta em lianas. Assim, este estudo investigou experimentalmente o efeito da desidratação de caules e folhas na estimativa do módulo estrutural de Young do caule e da tenacidade à fratura da folha ao longo do tempo, na liana Amphilophium crucigerum (Bignoniaceae). Dez amostras de caules e folhas foram coletadas e distribuídas em duas condições distintas: (i) amostras mantidas úmidas e (ii) amostras em processo de desidratação gradativa com perda natural de umidade quando expostas ao ar. Medidas sucessivas do módulo de Young e da resistência à fratura dos órgãos foram tomadas a cada 4 horas durante um período de 48 horas em ambas as condições. Amostras de caule e folhas que sofreram desidratação gradual apresentaram maior rigidez à flexão e tenacidade à fratura, respectivamente, enquanto as amostras mantidas úmidas não alteraram essas características durante o experimento. Concluímos que a umidade das amostras de caules e folhas em lianas também é um fator crítico para estimar as propriedades biomecânicas desses órgãos em seu ambiente natural.
Examining interactions among sympatric primate species can provide interesting information about competition, cooperation, and avoidance between those species. Those interactions can be neutral, positive, or negative for the species involved. Capuchin monkeys are medium-sized primates that can encounter both larger and smaller primates in their varied habitats. Gracile capuchins (Cebus) are reported to present different types of interactions with other primates. Interactions with howler monkeys frequently include physical aggression, while interactions with spider monkeys are mostly threats and chases. Moreover, interaction types are not consistent across populations. Among robust capuchins (Sapajus spp.), however, no reports have been published. Here we describe and classify encounters of Sapajus libidinosus and S. nigritus with Alouatta caraya, A. guariba, Brachyteles arachnoides, and Callithrix jacchus in three sites in the environments of Cerrado, Caatinga (savannah-like), and Atlantic forest, and compare the interaction patterns among sites and different group sizes. The latter is a factor that can influence the outcome, and we expected capuchins in larger groups to be more aggressive toward other primates. Our results of 8421 h of total contact with the capuchin groups show that, indeed, capuchins in sites with larger groups presented aggressive interactions with higher frequency. However, the other species' body size also seems important as smaller primates apparently avoided capuchins, and interactions with the larger muriquis were mostly neutral for the capuchin. Capuchins showed neutral or aggressive behaviors toward howler monkeys, with differences between the rainforest and savannah groups. We found that robust capuchins can present aggressive interactions even to primates larger than themselves and that aggressive behavior was the most common response in populations living in larger groups and drier environments.
Alouatta/physiology , Atelinae/physiology , Behavior, Animal , Cebus/physiology , Sapajus/physiology , Aggression , Animals , Brazil , Ecosystem , Female , Male , Rainforest , Seasons , Social Behavior
The biomechanical and adaptive significance of variation in craniodental and mandibular morphology in fossil hominins is not always clear, at least in part because of a poor understanding of how different feeding behaviors impact feeding system design (form-function relationships). While laboratory studies suggest that ingestive behaviors produce variable loading, stress, and strain regimes in the cranium and mandible, understanding the relative importance of these behaviors for feeding system design requires data on their use in wild populations. Here we assess the frequencies and durations of manual, ingestive, and masticatory behaviors from more than 1400 observations of feeding behaviors video-recorded in a wild population of bearded capuchins (Sapajus libidinosus) at Fazenda Boa Vista in Piauí, Brazil. Our results suggest that ingestive behaviors in wild Sapajus libidinosus were used for a range of food material properties and typically performed using the anterior dentition. Coupled with previous laboratory work indicating that ingestive behaviors are associated with higher mandibular strain magnitudes than mastication, these results suggest that ingestive behaviors may play an important role in craniodental and mandibular design in capuchins and may be reflected in robust adaptations in fossil hominins.
Cebinae/metabolism , Feeding Behavior/physiology , Mastication/physiology , Animals , Animals, Wild , Anthropology, Physical/methods , Biological Evolution , Biomechanical Phenomena , Eating/physiology , Female , Male , Mandible/physiology
Membros de um grupo social de primatas diurnos reúnem-se ao final do dia num local apropriado para passar a noite. O local de dormida é denominado sitio de dormir e pode consistir em uma ou mais arvores. Hipoteses adaptativas tabem sido sugeridas para explicar preferencias por arvores e sitios de dormir. O risco de predacao tem sido apontado como uma das principais pressoes seletivas que afetam a escolha de arvores e sitios de dormir. A estrategia de escolha de sitio de dormir e de arvore de dormir, para um mesmo grupo de primatas, pode diferir. Assim, o sitio de dormir pode estar localizado proximo as fontes alimentares, facilitando o forrageamento pela manha e as arvores usadas nesse sitio podem proporcionar conforto e seguranca, pela viscosidade e presenca de galhos horizontais e largos. Encontramos, para um grupo de macacos-prego, no Parque Estadual Carlos Botelho, SP, evidencias de selecao por caracteristicas de arvores e sitios de dormir. As especies de arvores mais usadas como arvore de dormir foram Copaifera langsdorfii e Attalea dubia, sendo a segunda relacionada com noites de baixa temperatura ambiente e do vento. Houve tambem preferencia por arvores altas e com grande DAP, por sitios localizados entre 820 e 840 metros de altitude e em encostas e topos de morro. Embora tenhamos encontrado evidencias de seletividade para arvore e sitio de dormir, os sitios e arvores preferidos estao distribuidos por toda a area de uso e sao pouco reutilizados. Como consequencia, o grupo dorme perto da area explorada para forrageamento durante o dia. Assim, a localizacao do sitio de dormir nao parece afetar a rota diaria do grupo
Group members of diurnal primates meet at the end of the day in a suitable area to spend the night. This location is called sleeping site and may consist of one or more trees. Ultimate hypotheses have been suggested to explain primate preferences for sleeping trees and sleeping sites. The risk of predation has been identified as one of the main selective pressures that affect the choice of sleeping trees and sleeping sites. The strategy of sleeping tree and sleeping site selection, by a single group of primates, may differ. Thus, the sleeping site can be located close to food sources, facilitating the foraging in the morning and the trees used on this site can guarantee comfort and safety, due to viscosity and presence of horizontal large branches. Studying a group of tufted capuchin monkeys, at Carlos Botelho State Park, SP, we found evidence of selection of sleeping trees and sleeping sites features. The most commonly used species of trees as sleeping trees were Copaifera langsdorfii and Attalea dubia, the second was related to nights with low environment and wind temperatures. There is also a preference for high trees with large DBH, and for sites located at 820 and 840 metres, on hillsides and hilltops. Although we have found evidence of selectivity for sleeping trees and sleeping sites, the sites and preferred trees occur throughout the monkeys home range and are not normally reused. As a consequence, the group sleep near the area explored during daily foraging. Therefore, the sleeping site location does not seem to affect the animals daily route
