Highly polymorphic colour vision in a New World monkey with red facial skin, the bald uakari (Cacajao calvus).

Colour vision is highly variable in New World monkeys (NWMs). Evidence for the adaptive basis of colour vision in this group has largely centred on environmental features such as foraging benefits for differently coloured foods or predator detection, whereas selection on colour vision for sociosexual communication is an alternative hypothesis that has received little attention. The colour vision of uakaris (Cacajao) is of particular interest because these monkeys have the most dramatic red facial skin of any primate, as well as a unique fission/fusion social system and a specialist diet of seeds. Here, we investigate colour vision in a wild population of the bald uakari,C. calvus, by genotyping the X-linked opsin locus. We document the presence of a polymorphic colour vision system with an unprecedented number of functional alleles (six), including a novel allele with a predicted maximum spectral sensitivity of 555 nm. This supports the presence of strong balancing selection on different alleles at this locus. We consider different hypotheses to explain this selection. One possibility is that trichromacy functions in sexual selection, enabling females to choose high-quality males on the basis of red facial coloration. In support of this, there is some evidence that health affects facial coloration in uakaris, as well as a high prevalence of blood-borne parasitism in wild uakari populations. Alternatively, the low proportion of heterozygous female trichromats in the population may indicate selection on different dichromatic phenotypes, which might be related to cryptic food coloration. We have uncovered unexpected diversity in the last major lineage of NWMs to be assayed for colour vision, which will provide an interesting system to dissect adaptation of polymorphic trichromacy.

Foraging with finesse: A hard-fruit-eating primate selects the weakest areas as bite sites.

OBJECTIVES: Fruit husks are rarely uniformly hard, varying in penetrability via sulci and changes in thickness. We tested whether a hard-food specialist primate i) bites randomly on food fruit husk surfaces to access seeds, or ii) selects areas most easily penetrated by canines. We consider this would occur so as to minimize deployed mechanical force, energetic expenditure and risk of dental breakage when feeding. METHODS: A sulcus is the natural line of weakness where a dehiscent fruit breaks open. Using fruits dentally opened for seeds by golden-back uacaris (Cacajao ouakary) we: 1) analysed bite mark distribution on surface of four fruits types (hard-with-sulcus, soft-with-sulcus, hard-no-sulcus, soft-no-sulcus); 2) quantified the force needed to penetrate hard and soft fruits at sulci and elsewhere on fruit surface; 3) measured fruit wall thickness and correlated it with bite-mark distribution in all four categories of fruit. RESULTS: 1) Bite marks were distributed at random only on surfaces of soft fruits. For other fruits types, bite locations were concentrated at the thinnest areas of husk, either over the entire surface (non-sulcate fruits), or at sulci (sulcate fruits). 2) For hard-husked fruits, areas where uacaris concentrated their bites were significantly easier to penetrate than those where they did not. CONCLUSIONS: This hard-fruit feeding specialist primate is not biting at random on the surface of diet fruits. To access seeds they are focusing on those areas requiring less force to penetrate. This may be to save energy, to minimize the risk of breaking teeth used in food processing, or a combination of both. The study shows, for the first time, the subtlety by which these powerfully-jawed animals process their diet items.

Pitheciids in fragmented habitats: Land cover change and its implications for conservation.

Pitheciids (Cacajao, Callicebus, Chiropotes, and Pithecia) have experienced habitat loss and fragmentation across their geographic range in South America. Some populations living in habitat fragments live in smaller groups, travel shorter distances, and consume items that are not regularly found in the diets of populations living in continuous habitat; however, these patterns are not consistent across species. I used the IUCN Red List of Threatened Species to delineate the geographic range and conservation status of 43 pitheciid species. I calculated the amount of modified land cover within the range of each species, as well as the extent to which the remaining habitat exists in small fragments and the amount of forest lost from 2000 to 2012. Mean forest fragment size ranged from 12 to 12,027 ha, and mean forest loss from 2000 to 2012 ranged from 10.7% for Chiropotes to 0.9% for Pithecia. Critically Endangered and Endangered species represented 20.9% of the pitheciid species, and 46.5% of these species had population trends documented as decreasing. Total modified land cover was greatest for Callicebus species (18.0% of geographic range), followed by Chiropotes (13.8%), Pithecia (4.4%), and Cacajao (1.1%). Species of greater conservation concern had smaller geographic ranges, and a greater percentage of their range consisting of modified land cover than species of lower conservation concern. Species of greater conservation concern also had a greater percentage of forest lost from 2000 to 2012 and a smaller percentage of the remaining forest being protected. Most studies of pitheciids in fragments have concentrated on census data; the behavior of pitheciids in fragments has been examined for only 9 of the 43 species. Increased data on the responses of pitheciid species to forest loss and fragmentation are necessary in order to address pitheciid conservation, especially in areas undergoing severe habitat loss.

Pitheciid research comes of age: Past puzzles, current progress, and future priorities.

For a long time, members of the Pitheciidae were among the least studied of all Neotropical primates. But times have changed. Here, we trace the trajectory of this change and show how the articles in this special edition illustrate new knowledge and developments in our understanding of pitheciid ecology, behavior, and conservation. We propose new directions and priorities for future research, especially to ensure the effective conservation of pitheciids, and demonstrate how studies of this family are now the focus of hypothesis-driven research that not only allows the details of this family's biology to be explored, but will allow its biology to be compared with other primate lineages.

Proximate causes of the red face of the bald uakari monkey (Cacajao calvus).

In social species, such as primates, facial appearances transmit a variety of social signals. Although it is suggested that the intense red colour of the face of the bald uakari monkey might be an indicator of health, this hypothesis still has not been verified. This study describes the histological structure of the skin of the face in the bald uakari, compared with other non-red neotropical primates, to better understand the maintenance of its colour. The facial skin of the bald uakari monkey is characterized by a thinner epidermis, absence of melanin pigments and a high density of vascular capillaries that spread below the epidermis. These vascular capillaries are larger and more tortuous than in other neotropical primates. The skin of the face of the bald uakari monkey allows a direct external assessment of haematological status, suggesting that the colour of the face would be an honest indicator of health, but could also signal sexual or behavioural states.

Uacaries, new world monkeys of the genus Cacajao(Cebidae, Platyrrhini): A preliminary taxonomic review with the description of a new subspecies.

The two known species of uacaries, inhabitants of the upper Amazonian region, are the black head Cacajao melanocephalus with subspecies C. m. melanocephalus Humboldt and C. m. ouakary Spix, and the larger bald head uacari C. calvus with subspecies C. c. ucayalii Thomas, C. c. rubicundus I. Geoffroy and Deville, C. c. calvus I. Geoffroy, and C. c. novaesi described as new. The diagnostic generic characters described are the external, cranial, dental, some postcranial, and cytogenetic. The species are described and compared and their geographic distribution plotted with those of their subspecies delimited. Sexual differences are outlined. Apart from size-related characters, the species and subspecies are distinguished by pelage pattern of head and coloration in general. It is shown that both species could have diverged from a hairy-headed melanistic ancestral form. Pelage divergence in the descendants was expressed by the more pilose head of C. melanocephalus, and less pilose of C. calvus. Coloration differentiation was geographic and followed metachromic lines with mutation from eumelanism to partial pheomelanism (reddish or golden) in C. melanocephalus and to virtually complete pheomelanism in C. calvus. The subspecies of each species are distinguished by color patterns resulting from selective bleaching or dilution of the pheomelanin fields. The most saturate pheomelanic subspecies of C. calvus is C. c. ucayalii and the most dilute is the albinotic C. c. calvus. Correlation between coloration and environment is not evident. A gazetteer identifies all locality records plotted by numbers on the geographic distribution maps.

Locomotor behavior and skeletal morphology of two sympatric pitheciine monkeys, Pithecia pithecia and Chiropotes satanas.

Field observations of two sympatric pitheciine species reveal that the positional repertoire of the white-faced saki, Pithecia pithecia, is dominated by leaping behaviors, whereas the bearded saki, Chiropotes satanas, is predominantly quadrupedal. Examination and comparison of the postcranial skeletal morphologies and limb proportions of these species display numerous features associated with their respective locomotor behaviors. These observations accord with associations found in other primate and mammalian groups and with predictions based on theoretical and experimental biomechanics. Preliminary observations of the skeletal morphology of Cacajao calvus demonstrate a marked similarity to that of Chiropotes. The fossil platyrrhine Cebupithecia sarmientoi displays greater similarity to Pithecia, suggesting that its positional repertoire also included significant leaping and clinging behaviors.

New records and range expansion of the white bald uakari (Cacajao calvus calvus, I. Geoffroy, 1847) in Central Brazilian Amazonia.

The white bald uakari (Cacajao calvus calvus) is among the least studied of the Amazonian primates and is found exclusively in remote areas of the central Amazon. The geographic distribution of this subspecies is still uncertain, and information on current threats and its conservation status is sparse. In this paper, we identify new locations of occurrence and propose range expansion of the Cacajao calvus calvus. Between 2008 and 2010, six field expeditions were undertaken in the middle Solimões region to search for the subspecies and to conduct interviews with local residents regarding its presence. The presence of the white bald uakari was confirmed in the lower courses of the Juruá and lower Jutaí rivers, in addition to areas inside the Mamirauá Reserve, where its presence was expected. Results indicate an expansion and new limits on the geographic range of the subspecies, including its detection in areas in which it had not previously been reported and its exclusion from areas where white bald uakaris were assumed to occur. The new information provided by this study and the remaining shortcomings regarding the distribution of the calvus group point to the urgent need for further research on the geographic distribution and habitat use of this group, especially along the lower courses of the Juruá and Jutaí rivers, which remain little explored.