Capuchin monkey tool use: Overview and implications

Nutcracking capuchins are mentioned in reports dating as far back as the sixteenth century,(1,2) as well as in Brazilian folklore.(3) However, it was barely a decade ago that primatologists ""discovered"" the spontaneous use of stones to crack nuts in a semi-free ranging group of tufted capuchin monkeys. Since then, we have found several more capuchin populations in savanna-like environments which(5-7) employ this form of tool use. The evidence so far only weakly supports geneti cally based behavioral differences between populations and does not suggest that dietary pressures in poor environments are proximate determinants of the likelihood of tool use. Instead, tool use within these capuchin populations seems to be a behavioral tradition that is socially learned and is primarily associated with more terrestrial habits. However, differences in the diversity of ""tool kits"" between populations remain to be understood.

Anatomical and radiographic appearance of the capuchin monkey thoracic cavity (Cebus apella)

The capuchin monkey is widespread both north and south of the Legal Amazon and in the Brazilian cerrado. Ten clinically healthy capuchin monkeys were submitted to an anatomical and radiographic study of their thoracic cavities. The radiographic evaluation allowed the description of biometric values associated with the cardiac silhouette and thoracic structures. Application of the VHS (vertebral heart size) method showed positive correlation (P<0.05) with depth of the thoracic cavity, as well as between the body length of vertebrae T 3, T 4, T 5 and T 6 and the cardiac length and width. The lung fields showed a diffuse interstitial pattern, more visible in the caudal lung lobes and a bronchial pattern in the middle and cranial lung lobes. The radiographic examination allowed preliminary inferences to be made concerning the syntopy of the thoracic structures and modifiication of the pulmonary patterns and cardiac anatomy for the capuchin monkey.

Intrinsic organization of the suprachiasmatic nucleus in the capuchin monkey

The suprachiasmatic nucleus (SCN), which is the main circadian biological clock in mammals, is composed of multiple cells that function individually as independent oscillators to express the self-sustained mRNA and protein rhythms of the so-called clock genes. Knowledge regarding the presence and localization of the proteins and neuroactive substances of the SCN are essential for understanding this nucleus and for its successful manipulation. Although there have been advances in the investigation of the intrinsic organization of the SCN in rodents, little information is available in diurnal species, especially in primates. This study, which explores the pattern of expression and localization of PER2 protein in the SCN of capuchin monkey, evaluates aspects of the circadian system that are common to both primates and rodents. Here, we showed that PER2 protein immunoreactivity is higher during the light phase. Additionally, the complex organization of cells that express vasopressin, vasoactive intestinal polypeptide, neuron-specific nuclear protein, calbindin and calretinin in the SCN, as demonstrated by their immunoreactivity, reveals an intricate network that may be related to the similarities and differences reported between rodents and primates in the literature.

Cone photopigment variations in Cebus apella monkeys evidenced by electroretinogram measurements and genetic analysis

We investigated the color vision pattern in Cebus apella monkeys by means of electroretinogram measurements (ERG) and genetic analysis. Based on ERG we could discriminate among three types of dichromatic males. Among females, this classification is more complex and requires additional genetic analysis. We found five among 10 possible different phenotypes, two trichromats and three dichromats. We also found that Cebus present a new allele with spectral peak near 552 nm, with the amino acid combination SFT at positions 180, 277 and 285 of the opsin gene, in addition to the previously described SYT, AFT and AFA alleles. (C) 2009 Elsevier Ltd. All rights reserved.

PREPARATORY EMG ACTIVITY REVEALS A RAPID ADAPTATION PATTERN IN HUMANS PERFORMING LANDING MOVEMENTS IN BLINDFOLDED CONDITION

The main questions addressed in this work were whether and how adaptation to suppression of visual information occurs in a free-fall paradigm, and the extent to which vision availability influences the control of landing movements. The prelanding modulation of EMG timing and amplitude of four lower-limb muscles was investigated. Participants performed six consecutive drop-landings from four different heights in two experimental conditions: with and without vision. Experimental design precluded participants from estimating the height of the drop. Since cues provided by proprioceptive and vestibular information acquired during the first trials were processed, the nervous system rapidly adapted to the lack of visual information, and hence produced a motor output (i.e., prelanding EMG modulation) similar to that observed when performing the activity with vision available.

Characterization of Opsin Gene Alleles Affecting Color Vision in a Wild Population of Titi Monkeys (Callicebus brunneus)

The color vision of most platyrrhine primates is determined by alleles at the polymorphic X-linked locus coding for the opsin responsible for the middle- to long-wavelength (M/L) cone photopigment. Females who are heterozygous at the locus have trichromatic vision, whereas homozygous females and all males are dichromatic. This study characterized the opsin alleles in a wild population of the socially monogamous platyrrhine monkey Callicebus brunneus (the brown titi monkey), a primate that an earlier study suggests may possess an unusual number of alleles at this locus and thus may be a subject of special interest in the study of primate color vision. Direct sequencing of regions of the M/L opsin gene using feces-, blood-, and saliva-derived DNA obtained from 14 individuals yielded evidence for the presence of three functionally distinct alleles, corresponding to the most common M/L photopigment variants inferred from a physiological study of cone spectral sensitivity in captive Callicebus. Am. J. Primatol. 73:189-196, 2011. (C) 2010 Wiley-Liss, Inc.

Using the Hard, Randy, and Rittler Test to Evaluate Color Vision in Capuchins (Cebus libidinosus)

The identification of color vision types in primates is fundamental to understanding the evolution and biological function of color perception. The Hard, Randy, and Rittler (HRR) pseudoisochromatic test categorizes human color vision types successfully. Here we provide an experimental setup to employ HRR in a nonhuman primate, the capuchin (Cebus libidinosus), a platyrrhine with polymorphic color vision. The HRR test consists of plates with a matrix composed of gray circles that vary in size and brightness. Differently colored circles form a geometric shape (X, O, or Delta) that is discriminated visually from the gray background pattern. The ability to identify these shapes determines the type of dyschromatopsy (deficiency in color vision). We tested six capuchins in their own cages under natural sunlight. The subjects chose between two HRR plates in each trial: one with the gray pattern only and the other with a colored shape, presented on the left or right side at random. We presented the test 40 times and calculated the 95 % confidence limits for chance performance based on the binomial test. We also genotyped all subjects for exons 3 and 5 of the X-linked opsin genes. The HRR test diagnosed two subjects as protan dichromats (missing or defective L-cone), three as deutan dichromats (missing or defective M-cone), and one female as trichromat. Genetic analysis supported the behavioral data for all subjects. These findings show that the HRR test can be applied to diagnose color vision in nonhuman primates.

ELECTROCARDIOGRAPHIC PARAMETERS OF CAPTIVE TUFTED CAPUCHINS (CEBUS APELLA) UNDER CHEMICAL IMMOBILIZATION

This study presents the electrocardiogram findings from 97 captive tufted capuchin monkeys (Cebus apella) at the Sao Paulo Zoo (Sao Paulo, Brazil) while under ketamine anesthesia. The results did not differ greatly from data of domestic carnivores or other studied primate species. The most common rhythm recorded was normal sinus rhythm, followed by normal sinus rhythm with wandering pacemaker. Electrical axis varied from 0 degrees to -150 degrees but was most commonly between +60 degrees and +90 degrees. QRS complexes were predominantly positive in leads DI, DII, DIII, and AVF. These findings allow for the recognition of abnormal rhythms in these primate species and can contribute to future investigations into the cardiovascular diseases routinely diagnosed in primates and humans.

Permanent anosmia and ageusia after resection of a left temporoinsular low-grade glioma: anatomofunctional considerations

Five percent of the general population has olfactory or gustatory disorders, although most do not complain about it. However, in some cases, these symptoms can be disabling and may affect quality of life. Anosmia was reported as a possible complication following head injury and neurosurgical procedures, particularly after the resection of tumors located in the anterior fossa and the treatment of aneurysms in the anterior circulation. Nonetheless, in all of these situations, olfactory dysfunction could be explained by damage to the peripheral olfactory system. Here, the authors report a case of complete anosmia associated with ageusia following awake resection of a low-grade glioma involving the left temporoinsular region, with no recovery during a follow-up of 3 years. The frontal lobe was not retracted, and the olfactory tract was not visualized during surgery; therefore, postoperative anosmia and ageusia are likely explained by damage to the cortex and central pathways responsible for these senses. The authors suggest that the patient might have had a subclinical right hemianosmia before surgery, which is a common condition. After resection of the central structures critical for smell and taste processing in the left hemisphere, the patient could have finally had bilateral and complete olfactory and gustatory loss. This is the first known report of permanent anosmia and ageusia following glioma surgery. Because these symptoms might have been underestimated, more attention should be devoted to olfaction and taste, especially with regard to possible subclinical preoperative deficit. (http://thejns.org/doi/abs/10.3171/2012.2.JNS111982)

Laminar Displacement and Prelaminar Tissue Thickness Change after Glaucoma Surgery Imaged with Optical Coherence Tomography

PURPOSE. To study changes in lamina cribrosa position and prelaminar tissue thickness (PTT) after surgical IOP reduction in glaucoma patients. METHODS. Twenty-two patients (mean age, 71.4 years) were imaged with spectral domain optical coherence tomography (SD-OCT; 24 radial B-scans centered on the optic nerve head [ONH]) before trabeculectomy or tube shunt implantation. Follow up images were acquired 1 week, 1 month, 3 months, and 6 months postsurgery. Bruch's membrane opening (BMO), the internal limiting membrane (ILM) and the anterior laminar surface (ALS) were segmented in each radial scan with custom software. Surfaces were fitted to the ILM and ALS with the extracted three-dimesional coordinates. PTT was the distance between the ILM and ALS, perpendicular to a BMO reference plane. Serial postsurgical laminar displacement (LD), relative to the BMO reference plane, and changes in PTT were measured. Positive values indicated anterior LD. RESULTS. Mean (SD) presurgery IOP was 18.1 (6.5) mm Hg, and reduced by 4.7 (5.5), 2.4 (7.7), 7.0 (6.2), and 6.8 (7.5) mm Hg at 1 week, 1 month, 3 months, and 6 months postsurgery, respectively. At the four postsurgery time points, there was significant anterior LD (1.8 [9.5], -1.1 [8.9], 8.8 [20.2], and 17.9 [25.8] mu m) and PTT increase (1.7 [13.3], 2.4 [11.9], 17.4 [13.7], and 13.9 [18.6] mu m). LD was greater in ONHs with larger BMO area (P = 0.01) and deeper ALS (P = 0.04); however, PTT was not associated with any of the tested independent variables. CONCLUSIONS. Both anterior LD and thickening of prelaminar tissue occur after surgical IOP reduction in patients with glaucoma. (Invest Ophthalmol Vis Sci. 2012;53:5819-5826) DOI:10.1167/iovs.12-9924

Anointing variation across wild capuchin populations: a review of material preferences, bout frequency and anointing sociality in Cebus and Sapajus

The frequency of anointing bouts and the materials used for self- and social anointing vary across capuchin species in captivity, but there is little published data on capuchin anointing in the wild. Here we present previously unpublished data on anointing behaviors from capuchin monkey populations at ten different field sites and incorporate these data into a review of the anointing literature for captive and wild capuchins. Using a comparative phylogenetic framework, we test four hypotheses derived primarily from captive literature for variation in anointing between wild untufted capuchins (Cebus) and tufted capuchins (Sapajus), including that (1) the frequency of anointing is higher in Cebus, (2) Cebus uses a higher proportion of plant species to insect species for anointing compared with Sapajus, (3) anointing material diversity is higher in Cebus, and (4) social indices of anointing are higher in Cebus. We found that wild Cebus anoints more with plant parts, including fruits, whereas wild Sapajus anoints more with ants and other arthropods. Cebus capucinus in particular uses more plant species per site for anointing compared with other capuchins and may specialize in anointing as an activity independent from foraging, whereas most other capuchin species tend to eat the substances they use for anointing. In agreement with captive studies, we found evidence that wild Cebus anoints at a significantly higher frequency than Sapajus. However, contrary to the captive literature, we found no difference in the range of sociality for anointing between Cebus and Sapajus in the wild. We review anointing in the context of other Neotropical primate rubbing behaviors and consider the evidence for anointing as self-medication; as a mechanism for enhanced sociality; and as a behavioral response to chemical stimuli. Am. J. Primatol. 74:299314, 2012. (c) 2011 Wiley Periodicals, Inc.

Pilot survey of expressed sequence tags (ESTs) from the asexual blood stages of Plasmodium vivax in human patients

Abstract Background Plasmodium vivax is the most widely distributed human malaria, responsible for 70–80 million clinical cases each year and large socio-economical burdens for countries such as Brazil where it is the most prevalent species. Unfortunately, due to the impossibility of growing this parasite in continuous in vitro culture, research on P. vivax remains largely neglected. Methods A pilot survey of expressed sequence tags (ESTs) from the asexual blood stages of P. vivax was performed. To do so, 1,184 clones from a cDNA library constructed with parasites obtained from 10 different human patients in the Brazilian Amazon were sequenced. Sequences were automatedly processed to remove contaminants and low quality reads. A total of 806 sequences with an average length of 586 bp met such criteria and their clustering revealed 666 distinct events. The consensus sequence of each cluster and the unique sequences of the singlets were used in similarity searches against different databases that included P. vivax, Plasmodium falciparum, Plasmodium yoelii, Plasmodium knowlesi, Apicomplexa and the GenBank non-redundant database. An E-value of <10-30 was used to define a significant database match. ESTs were manually assigned a gene ontology (GO) terminology Results A total of 769 ESTs could be assigned a putative identity based upon sequence similarity to known proteins in GenBank. Moreover, 292 ESTs were annotated and a GO terminology was assigned to 164 of them. Conclusion These are the first ESTs reported for P. vivax and, as such, they represent a valuable resource to assist in the annotation of the P. vivax genome currently being sequenced. Moreover, since the GC-content of the P. vivax genome is strikingly different from that of P. falciparum, these ESTs will help in the validation of gene predictions for P. vivax and to create a gene index of this malaria parasite.

A new species of Callicebus Thomas, 1903 (Primates, Pitheciidae) from the states of Mato Grosso and Pará, Brazil

A new species of titi monkey, genus Callicebus Thomas, 1903, is described based on four individuals, one from a small tributary of the left bank of Rio Teles Pires, northern state of Mato Grosso, and three others from Largo do Souza, Rio Iriri, Pará, Brazil. The new species belongs to the Callicebus moloch species group, and the main diagnostic characteristics of the new species are the whitish forehead, sideburns and beard coloration, which are contiguous, forming a frame around the blackish face; overall body pelage coloration is pale grayish-brown agouti; hands, feet and tip of the tail whitish; belly and inner sides of fore and hind limbs uniformly orange. The pattern of pelage coloration and qualitative and quantitative skull morphology are described and compared to the other species of the Callicebus moloch group. Species of the Callicebus moloch group show great similarity in skull morphology and morphometrics, making the external morphological characters, specially the chromatic fields, the most reliable diagnostic trait to identify the species.

Cytoprotective role of heme oxygenase-1 and heme degradation derived end products in liver injury

The activation of heme oxygenase-1 (HO-1) appears to be an endogenous defensive mechanism used by cells to reduce inflammation and tissue damage in a number of injury models. HO-1, a stress-responsive enzyme that catabolizes heme into carbon monoxide (CO), biliverdin and iron, has previously been shown to protect grafts from ischemia/reperfusion and rejection. In addition, the products of the HO-catalyzed reaction, particularly CO and biliverdin/bilirubin, have been shown to exert protective effects in the liver against a number of stimuli, as in chronic hepatitis C and in transplanted liver grafts. Furthermore, the induction of HO-1 expression can protect the liver against damage caused by a number of chemical compounds. More specifically, the CO derived from HO-1-mediated heme catabolism has been shown to be involved in the regulation of inflammation; furthermore, administration of low concentrations of exogenous CO has a protective effect against inflammation. Both murine and human HO-1 deficiencies have systemic manifestations associated with iron metabolism, such as hepatic overload (with signs of a chronic hepatitis) and iron deficiency anemia (with paradoxical increased levels of ferritin). Hypoxia induces HO-1 expression in multiple rodent, bovine and monkey cell lines, but interestingly, hypoxia represses expression of the human HO-1 gene in a variety of human cell types (endothelial cells, epithelial cells, T cells). These data suggest that HO-1 and CO are promising novel therapeutic molecules for patients with inflammatory diseases. In this review, we present what is currently known regarding the role of HO-1 in liver injuries and in particular, we focus on the implications of targeted induction of HO-1 as a potential therapeutic strategy to protect the liver against chemically induced injury.