Developmental Programming of Capuchin Monkey Adrenal Dysfunction by Gestational Chronodisruption.

In the capuchin monkey (Cebus apella), a new-world nonhuman primate, maternal exposure to constant light during last third of gestation induces precocious maturation of the fetal adrenal and increased plasma cortisol in the newborn. Here, we further explored the effects of this challenge on the developmental programming of adrenal function in newborn and infant capuchin monkeys. We measured (i) plasma dehydroepiandrosterone sulphate (DHAS) and cortisol response to ACTH in infants with suppressed endogenous ACTH, (ii) plasma DHAS and cortisol response to ACTH in vitro, and (iii) adrenal weight and expression level of key factors in steroid synthesis (StAR and 3ß-HSD). In one-month-old infants from mothers subjected to constant light, plasma levels of cortisol and cortisol response to ACTH were twofold higher, whereas plasma levels of DHAS and DHAS response to ACTH were markedly reduced, compared to control conditions. At 10 months of age, DHAS levels were still lower but closer to control animals, whereas cortisol response to ACTH was similar in both experimental groups. A compensatory response was detected at the adrenal level, consisting of a 30% increase in adrenal weight and about 50% reduction of both StAR and 3ß-HSD mRNA and protein expression and the magnitude of DHAS and cortisol response to ACTH in vitro. Hence, at birth and at 10 months of age, there were differential effects in DHAS, cortisol production, and their response to ACTH. However, by 10 months of age, these subsided, leading to a normal cortisol response to ACTH. These compensatory mechanisms may help to overcome the adrenal alterations induced during pregnancy to restore normal cortisol concentrations in the growing infant.

Renal artery in tufted capuchin monkey: structure and morphometry / Artéria renal do macaco prego: estrutura e morfometria

The objective was to describe the structure of the renal artery in capuchin monkey at the level of the proximal and distal arterial segments. Morphometric analysis was performed referring to the thickness and quantification of tissue elements of the renal artery tunica media in both segments. Renal arteries of eight adult capuchin monkeys were collected for histological analysis of the two segments, being the proximal part branched from the abdominal aorta, and the distal part localized next to the renal hilus. The quantification of smooth muscle cells and connective elements was carried out in transversal sections of the two segments; for the tunica media, it was used the volume densities of smooth muscle cells, collagen and elastic fibers. Considering these volume densities obtained for each segment, it was verified that the proximal segment showed a marked myoconnective architecture, while the distal segment was characterized by a single muscular artery. Apparently, the mixed architecture of the proximal segment could be related to a blood flow control at the aortic emergence of the renal artery, which helped to guarantee a priority flow of enriched plasma into the kidney parenchyma.

O objetivo foi descrever a estrutura da artéria renal no macaco prego ao nível dos segmentos arteriais proximal e distal. Uma análise morfométrica foi realizada, tendo como parâmetros a espessura e a quantificação dos elementos constituintes da túnica média da parede vascular, nos dois segmentos. Foram coletadas as artérias renais de oito macacos pregos adultos para estudos histológicos dos dois segmentos, sendo o segmento proximal a parte originária da aorta abdominal e o segmento distal a parte arterial junto ao hilo renal. A quantificação de células musculares lisas e de elementos conjuntivos da matriz extracelular foi realizada em secções transversais dos dois segmentos, sendo empregadas para a túnica média as densidades de volumes (DV), dos componentes musculares e das fibras elásticas e colágenas. Tendo por base estas densidades de volumes obtidas para cada segmento arterial verificou-se que o segmento proximal apresentou estrutura mioconjuntiva marcante, enquanto que o segmento distal foi caracterizado como uma artéria muscular padrão. Aparentemente, a arquitetura mista do segmento proximal estaria relacionada com o controle de fluxo sanguíneo na emergência aórtica da artéria renal, garantindo um direcionamento prioritário de fluxo de plasma sanguíneo enriquecido para dentro do parênquima renal.

Tufted capuchin monkeys (Sapajus sp) learning how to crack nuts: does variability decline throughout development?

We investigated the process of nut-cracking acquisition in a semi-free population of tufted capuchin monkeys (Sapajus sp) in São Paulo, Brazil. We analyzed the cracking episodes from monkeys of different ages and found that variability of actions related to cracking declined. Inept movements were more frequent in juveniles, which also showed an improvement on efficient striking. The most effective behavioral sequence for cracking was more frequently used by the most experienced monkeys, which also used non-optimal sequences. Variability in behavior sequences and actions may allow adaptive changes to behavior under changing environmental conditions.

Development of snake-directed antipredator behavior by wild white-faced capuchin monkeys: I. Snake-species discrimination.

Young animals are known to direct alarm calls at a wider range of species than adults. Our field study examined age-related differences in the snake-directed antipredator behavior of infant, juvenile, and adult white-faced capuchin monkeys (Cebus capucinus) in terms of alarm calling, looking behavior, and aggressive behavior. In the first experiment, we exposed infant and juvenile white-faced capuchins to realistic-looking inflatable models of their two snake predators, the boa constrictior (Boa constrictor) and neotropical rattlesnake (Crotalus durissus) and a white airplane as a novel control. In the second experiment, infants, juveniles, and adults were presented photographic models of a coiled boa constrictor, rattlesnake, indigo snake (Drymarchon corais), a noncapuchin predator, and a white snake-like model. We found that antipredator behavior changed during the immature stage. Infants as young as 4 months old were able to recognize snakes and display antipredator behavior, but engaged in less snake-model discrimination than juveniles. All age classes exhibited a lower response to the white snake-like model, indicating that the absence of color and snake-scale patterns affected snake recognition. Infants also showed a higher level of vigilance after snake-model detection as exhibited by a higher proportion of time spent looking and head cocking at the models. Aggressive antipredator behavior was found in all age classes, but was more prevalent in juveniles and adults than infants. This study adds to the knowledge of development of antipredator behavior in primates by showing that, although alarm calling behavior and predator recognition appear at a very young age in capuchins, snake-species discrimination does not become apparent until the juvenile stage.

Development of snake-directed antipredator behavior by wild white-faced capuchin monkeys: II. Influence of the social environment.

Young animals are known to direct alarm calls at a wider range of animals than adults. If social cues are safer and/or more reliable to use than asocial cues for learning about predators, then it is expected that the development of this behavior will be affected by the social environment. Our study examined the influence of the social environment on antipredator behavior in infant, juvenile, and adult wild white-faced capuchin monkeys (Cebus capucinus) at Lomas Barbudal Biological Reserve in Costa Rica during presentations of different species of model snakes and novel models. We examined (a) the alarm calling behavior of the focal animal when alone versus in the vicinity of conspecific alarm callers and (b) the latency of conspecifics to alarm call once the focal animal alarm called. Focal animals alarm called more when alone than after hearing a conspecific alarm call. No reliable differences were found in the latencies of conspecifics to alarm call based on age or model type. Conspecifics were more likely to alarm call when focal individuals alarm called at snake models than when they alarm called at novel models. Results indicate (a) that alarm calling may serve to attract others to the predator's location and (b) that learning about specific predators may begin with a generalized response to a wide variety of species, including some nonthreatening ones, that is winnowed down via Pavlovian conditioned inhibition into a response directed toward specific dangerous species. This study reveals that conspecifics play a role in the development of antipredator behavior in white-faced capuchins.

Tail growth tracks the ontogeny of prehensile tail use in capuchin monkeys (Cebus albifrons and C. apella).

Physical anthropologists have devoted considerable attention to the structure and function of the primate prehensile tail. Nevertheless, previous morphological studies have concentrated solely on adults, despite behavioral evidence that among many primate taxa, including capuchin monkeys, infants and juveniles use their prehensile tails during a greater number and greater variety of positional behaviors than do adults. In this study, we track caudal vertebral growth in a mixed longitudinal sample of white-fronted and brown capuchin monkeys (Cebus albifrons and Cebus apella). We hypothesized that young capuchins would have relatively robust caudal vertebrae, affording them greater tail strength for more frequent tail-suspension behaviors. Our results supported this hypothesis. Caudal vertebral bending strength (measured as polar section modulus at midshaft) scaled to body mass with negative allometry, while craniocaudal length scaled to body mass with positive allometry, indicating that infant and juvenile capuchin monkeys are characterized by particularly strong caudal vertebrae for their body size. These findings complement previous results showing that long bone strength similarly scales with negative ontogenetic allometry in capuchin monkeys and add to a growing body of literature documenting the synergy between postcranial growth and the changing locomotor demands of maturing animals. Although expanded morphometric data on tail growth and behavioral data on locomotor development are required, the results of this study suggest that the adult capuchin prehensile-tail phenotype may be attributable, at least in part, to selection on juvenile performance, a possibility that deserves further attention.

Cranial ontogeny and sexual dimorphism in two new world monkeys: Alouatta caraya (Atelidae) and Cebus apella (Cebidae).

Pattern of skull development and sexual dimorphism was studied in Cebus apella and Alouatta caraya using univariate, bivariate, and multivariate statistics. In both species, sexual dimorphism develops because the common growth trajectory in males extends and because of differences in growth rates between sexes. The expectation that the ontogenetic bases of adult dimorphism vary interspecifically is well substantiated by this study. A. caraya exhibits transitional dimorphism in its subadult stage, although the condylobasal length, zygomatic breadth, and rostrum length are strongly dimorphic in the final adult stage, being greater in males. Most cranial measurements in C. apella exhibit significant dimorphism in the adult stage, being strongly influenced by a faster rate of growth in males. Sexual dimorphism is also evidenced through sex differences in growth rates in several cranial measurements. These results also indicate that different ontogenetic mechanisms are acting in C. apella and A. caraya and reveal differences in the way through which neotropical primates attain adult sexual dimorphism.

The ontogeny of handling hard-to-process food in wild brown capuchins (Cebus apella apella): evidence from foraging on the fruit of Maximiliana maripa.

We examined age-related differences in wild brown capuchins' foraging efficiency and the food-processing behaviors directed toward maripa palm fruit (Maximiliana maripa). A detailed comparison of the different foraging techniques showed that plucking the fruit from the infructescence constituted the main difficulty of this task. Foraging efficiency tended to increase with age, with a threshold at which sufficient strength allowed immatures by the age of three to reach adult-level efficiency. Youngsters spent more time than older individuals browsing the infructescence and pulling the fruit in an attempt to harvest it. Infants tried to compensate for their inability to pluck fruit by adopting alternative strategies but with low payback, such as gnawing unplucked fruit and opportunistically scrounging others' partially processed food. Although around 2 years of age, young capuchins exhibited all of the behaviors used by adults, they did not reach adult-level proficiency at feeding on maripa until about 3 years (older juveniles). We compared this developmental pattern with that of extractive foraging on beetle larvae (Myelobia sp.) hidden in bamboo stalks, a more difficult food for these monkeys [Gunst N, Boinski S, Fragaszy DM. Behaviour 145:195-229, 2008]. For maripa, the challenge was mainly physical (plucking the fruit) once a tree was encountered, whereas for larvae, the challenge was primarily perceptual (locating the hidden larvae). For both foods, capuchins practice for years before achieving adult-level foraging competence, and the timeline is extended for larvae foraging (until 6 years) compared with maripa (3 years). The differing combinations of opportunities and challenges for learning to forage on these different foods illustrate how young generalist foragers (i.e. exploiting a large number of animal and plant species) may compensate for their low efficiency in extractive foraging tasks by showing earlier competence in processing less difficult but nutritious foods, such as maripa fruit.

Ontogeny of long bone geometry in capuchin monkeys (Cebus albifrons and Cebus apella): implications for locomotor development and life history.

Studies of a diverse array of animals have found that young individuals often have robust bones for their body size (i.e. augmented cross-sectional dimensions), limiting fracture risk despite general musculoskeletal immaturity. However, previous research has focused primarily on precocial taxa (e.g. rodents, lagomorphs, bovids, goats and emu). In this study, we examined the ontogenetic scaling of humeral and femoral cross-sectional robusticity in a mixed-longitudinal sample of two slow-growing, behaviourally altricial capuchin monkeys. Results showed that, when regressed against biomechanically appropriate size variables (i.e. the product of body mass and bone length), humeral and femoral bending strengths generally scale with negative allometry, matching the scaling patterns observed in previous studies of more precocial mammals. Additionally, bone strength relative to predicted loads (e.g. 'safety factors') peaks at birth and rapidly decreases during postnatal growth, falling to less than 5 per cent of peak values by weaning age. We suggest that increased safety factors during early ontogeny may be an adaptation to mitigate injury from falling during initial locomotor efforts. Overall, the results presented here suggest that ontogenetic declines in relative long bone strength may represent a common pattern among mammals that is perhaps preadaptive for different purposes among different lineages.

Developmental sources of conservation and variation in the evolution of the primate eye.

Conserved developmental programs, such as the order of neurogenesis in the mammalian eye, suggest the presence of useful features for evolutionary stability and variability. The owl monkey, Aotus azarae, has developed a fully nocturnal retina in recent evolution. Description and quantification of cell cycle kinetics show that embryonic cytogenesis is extended in Aotus compared with the diurnal New World monkey Cebus apella. Combined with the conserved mammalian pattern of retinal cell specification, this single change in retinal progenitor cell proliferation can produce the multiple alterations of the nocturnal retina, including coordinated reduction in cone and ganglion cell numbers, increase in rod and rod bipolar numbers, and potentially loss of the fovea.

Intimate social behavior in infant interactions in Cebus apella.

The development and individual stability of three intimate social behaviors (Lipsmacking, Carrying Attempts, and Facial Inspection) were examined for 43 group-housed Cebus apella infants from birth to 2 years of age. Occurrence of these behaviors was scored from 10-min videotape samples recorded three times a week over that time. Frequency of Lipsmacking and Carrying Attempts by adult males, adult females, and juveniles were all highest in early months and decreased to low levels by the end of the first year. Facial Inspection of partners by infants, in contrast, first began at 3-4 months and increased over time, at least to adult males and juveniles. Correlational analyses indicated stable individual differences in these interactions with infants and outlined a relationship between these intimate behaviors and more general social patterns reported previously for these animals. Results suggest that adult males may play a special role in affording juveniles opportunities for social learning of foraging and manipulative skills.

Cortical development in brown capuchin monkeys: a structural MRI study.

Relative to other primates, Cebus monkeys display unusually fast postnatal brain growth and motor skill development. The neonatal capuchin brain, at approximately 29-34 g, is a smaller proportion of the adult brain weight (c. 50%) than is the brain of other primates except humans and great apes. Here we describe, from a cross-sectional sample, brain development in 29 brown capuchin monkeys (Cebus apella) using high-resolution structural magnetic resonance images, focusing on growth patterns in total brain volume, cortical gray and white matter volume, frontal lobe gray and white matter volume, and corpus callosum area. Non-linear age-related changes in total brain volume, cortical white matter volume and frontal white matter volume were detected from birth - 5 years. Sex differences in corpus callosum:brain ratio were also found, with males having a 10% smaller corpus callosum:brain ratio than females regardless of age. Female corpus callosum:brain ratio showed significant age-related related changes, whereas males did not display any significant changes across age. Sex differences were also found in cortical gray and frontal lobe gray matter volumes, with males having larger volumes than females. These findings support the conclusion that capuchins undergo rapid neurological change during the first few years of life.

When size makes a difference: allometry, life-history and morphological evolution of capuchins (Cebus) and squirrels (Saimiri) monkeys (Cebinae, Platyrrhini).

BACKGROUND: How are morphological evolution and developmental changes related? This rather old and intriguing question had a substantial boost after the 70s within the framework of heterochrony (changes in rates or timing of development) and nowadays has the potential to make another major leap forward through the combination of approaches: molecular biology, developmental experimentation, comparative systematic studies, geometric morphometrics and quantitative genetics. Here I take an integrated approach combining life-history comparative analyses, classical and geometric morphometrics applied to ontogenetic series to understand changes in size and shape which happen during the evolution of two New World Monkeys (NWM) sister genera. RESULTS: Cebus and Saimiri share the same basic allometric patterns in skull traits, a result robust to sexual and ontogenetic variation. If adults of both genera are compared in the same scale (discounting size differences) most differences are small and not statistically significant. These results are consistent using both approaches, classical and geometric Morphometrics. Cebus is a genus characterized by a number of peramorphic traits (adult-like) while Saimiri is a genus with paedomorphic (child like) traits. Yet, the whole clade Cebinae is characterized by a unique combination of very high pre-natal growth rates and relatively slow post-natal growth rates when compared to the rest of the NWM. Morphologically Cebinae can be considered paedomorphic in relation to the other NWM. Geometric morphometrics allows the precise separation of absolute size, shape variation associated with size (allometry), and shape variation non-associated with size. Interestingly, and despite the fact that they were extracted as independent factors (principal components), evolutionary allometry (those differences in allometric shape associated with intergeneric differences) and ontogenetic allometry (differences in allometric shape associated with ontogenetic variation within genus) are correlated within these two genera. Furthermore, morphological differences produced along these two axes are quite similar. Cebus and Saimiri are aligned along the same evolutionary allometry and have parallel ontogenetic allometry trajectories. CONCLUSION: The evolution of these two Platyrrhini monkeys is basically due to a size differentiation (and consequently to shape changes associated with size). Many life-history changes are correlated or may be the causal agents in such evolution, such as delayed on-set of reproduction in Cebus and larger neonates in Saimiri.

Transfer pathways between the ovaries and the uterus in the cebus monkeys (Cebus apella).

The aim of this work was to study, in the Cebus apella monkey, the developmental changes in the microanatomy of the utero-ovarian ligament (UOL) and whether their vascular and neural elements might be involved in the transfer of signals between the ovaries and uterus. Sections including uterus, UOL, and ovary obtained from two foetuses, two prepubertal, and four cycling monkeys, two of them treated with a neuron-axonal tracer, diamidino yellow (DY) into the corpus luteum (CL) and the remaining two into the endometrium, were analyzed for the expression of neurofilament protein (NFP) and tracer distribution. Eight regularly cycling females were used to investigate the transfer to the CL of pulses of prostaglandin F(2alpha) (PGF(2alpha)) (n=4) or its vehicle (n=4) given intra-uterus. A convoluted artery, in conjunction with various vein channels, passed over the UOL allowing for a direct communication between uterus and ovaries. The artery acquired prominence during adulthood, in a manner well suited with the ovarian status. Immunohistochemical analysis revealed that NFP expression by the oocyte and by the endometrial epithelial cells was a highly conserved feature during development, whereas the appearance of NFP fibers in the ovaries, UOL, and uterus was a late event in the ontogenesis, likely regulated by the hormonal environment. Neurons, as an obvious source for these NFP fibers, were not recognized at any developmental stage, although some neuron-like cells were observed within the CL. The pattern displayed by the tracer DY, further suggested a reciprocal axonal transport among endometrial cells and follicular and luteal cells of both ovaries and between the ovaries themselves. The functionality of the utero-ovarian connection was assessed after injecting PGF(2alpha) intra-uterus. A short exposition to PGF(2alpha) pulses was required for lowering ovarian and peripheral progesterone concentrations causing luteolysis, indicating that transport mechanism operating between uterus and ovary must be very efficient. The results suggest that the vessels and axons contained in the UOL of the Capuchin monkeys might be two combined key pathways underlying the reciprocal transfer of signals controlling utero-ovarian homeostasis.

Handedness and cortisol in tufted capuchin monkey infants.

In this research, we examined the relationship between handedness and levels of plasma cortisol in infant monkeys (Cebus apella). Specifically, we sought to test the hypothesis that stress functioning is related to hemispheric specialization and is manifested in a positive correlation between cortisol levels and the frequency of right- versus left-hand use. We found a significant relationship between stress cortisol at age 6 months and lateral bias towards greater use of the right versus left hand at ages 6 and 12 months. These data suggest an early developmental influence of stress reactivity on the emergence of hemispheric specialization for manual control in infant monkeys through the 1st year of postnatal life.

Growth and reproduction in captive tufted capuchins (Cebus apella).

We present data on weight and reproduction from a colony of tufted capuchins monkeys (Cebus apella) over a 12 year period. The data constitute a normative record for this species. Weight at birth averages 210 g, and infants gain weight rapidly. Females typically first conceived just after their fifth birthday, and males were fertile by 4 years, 5 months. Interbirth intervals average 576 days. Eighty-seven percent of live-born infants survived past 6 months. Three of eight live-born infants that died prior to 6 months succumbed from trauma inflicted by cage mates.

Effects of upright posture on hand preference for reaching vs. the use of probing tools by tufted capuchins (Cebus apella).

This research examined the effects of task (reaching vs. tool use) and posture (quadrupedal vs. bipedal) on hand preference in tufted capuchins (Cebus apella). Regarding direction of hand preference, we found a significant main effect of posture, as the bipedal stance elicited greater use of the right hand than did the quadrupedal stance, and a significant posture x task interaction, as bipedal reaching elicited greater use of the right hand than did other postural and task conditions. Further, we found a significant main effect of task on strength of hand preference, as tool use elicited more consistent use of one hand over the other than did reaching. Our findings indicate that bipedal reaching facilitates a mild right-hand bias in intensely manipulative primates. We speculate that this moderate bias may have been pushed in the direction of nearly exclusive right-hand preference in most humans with the development of complex tool use.

Relationship of early infant state measures to behavior over the first year of life in the tufted capuchin monkey (Cebus apella).

Data on activity states were collected from 29 group-housed capuchin monkey (Cebus apella) infants for 3 h each week from birth to 11 weeks of age. The amounts of time spent in sleeping/drowsy, alert-quiet, and alert-active states were measured in these subjects. Videotaped observations of these infants were recorded 3 times/week in the home cage over the first year of life and were scored for a number of social and exploratory behaviors. The extent to which early infant activity state scores predicted later behavior in the home cage was examined. Infant state measures correlated significantly with home cage behavior during months 2-6 in that infants that had been more active in early infancy spent more time alone, with other animals, and in exploration and play and less time with mothers than did quieter infants. Early state measures were less successful in predicting home cage scores beyond 8 months of age, whereas differences in behavior attributable to housing variables became more salient in the latter part of the first year. There was also a negative correlation between mother and infant activity in months 2 and 3, in that more sedentary mothers tended to have more active infants.

Efecto del GnRH combinado con destete temporal y definitivo sobre el anestro posparto en vacas cebú en el trópico húmedo / Effect of combined GnRH, temporary and definitive weaning on postpartum anestrus in Zebu cows in the humid tropics

Este experimento se efectuó con la finalidad de buscar alternativas de solución al anestro posparto en vacas Bos indicus. Se utilizaron 38 vacas Cebú Gyr e Indobrasil, entre 90 y 120 días posparto, en anestro y con buena condición corporal. Los animales se asignaron aleatoriamente a cuatro grupos: 7 vacas (Grupo A) recibieron 20 mg de bucerelina (GnRH) por vía intramuscular (im) y fueron destetadas temporalmente por 72 horas; 12 vacas (Grupo B), sólo fueron destetadas temporalmente por 72 horas; a 9 vacas (Grupo C) se les aplicó 20 mg de GnRH vía im y fueron destetadas definitivamente, y 10 vacas (Grupo D), sólo recibieron 20 mg de GnRH vía im y continuaron amamantando. Las vacas se observaron 2 veces por día para detectar estros, durante 45 días postratamiento. La inseminación artificial (IA) se realizó 12 horas después de detectado el estro. Se calcularon el intervalo tratamiento-IA (T-IA), índice de no-retorno a estro y tasa de preñez. El porcentaje de animales que presentaron estros durante el periodo fue superior en el grupo C (7/9) (P< 0.01), en contraste con los grupos D (5/10), A (2/7) y B (2/12), entre los que no fue significativa la diferencia (P> 0.05). El T-IA fue significativamente menor (P< 0.01) en el grupo C (9 ñ 2 días), en contraste con los grupos D, B y A (29 ñ 2.9, 35 ñ 6 y 52 ñ 9 días, respectivamante); entre los cuales no hubo diferencias (P> 0.05). Los índices de no-retorno a estro fueron 88.9 por ciento, 100 por ciento, 66.6 por ciento y 70 por ciento para los grupos A, B, C y D, respectivamante (P> 0.05). Se obtuvieron 28.6 por ciento (2/7), 41.7 por ciento (5/12), 22.2 por ciento (2/9) y 10 por ciento (1/10) de vacas gestantes para los grupos A, B, C y D respectivamante. La fertilidad de los servicios de IA fue de 100 por ciento para los grupos A, B y D, con contraste con el 40 por ciento en el grupo C (P< 0.01). Se concluye que la combinación de GnRH y el destete definitivo de las crías, fue el tratamiento más eficaz para disminuir la duración del anestro posparto; sin embargo, no mejoró la fertilidad a la primera inseminación