Opportunistic meat-eating by urban folivorous-frugivorous monkeys.

The consumption of vertebrate tissues and eggs (hereinafter "meat") is relatively common among some primates that are highly frugivorous or eclectic omnivores, but rare or absent in those that are highly folivorous. The Neotropical howler monkeys (Alouatta spp.) belong in the latter group. Here we report the consumption of meat by free-ranging urban black and gold howler monkeys (Alouatta caraya) and discuss the potential role of the consumed meat as a source of energy, protein, or micronutrients. We studied three groups of howler monkeys (comprising four to seven individuals), living in city squares (0.6, 1.5, and 1.9 ha) in south Brazil, from July 2022 to May 2023 (65 days; 797 h of observations). All of the study groups were spontaneously supplemented daily by people with variable amounts and types of food provided. Meat was only offered in the two larger squares. The groups' diets included leaves (42-49% scan sampling feeding records), fruit (3-20%), and flowers (2-5%) from 13 to 20 plant species, and considerable amounts of supplemented food (27-50%). We recorded 33 individual events of ingestion of supplemented cooked meat, three individual events of dove egg predation, and three bird nest inspections without egg consumption. All members of the two groups in the larger squares, except an infant male, ingested meat at least once. Meat accounted for 1% of total scan feeding records of both groups with access to this supplement. We conclude that whereas the opportunistic consumption of meat probably contributed only minor amounts of energy and protein to the study subjects, it may have benefitted them with micronutrients that are scarce in plant foods.

Molecular identification of Leishmania in free-ranging black and gold howler monkeys (Alouatta caraya) in northeastern Argentina.

Parasitological surveys of non-human primates provides an important opportunity to better understand the epidemiology, transmission dynamics and emergence risk of anthropozoonoses such as leishmaniasis, which affect human populations in several regions accross South America. Our study area, in northeastern Argentina, can be considered a southern marginal region for the presence of leishmaniases and includes the habitat of black and gold howler monkeys, Alouatta caraya. To evaluate if A. caraya serve as potential hosts in the Leishmania cycle, we used molecular methods to examine infection by Leishmania spp. in 109 howler monkeys of different ages captured between July and August 2010. External ear tissue samples were subjected to PCR amplification for the Leishmania ribosomal internal transcribed spacer (ITS-1) and a RFLP assay with the Hae III restriction enzyme, and finally confirmed by sequencing. Nine howler monkeys (8.3%) were infected with Le. braziliensis (2.8%), Le. amazonensis (2.8%) and/or Le. infantum (3.7%). The results also suggest a case of co-infection between Le. braziliensis and Le. amazonensis. Further, we report the first observation of Le. amazonensis in the northeastern region of Argentina. The detection of Leishmania spp. in free-ranging howler monkeys gives rise to questions about the actual prevalence of the parasite in the wild, as well as if the number of infected wild monkeys detected may present a risk of leishmaniasis emergence in surronding human populations. Anyway, the presence of Leishmania spp. in A. caraya suggests the possible importance of these monkeys in the sylvatic and periurban transmission.

Morphological and molecular characterization of Bertiella sp. (Cestoda, Anoplocephalidae) infection in a human and howler monkeys in Argentina.

Bertiella sp. is a typical parasite in non-human primates and only a few cases of bertiellosis have been reported in humans. We present a new case study of bertiellosis in a 42-year-old woman caretaker of howler monkeys in a wild rehabilitation center in Argentina. Bertiella sp. infection was also diagnosed in the monkeys. Proglottids and feces were collected from the caretaker and monkeys; the samples were submitted for parasitological examination by morphological characterization and molecular identification using both nuclear (18S and ITS1-5.8-ITS2 rDNA) and mitochondrial (cox1) markers. Morphological and molecular data were consistent and allowed the classification of the specimen to the genus level. The analyses also showed the presence of cysts of Giardia lamblia and oocysts of Cryptosporidium spp. in howler monkeys, and cysts of Blastocystis sp. in both the caretaker and monkeys. This study recorded the fourth case of bertiellosis in a human host from Argentina and the eighth case in South America. Moreover, this is the first study that compares the morphological and molecular features of Bertiella sp. found in both a human and monkeys from the same geographical region. These results suggest that the cohabitation between humans and monkeys increases the opportunities of infection by Bertiella sp. and other potential zoonotic parasites.

Adoption of an orphaned and temporarily captive infant by an unrelated adult female in black-and-gold howler monkey: implications for management strategies.

Conservation behavior involves the application of general principles of animal behavior for solving conservation problems. In primates, adoption of infants has been reported in several species and consists of an individual other than the biological parents taking primary care of them. Based on cases of adoption reported in howler monkeys (genus Alouatta), in the present study we facilitated the adoption of an orphaned and temporarily captive male infant by an unrelated adult female black-and-gold howler monkey (A. caraya), in the wild. The adoption process involved presenting the orphaned infant, inside a cage, to the female in the forest fragment that she occupied. We recorded the interactions between the individuals, and decided to open the cage. The female became the sole caregiver of the orphan, providing him with protection, transportation, and feeding, although she did not nurse him. The follow-up of these same individuals between 2006 and 2007 confirmed the success of the adoption. These findings indicate that carefully managed adoption can be a possible management strategy for the conservation and the welfare of howler monkeys in both nature and captivity.

Social play among black and gold howler monkey (Alouatta caraya) immatures during intergroup encounters.

We studied intergroup social play (IGSP) among immatures in wild black and gold howler monkeys (Alouatta caraya) in northeastern Argentina. IGSP events are one form of affiliative interaction that can occur during intergroup encounters. The main goal of this study was to analyze IGSP in A. caraya immatures and assess how intrinsic (e.g., age and sex) and extrinsic (e.g., seasonality) factors can influence the development of this type of social behavior. We followed 12 groups between 2008 and 2015 and recorded 182 encounters and 61 events of IGSP. Considering the composition of play partners, most IGSP events occurred among juveniles of both sexes (33%), followed by juveniles that were only-male (31%), and finally between mixed-sex juveniles and infants (20%) interactions. Additionally, most IGSP events occurred mainly in summer (56%), followed by spring (29%), with fewer events occurring in autumn (15%) and no IGSP events recorded in winter. Our results suggest that IGSP constitutes a beneficial activity in wild A. caraya that promotes behavioral flexibility, where immatures acquire social skills, such as tolerance, by interacting with unknown individuals. Moreover, the higher participation of young males in IGSP is consistent with the fact that adult black and gold howler males tend to be more actively involved in group encounters than females, supporting the hypothesis that social play provides benefits in the development of motor and social skills. Finally, seasonality in the frequencies of IGSP might be related to availability of foods with high and easily mobilized energy content in summer and spring.

Molecular characterization of trypanosomatid infections in wild howler monkeys (Alouatta caraya) in northeastern Argentina.

The transmission of Trypanosoma cruzi by vectors is confined to the Americas, and the infection circulates in at least two broadly defined transmission cycles occurring in domestic and sylvatic habitats. This study sought to detect and characterize infection by T. cruzi and other trypanosomes using PCR strategies in blood samples from free-ranging howler monkeys, Alouatta caraya, in the northeastern Argentina. Blood samples were collected at four sites with variable levels of habitat modification by human activity. PCR was conducted using primers for kinetoplast DNA, satellite DNA and ribosomal DNA of the trypanosomatid parasites. Ribosomal and satellite DNA fragments were sequenced to identify the trypanosomatid species and to characterize the discrete typing units (DTUs) of T. cruzi. Overall, 46% (50/109) of the howlers were positive according to the kDNA-PCR assay, but only 7 of the howlers were positive according to the SatDNA-PCR protocol. We sequenced the amplicons of the satellite DNA obtained from five specimens, and the sequences were 99% and 100% similar to T. cruzi. A sequence typical of DTU T. cruzi I was found in one howler monkey from the "remote" site, while sequences compatible with DTUs II, V, and VI were found in howlers from the "remote", "rural" and "village" sites. We detected 96% positive samples for RibDNA-PCR, 9 of which were sequenced and displayed 99% identity with Trypanosoma minasense, while none showed identity with T. cruzi. The results demonstrated the presence of T. cruzi and a species closely related to T. minasense in blood samples from free-ranging A. caraya, belonging to different T. cruzi DTUs circulating in these howler monkey populations. The results obtained in this study could help evaluate the role of A. caraya as a reservoir of T. cruzi in regions where Chagas disease is hyper-endemic and where the human-wildlife interface is increasing.

Determinants of daily path length in black and gold howler monkeys (Alouatta caraya) in northeastern Argentina.

Models used to explain the social organization of primates suggest that variation in daily path length (DPL) is a response to variation in resource distribution and the intensity of intragroup feeding competition. However, daily path length may be affected by a number of other factors including the availability and distribution of nutritionally complementary food items, temperature which can influence activity budget, patterns of subgrouping, and the frequency and function of intergroup encounters. In this 6-month study (total 495 hr of quantitative data), we examined daily path lengths in two neighboring groups of black and gold howler monkeys (Alouatta caraya) inhabiting a semi-deciduous gallery forest in San Cayetano (27° 30'S, 58° 41'W), in the northwest province of Corrientes, Argentina. Both study groups were of similar size and composition. We identified relationships across groups between time spent feeding on fruits, leaves, and flowers, the number of trees visited, group spread, frequency of intergroup encounters, mean daily temperature, and DPL. Our results suggest that variation in food availability had a significant impact on howler ranging behavior by increasing DPL under conditions of high immature and mature fruit availability, and by decreasing DPL with increased availability and increased time invested in feeding on mature leaves. These results do not support the contention that a reduction in food availability or an increase in within-group feeding competition increased DPL in black and gold howler monkeys. DPL in black and gold howlers is influenced by several interrelated factors. In this regard we suggest that models of socio-ecology and ecological constraints need to reconsider how factors such as individual nutritional requirements, social tolerance and group cohesion, and the spatial and temporal availability of preferred and nearby food resources influence primate ranging behavior. Am. J. Primatol. 78:825-837, 2016. © 2016 Wiley Periodicals, Inc.

How do demographic and social factors influence parent-offspring conflict? The case of wild black and gold howler monkeys (Alouatta caraya).

In this study, we examined the influence of demography and social context on mother-offspring conflict in wild black and gold howler monkeys (Alouatta caraya) inhabiting two nearby sites in northern Argentina, one comprising continuous forest and one fragmented forest. These sites differed in population density (3.25 vs. 1.04 individuals/ha), degree of home range overlap between neighboring groups (70 vs. 31%), and rate of intergroup encounters (2 vs. 0.02-1 encounters/day), though not in interbirth interval or rate of infant mortality. During a 27-month study (September 2008 through November 2010), we observed 37 mother-offspring dyads across the two sites. We found a very similar pattern of mother-offspring conflict in both populations; specifically, the sites did not differ in any of the variables used to characterize the mother-offspring relationship (the time spent in contact, the rate at which the mother makes and breaks contact, the rate at which the infant breaks contact, the rate of maternal rejection, and signs of infant distress) except one (the rate at which the infant makes contact). Although mother-offspring conflict is a dynamic process that varies over time, our results suggest that the different demographic and social contexts found at the two study sites did not have a marked effect on quantitative aspects of the mother-offspring relationship in these populations of black and gold howlers. Finally, this study suggests that the environmental variability (ecological, demographic, and social traits) leads to a set of strategies used both by infants and mothers with a main goal of conflict resolution, with mothers specifically aiming to cope with the tradeoff between current and future reproduction.

Comprehensive characterization of evolutionary conserved breakpoints in four New World Monkey karyotypes compared to Chlorocebus aethiops and Homo sapiens.

Comparative cytogenetic analysis in New World Monkeys (NWMs) using human multicolor banding (MCB) probe sets were not previously done. Here we report on an MCB based FISH-banding study complemented with selected locus-specific and heterochromatin specific probes in four NWMs and one Old World Monkey (OWM) species, i.e. in Alouatta caraya (ACA), Callithrix jacchus (CJA), Cebus apella (CAP), Saimiri sciureus (SSC), and Chlorocebus aethiops (CAE), respectively. 107 individual evolutionary conserved breakpoints (ECBs) among those species were identified and compared with those of other species in previous reports. Especially for chromosomal regions being syntenic to human chromosomes 6, 8, 9, 10, 11, 12 and 16 previously cryptic rearrangements could be observed. 50.4% (54/107) NWM-ECBs were colocalized with those of OWMs, 62.6% (62/99) NWM-ECBs were related with those of Hylobates lar (HLA) and 66.3% (71/107) NWM-ECBs corresponded with those known from other mammalians. Furthermore, human fragile sites were aligned with the ECBs found in the five studied species and interestingly 66.3% ECBs colocalized with those fragile sites (FS). Overall, this study presents detailed chromosomal maps of one OWM and four NWM species. This data will be helpful to further investigation on chromosome evolution in NWM and hominoids in general and is prerequisite for correct interpretation of future sequencing based genomic studies in those species.

Extra group copulation in alouatta caraya (primates, atelidae) living on an island of urban forest from southeast São Paulo, Brazil

Extra group copulations are rarely observed among the Alouatta genus, which lives in a fragmented area in Brazil. Here, we describe the second extra group copulation in A. caraya in literature, which was the first from Brazil. This happened in the southeast urban island forest, which measures 25 ha. In this forest there are two troops: one of them with thirteen howlers and the other with four. These howlers may be extinct in a few years since in the region there is only 3.89 % of native forests and high anthropic action due to agribusiness. We discuss the possible issues that led to the extra group copulation.

Cópulas extra grupo raramente são observados em animais do gênero Alouatta, que vivem em áreas fragmentadas do Brasil. Aqui, descrevemos a segunda cópula extra grupo em A. caraya na literatura, que foi a primeira do Brasil. Isso aconteceu na floresta ilha urbana sudeste, que mede 25 ha. Nesta floresta existem dois bandos: um deles com treze bugios e o outro com quatro. Estes bugios podem ser extintos em poucos anos, uma vez que na região há apenas 3,89% de florestas nativas e alta ação antrópica, devido ao agronegócio. Nós discutimos os possíveis aspectos que levaram à cópula extra grupo.

Extra group copulation in Alouatta caraya (Primates, Atelidae) living on an island of urban forest from southeast São Paulo, Brazil

Extra group copulations are rarely observed among the Alouatta genus, which lives in a fragmented area in Brazil. Here, we describe the second extra group copulation in A. caraya in literature, which was the first from Brazil. This happened in the southeast urban island forest, which measures 25 ha. In this forest there are two troops: one of them with thirteen howlers and the other with four. These howlers may be extinct in a few years since in the region there is only 3.89 % of native forests and high anthropic action due to agribusiness. We discuss the possible issues that led to the extra group copulation.(AU)

Cópulas extra grupo raramente são observados em animais do gênero Alouatta, que vivem em áreas fragmentadas do Brasil. Aqui, descrevemos a segunda cópula extra grupo em A. caraya na literatura, que foi a primeira do Brasil. Isso aconteceu na floresta ilha urbana sudeste, que mede 25 ha. Nesta floresta existem dois bandos: um deles com treze bugios e o outro com quatro. Estes bugios podem ser extintos em poucos anos, uma vez que na região há apenas 3,89% de florestas nativas e alta ação antrópica, devido ao agronegócio. Nós discutimos os possíveis aspectos que levaram à cópula extra grupo.(AU)

Ultraestrutura comparativa da língua do sagui-de-tufo-preto (Callithrix penicillata) e do bugio-preto (Alouatta caraya) em diferentes faixas etárias / Comparative ultrastructure of the tongue of black-tufted-ear-marmoset (Callithrix penicillata) and black-howler-monkey (Alouatta caraya) in different age groups

Para a análise e descrição comparativa da morfologia da língua e de suas papilas, bem como a distribuição destas, foram utilizados três animais de faixas etárias distintas (filhote, jovem, adulto), de duas espécies de primatas, Callithrix penicillata (sagui-de-tufo-preto) e Alouatta caraya (bugio-preto), ambas sendo observadas através da microscopia eletrônica de varredura. Os animais da espécie Callithrix penicillata eram procedentes de um criadouro comercial de animais selvagens em Atibaia/SP e vieram a óbito por causas naturais, e os da espécie Alouatta caraya eram provenientes do acervo do Laboratório de Anatomia Macroscópica da Faculdade de Medicina Veterinária e Zootecnia da Universidade de São Paulo (FMVZ-USP). Com o material analisado e a técnica empregada pôde-se constatar que as línguas dos saguis-de-tufo-preto e dos bugios-pretos analisadas apresentavam papilas linguais similares às descritas para outras espécies de primatas. As línguas possuíam diferenças morfológicas, principalmente para alguns tipos de papilas linguais, em detrimento do avançar da idade dos animais. De forma geral, foram observados quatro tipos de papilas linguais, sendo estas: filiforme, fungiforme, valada e folhada. As línguas dos bugio-pretos apresentavam características de animais com dietas herbívoras. Possuindo desta forma papilas filiformes com formatos variados (coroa, lança, multifilamentar), de acordo com as regiões da língua, e também robustas papilas, principalmente na proeminência lingual. Já as línguas dos saguis-de-tufo-preto possuíam características de animais onívoros. Com papilas filiformes em formato de coroa, grandes quantidades de papilas fungiformes e desenvolvidas papilas folhadas. Observou-se que as modificações das papilas linguais que ocorrem nos animais após o nascimento apresentaram correlação com a mudança nos tipos de alimentos consumidos. Sendo presumível então concluir que as dietas possuem relação direta para com as alterações morfológicas e estruturais das papilas linguais nos animais ora aqui analisados.

For the comparative analysis and description of the morphology of the tongue and taste buds as well as the distribution of these we have used three animals of different age groups (puppy, young adult), of two species of primate, Callithrix penicillata (black-tufted-ear-marmoset) and Alouatta caraya (black-howler-monkey), both being observed by scanning electron microscopy. The animals of the species Callithrix penicillata were from a commercial breeding of wild animals in Atibaia-SP and they had died of natural causes, and the specie Alouatta caraya were from the collection of Macroscopic Anatomy Laboratory of Faculty of Veterinary Medicine and Animal Science University of São Paulo (FMVZ-USP). With the material analyzed and the technique employed could be seen that the tongue of black-tufted-ear-marmosets and black-howler-monkeys had examined lingual papillae similar to those described for other primate species. The tongue has morphological differences, especially for some types of lingual papillae, at the expense of advancing age of the animals. Overall, we found four types of lingual papillae, which are: filiform, fungiform, vallate and litter. The tongues of the black-howler-monkey had characteristics of animals with herbivorous diets. Possessing this way with the filiform papillae varied formats (crown, spear, multifilament), according to the regions of the tongue, and also robust taste, especially in the lingual prominence. Since the tongues of the black-tufted-ear-marmosets owned features of omnivorous animals. With filiform-shaped crown, large amounts of fungiform papillae and foliate papillae developed. It was observed that the changes of tongue papillae that occur in animals after birth correlated with the change in the types of foods consumed. Being suspected then conclude that diets have direct relation to the morphological and structural of the lingual papillae now here in the animals analyzed.

A study of a black howling monkey (Alouatta caraya) population in northern Argentina.

A population of Alouatta caraya in northern Argentina had an ecological density of 130 animals per km2 . Mean troop size varied from 7.2 to 8.9 individuals, and the ratio of adult males to adult females from 0.58 to 0.51. Infants comprised from 6% to 14% of the population, juveniles from 16% to 21%. These percentages probably vary seasonally in response to a birth peak at the beginning of the dry season. Males were age-graded in multi-male troops. Sexual dimorphism was extreme in this species. Males were all black and averaged 6.7 kg; females were yellow-brown and averaged 4.4 kg. Juvenile males retained the pelage color of the female until approximately 4.5 yr of age and 5 kg in weight. No genital mimicry or exaggeration occurred in this species. Vocalizations of A. caraya were similar to those of A. seniculus, both of which tend to be lower pitched than those of A. palliata.