Yellow Fever as Cause of Death of Titi Monkeys (Callicebus Spp.)

From 2016 to 2018, an epidemic wave of yellow fever (YF) occurred in Brazil, affecting a large number of Platyrrhini monkeys. Titi monkeys ( Callicebus spp.) were severely affected yet pathological characterizations are lacking. This study characterized epizootic YF in 43 titi monkeys ( Callicebus spp.) with respect to the microscopic lesions in liver, kidney, spleen, heart, brain, and lung, as well as the distribution of immunolabeling for YF virus antigen, and the flaviviral load in the liver. Of 43 titi monkeys examined, 18 (42%) were positive for yellow fever virus (YFV) by immunohistochemistry or reverse transcription quantitative real-time polymerase chain reaction (RT-qPCR). Affected livers had consistent marked panlobular necrotizing hepatitis, lipidosis, and mild inflammation, with intense immunolabeling for YFV mainly in centrilobular hepatocytes (zone 1; P = .05). In the spleen, consistent findings were variable lymphoid depletion (10/11), lymphoid necrosis (lymphocytolysis; 4/11), and immunolabeling for YFV in histiocytic cells (3/16). The main finding in the kidney was multifocal acute necrosis of tubular epithelium (5/7) that was occasionally associated with intracytoplasmic immunolabeling for YFV (6/15). These data indicate that titi monkeys are susceptible to YFV infection, developing severe hepatic lesions and high viral loads, comparable to humans and Alouatta spp. Thus, Callicebus spp. may be reliable sentinels for YF surveillance.

Titi monkey neophobia and visual abilities allow for fast responses to novel stimuli

The Snake Detection Theory implicates constricting snakes in the origin of primates, and venomous snakes for differences between catarrhine and platyrrhine primate visual systems. Although many studies using different methods have found very rapid snake detection in catarrhines, including humans, to date no studies have examined how quickly platyrrhine primates can detect snakes. We therefore tested in captive coppery titi monkeys (Plecturocebus cupreus) the latency to detect a small portion of visible snake skin. Because titi monkeys are neophobic, we designed a crossover experiment to compare their latency to look and their duration of looking at a snake skin and synthetic feather of two lengths (2.5 cm and uncovered). To test our predictions that the latency to look would be shorter and the duration of looking would be longer for the snake skin, we used survival/event time models for latency to look and negative binomial mixed models for duration of looking. While titi monkeys looked more quickly and for longer at both the snake skin and feather compared to a control, they also looked more quickly and for longer at larger compared to smaller stimuli. This suggests titi monkeys’ neophobia may augment their visual abilities to help them avoid dangerous stimuli.

Musical calling as a behavior ancestral to all modern primates

Music is a singular behavior humans exhibit via the creation of patterned sounds organized, for example, along rhythmic and melodic dimensions. Music-like behavior, however, also appears in many other animals including non-human primates. Calls with western musical attributes are primarily ascribed to species of gibbon, tarsier, indri, and potentially also marmoset, tamarin, and titi monkeys. A recent survey of primates, using a continuous measure of acoustic musicality, suggests that many other species—including galagos, several lemurs, and some old-world monkeys—also exhibit calls with music-like qualities. Based on this ubiquity and a recent arboreal-origins theory for musical behavior, I hypothesized that the ancestor of all living primates was likewise also somewhat musical. Ancestral character estimation was used to reconstruct ancestral phylogenetic states using scored spectrographic depictions of vocalizations of extant primates (n=58 species) to determine if musical calling is the initial primate condition. The results suggest that nearly all primate families have an ancestor with at least one moderately music-like call—two or more reappearing syllables—with the clear exception of Cercopithecine. These cheek-pouch monkeys likely experienced a multi-million year diminution in musical behavior, perhaps in conjunction with their recent adaptations for quadrupedal terrestriality. These findings largely indicate that exhibition of at least one music-like call is a normal, and likely quite ancient, constituent of primate vocalization behavior.

Potential self-medication by brown titi monkeys, <i>Plecturocebus brunneus</i>, in an urban fragment forest in the Brazilian Amazon

In this study, we report fur-rubbing behavior of brown titi monkeys, Plecturocebus brunneus, using chewed leaves from (Fabaceae) and Piper tuberculatum (Piperaceae). These reports were obtained during systematic monitoring of titi monkeys from May until December 2019 (218 h) in an urban fragment forest in the Brazilian Amazon. Both plant species contain chemical substances in their leaves that potentially repel ectoparasites. The genus Piper is known for its repelling action due to the presence of amides, alkaloids and benzoic acid. The presence of dogs, cats and human settlements may contribute to an increase of ectoparasites, making a potential self-medication function of fur rubbing in this primate species plausible.

Genetic monogamy and mate choice in a pair-living primate

In pair-living mammals, genetic monogamy is extremely rare. One possible reason is that in socially monogamous animals, mate choice can be severely constrained, increasing the risk of inbreeding or pairing with an incompatible or low-quality partner. To escape these constraints, individuals might engage in extra-pair copulations. Alternatively, inbreeding can be avoided by dispersal. However, little is known about the interactions between mating system, mate choice, and dispersal in pair-living mammals. Here we genotyped 41 wild individuals from 14 groups of coppery titi monkeys (Plecturocebus cupreus) in Peruvian Amazon using 18 microsatellite loci. Parentage analyses of 18 young revealed no cases of extra-pair paternity, indicating that the study population is mostly genetically monogamous. We did not find evidence for relatedness- or heterozygosity-based mate choice. Despite the lack of evidence for active inbreeding avoidance via mate choice, mating partners were on average not related. We further found that dispersal was not sex-biased, with both sexes dispersing opportunistically over varying distances. Our findings suggest that even opportunistic dispersal, as long as it is not constrained, can generate sufficient genetic diversity to prevent inbreeding. This, in turn, can render active inbreeding avoidance via mate choice and extra-pair copulations less necessary, helping to maintain genetic monogamy.