Neotropical Primate Species Research Articles

Cryopreservation of spermatozoa from black-and-gold howler monkeys (Alouatta caraya) using egg yolk-based or soy lecithin-based extenders.

There are more than 200 species and subspecies of Neotropical Primates of which more than 40% are listed as threatened by the IUCN Red List of Threatened Species. Both in situ and ex situ conservation programs can benefit from the use of assisted reproductive technologies. The objective of this study was to evaluate, for the first time, cryopreservation techniques for Alouatta caraya semen. Semen samples were collected from five adult males, analyzed, and frozen in either Test-egg yolk or Test-soy lecithin-based extenders containing either 3 or 4% glycerol. Frozen-thawed samples were analyzed at 10, 40, and 80min post-thaw. Egg yolk-based extenders were overall better than soy lecithin-based extenders. There was no significant difference between 3 and 4% glycerol in any of the parameters analyzed, however, 4% glycerol in egg yolk-based extender produced more favorable results for total motility, intact plasma membrane, lipidperoxidation, and DNA fragmentation index. This study brought novel information on semen characteristics and cryopreservation aspects for A. caraya, which can help shape future experiments to improve the outcome of frozen-thawed sperm for this and other species of Neotropical primates.

Review of Environmental and Health Factors Impacting Captive Common Marmoset Welfare in the Biomedical Research Setting.

As a small-bodied neotropical nonhuman primate species, common marmosets have unique requirements for adequate husbandry and veterinary care to ensure proper maintenance and to promote good animal welfare in a biomedical research setting. Environmental conditions, as well as medical and research-related manipulations, can impact marmoset welfare. Research focus areas, including basic neuroscience, transgenics, and aging, involve additional implications for marmoset welfare. This manuscript provides a comprehensive review of factors that should be considered and mitigated as needed by clinical and research staff working with marmosets in biomedical research facilities to optimize the welfare of captive marmosets.

New records of Amblyomma ticks parasitizing neotropical primates in Brazil

Amblyomma is an important tick genus for animal and human health, with some species being the vectors of zoonotic pathogens, such as Rickettsia rickettsii, in the Neotropical region. Knowing their hosts may help to understand the distribution of these agents and decrease the occurrence of clinical cases. Primates are intelligent and adaptable animals that can get close to humans in the search for food. So, they may be an important epidemiological link for the spread of these ticks. Beyond that, primates also suffer from these infections, serving as sentinels for different diseases. Thus, the present study aims to report the parasitism by Amblyomma spp. on six species of Neotropical primates from different locations in Brazil. The 337 collected ticks were morphologically identified using stereomicroscopes and taxonomic keys, and six distinct species of ticks were identified. We report here the first record of nymphs of the tick species Amblyomma cajennense sensu stricto on Alouatta belzebul, a male of Amblyomma fuscum on Alouatta guariba clamitans, nymphs of Amblyomma sculptum on Leontopithecus chrysopygus and Callithrix aurita, as well as nymphs of Amblyomma geayi on Saimiri collinsi. Of the 337 tick specimens collected, 256 (75,96%) were nymphs. The importance of primates in the life cycle of these species remains to be elucidated.

Lipid profile, apolipoproteins A-1 and B in owl monkeys (Aotus infulatus) in captivity.

Owl monkeys (Aotus infulatus) are frequently affected by heart diseases and, as in humans, dyslipidemia is one of the predisposing factors for adverse cardiovascular events. In view of this, the study of the lipid profile and plasma apolipoproteins can contribute to the clinical management of this neotropical primate species. Lipid profile as well as A-1 and B apolipoprotein values were analyzed in 60 owl monkeys, studying their relationship with body biometry and the presence of cardiac alterations. Animals suspected of having heart disease did not show significant differences (p < .05) in terms of biometry or in relation to lipid profile and apolipoproteins A-1 and B values; however, higher values of LDL and ApoB and ApoB/ApoA-1 were observed in this group. This study is the first to describe the lipid profile and apolipoprotein values in owl monkeys, and further work will be needed to better elucidate the worthiness of LDL, ApoB, and the ApoB/ApoA-1 ratio in this primate species.

Hematological reference values for Alouatta palliata (Primates: Atelidae) and Cebus imitator (Primates: Cebidae) from the Pacific Coast of Costa Rica

Introduction: Wildlife hematological patterns are fundamental for health monitoring, and allows elucidating variations both within and between populations. Among these, hematological parameters are particularly valuable to evaluate the health status of neotropical primate species in the wild. Objective: To define hematological reference values for two species of monkeys in Costa Rica. Methods: During 2014, we collected blood samples from free-ranging mantled howler monkeys, Alouatta palliata (17 females, 18 males) and white-faced capuchin monkeys, Cebus imitator (5 females, 7 males) in seven localities of the Costa Rican Pacific coast. Results: For both species, the hematological values were higher in males, and howler monkey populations differed significantly except for platelets. Conclusions: These hematological values, which differ by sex and locality, will help evaluate the health status of these neotropical primate populations.

Fur rubbing in Plecturocebus cupreus - an incidence of self-medication?

Fur rubbing, i.e. rubbing a substance or an object into the pelage, has been described in numerous Neotropical primate species, including species of titi monkeys, but it seems to be a rare behaviour. Here we describe a fur rubbing event in a wild coppery titi monkey (Plecturocebus cupreus) with Psychotria sp. (Rubiaceae) leaves observed and videotaped during a field study on vigilance behaviour between September–December 2019 in the Peruvian Amazon. Plants of the genus Psychotria contain a great diversity of secondary metabolites and are often used in traditional medicine. We suggest that the fur rubbing was an act of self-medication. This is the first record of fur rubbing in coppery titi monkeys in almost 4400 h of observation accumulated over more than 20 years.

Hematological and biochemical profile of spider monkey (Ateles geoffroyi) in captivity

Objective: To estimate the hematological and biochemical reference values inMAteles geoffroyi individuals in captivity. Methodology: Eleven males and 23 females were captured. We collected blood,from the coccygian vein; conventional techniques were used to analyze thesamples.Results: mean corpuscular volume (MCV; P &amp;lt; 0.03), platelets (PLT; P &amp;lt; 0.04) were significantly higher in females than in males. In relation to biochemical blood values wasn’t significantly in male and female groups.Limitations/Implications: hematological and biochemical reference values of A. geoffroyi are within normal health parameters, are between the ranges reported for other species of neotropical primates and can be used as a reference in for the management of the health of this species in captivity.Conclusions: hematological and biochemical parameters of captive specimens of A. geoffroyi are described, which provide reference indicators for the management of the health of the species.

Molecular detection of trypanosomatids in neotropical primates in the state of Mato Grosso, Midwest, Brazil.

Trypanosomatids are uniflagellate protozoa belonging to the Trypanosomatidae family. The genera Trypanosoma and Leishmania are of paramount importance as they contain species that cause serious diseases, such as Chagas disease and Leishmaniasis, respectively. The objective of the present study was to identify trypanosomatids present in the whole blood of free-living and captive neotropical primates in Mato Grosso State, Midwest Brazil. Between 2017 and 2019, 38 blood samples were collected from seven different neotropical primate species in seven cities in the state. Through molecular techniques, including polymerase chain reaction (PCR) to amplify a fragment of the kinetoplast DNA (kDNA) and 18S ribosomal RNA (18S rRNA) gene, sequencing, and phylogenetic analysis, nine Leishmania spp. [seven L. infantum and two L. (Leishmania) amazonensis] and two Trypanosoma spp. (T. minasense and T. rangeli) were identified. This study contributes to understanding the occurrence and epidemiology of trypanosomatids in Mato Grosso State and the importance of neotropical primates as trypanosome hosts and possible infection sources for other animals and humans. Future identification of other blood pathogens in neotropical primates will assist in disease control and prevention strategies.

Abdominal ultrasound in Saguinus ursulus.

The classification of Saguinus ursulus as a new taxon and the vulnerability of this species highlighted the need for data on its specific morphophysiological attributes. This study used ultrasound to determine the typical characteristics of pelvic-abdominal structures and organs. Nine healthy primates of the species S.ursulus were evaluated, through ultrasound tests, to determine the morphometry of the organs of the pelvic-abdominal cavity and the levels of ovarian activity. Topography, morphology, and biometrics of the organs were described. It was observed that organs of S.ursulus are similar to those of other Neotropical primate species. However, the kidney morphology is different,the left is triangular and the right is elliptical, while the gallbladder is bilobed. Ultrasonography has proven to be efficient and effective for organ evaluation. The ultrasound findings are a first step toward understanding the physiology of a less-known species.

Invalidation of taxa within the silvery wooly monkey (Lagothrix lagothricha poeppigii, Atelidae, Primates)

The systematics of the Humboldt’s wooly monkeys (L. lagothricha; Atelidae) is essential to preserve this Neotropical primate species. Traditionally, four morphological subspecies have been described, which recently have been molecularly confirmed. However, no population genetics studies have been carried out throughout the geographical distribution of one of these subspecies, Lagothrix lagothricha poeppigii. For this reason, we analyzed nine mitochondrial genes of L. l. poeppigii mainly collected from the Ecuadorian and Peruvian Amazon in order to better understand the evolutionary history of this taxon. The mitochondrial genetic diversity levels (haplotype and nucleotide diversity) we estimated are likely the highest yet reported for L. lagothricha. Our results did not detect important genetic structure within L. l. poeppigii. Furthermore, our phylogenetic analyses did not detect any relevant molecular cluster in the area where Groves hypothesized the existence of L. poeppigii castelnaui. Therefore, based on these data, castelnaui is not a valid taxon from a molecular perspective. The most differentiated subpopulation within L. l. poeppigii was from Morona-Santiago province (Ecuador) and had a genetic distance of 0.8–1.2% relative to the other subpopulations studied. However, this genetic distance range is within the variability found within a population. We estimated the mitochondrial temporal diversification within L. l. poeppigii to have occurred during the Pleistocene, 1.8–1.2 million years ago. Similarly, all our analyses detected a strong Pleistocene female population expansion for this taxon. Diverse spatial genetic analyses, perhaps with the exception of Monmonier’s Algorithm, did not detect differentiated taxa within the area analyzed for L. l. poeppigii. These genetics results could be of importance to conservation efforts to preserve this taxon as one unit.

Sperm Morphology in Neotropical Primates.

Simple SummaryThe spermatozoon is a highly differentiated cell, whose morphology has been affected throughout evolution by selective forces such as the competition between the sperm of rival males (sperm competition) and the joint evolution of male and female reproductive tracts (coevolution). The study of its morphology is important when analyzing the relationships between different species. In this contribution we analyzed new specimens and produced a database with all the spermatozoa dimensions recorded to date, comprising 75 individuals from 20 species and 8 genera, representing 2 families of neotropical primates (Cebidae and Atelidae). After an evolutionary analysis, we observed two different trends for the Cebidae and Atelidae families. Narrower and shorter spermatozoa seem to be the ancestral (oldest) form for Cebidae, with an evolutionary trend toward spermatozoa with wider and larger heads in the derived (younger) species. In Atelidae, on the contrary, narrower heads are observed in the more derived groups. We analyzed these results in the context of sperm competition and mating systems in these groups. More studies are needed to improve our knowledge of the evolution of the spermatozoa in neotropical primates.The morphological and morphometric characterization of spermatozoa has been used as a taxonomic and phylogenetic tool for different species of mammals. We evaluated and compared the sperm morphometry of five neotropical primate species: Alouatta caraya, Ateles belzebuth and Ateles chamek of family Atelidae; and Cebus cay (=Sapajus cay) and Cebus nigritus (=Sapajus nigritus) of family Cebidae. After the collection of semen samples, the following parameters were measured on 100 spermatozoa from each specimen: Head Length, Head Width, Acrosome Length, Midpiece Length, Midpiece Width and Tail Length. Considering the available literature on sperm morphometry, we gathered data of 75 individuals, from 20 species, 8 genera and 2 families. These data were superimposed on a phylogeny to infer the possible direction of evolutionary changes. Narrower and shorter spermatozoa seem to be the ancestral form for Cebidae, with a trend toward wider and larger heads in derived groups. The spermatozoa of Atelidae may show an increase in total length and midpiece length. Sperm heads would have become narrower in the more derived groups of Ateles. Sperm length may increase in the more derived species in both families. Our results are discussed in the context of sperm competition and sexual selection.

Effect of Site Attributes and Matrix Composition on Neotropical Primate Species Richness and Functional Traits: A Comparison Among Regions

Fragmentation threatens biodiversity and forest-dwelling animals can be especially vulnerable. Neotropical primates inhabit forests and play ecological roles in maintaining forest biodiversity. Currently, many primate communities are restricted to forest fragments. We (1) evaluated the influence of environmental, matrix, and site attributes on species richness and functional traits of primates in the Neotropics; and (2) evaluated the effect of the sub-region on the relationships between primates and environmental, matrix, and site attributes. We conducted literature searches to find published data on primate communities in forest fragments throughout the Neotropics. Each fragment was assigned to 1 of 11 sub-regions: Mesoamerica, Tumbes-Chocó-Magdalena, Caribbean, Orinoco, Amazon, Atlantic Forest, Cerrado, Chaco, Andes, Caatinga, and Pampa. Based on actual and expected species occurrences, we calculated the proportion of primate species retained in the fragments, the mass retained, and dietary items retained considering reproductive and vegetative plant parts and prey. We used linear mixed models to correlate primate variables with environmental, matrix, and site attributes. Fragment area was more important for primate retention than environmental, matrix, and site attributes, with primate retention being higher in larger fragments. Fragment size was positively correlated with all primate variables, except for retention of prey consumption, whose retention decreased as water bodies and density of buildings in the matrix increased. Fragments within protected areas retained larger species than unprotected fragments. The proportion of extant mass retained and vegetative plant parts in the diet were highest in Mesoamerica and lowest in the Atlantic Forest. Conservation planning of Neotropical primates should consider both the differences among sub-regions, forest restoration to increase fragment size, and the creation of new protected areas, even in fragmented landscapes.

Detection of Zika virus RNA and neutralizing antibodies in neotropical primates during the epidemic period for the disease in Brazil

Purpose: Zika virus (ZIKV) is a mosquito-borne viral disease associated with fetal microcephaly and other central nervous system (CNS) symptomatology. It was first identified in a Rhesus macaque in Uganda and later in humans (Zika fever), in 2015 ZIKV was notified in Northeast Brazil related to CNS alterations and rapid spread. Considering that old-world primates are susceptible to ZIKV, samples from neotropical primates from Ceara state, Northeast of Brazil, were preliminary tested and found to be positive for ZIKV by qPCR. The aim of this study was to extend the sampling of primates by revisiting the localities with positive animals and to study the presence of immune response to the virus. Methods & Materials: A total of 132 samples from six species of neotropical primates captured from June 2015 to December 2016 was tested, out of these, nine (six marmosets – Callithrix jacchus – and 03 capuchin monkeys – Sapajus libidinosus) were positive by quantitative RT-PCR assay. The genetic sequences showed high similarity with the strains circulating in Brazil. Neutralizing antibodies for ZIKV were detected by PRNT in two samples (PRNT50 = 73,7 and 13,2). Results: All the positive samples were obtained from peridomestic animals captured in proximity to humans and captured between the June of 2015 and February of 2016, from March to December of 2016 there were no positive samples. The temporal detection of ZIKV in the primates is in agreement with the reports and confirmations of congenital syndrome related to ZIKV in Ceara, where the majority of reports occurred from November/2015 to March/2016 with significant decrease after this period. The two animals that had neutralizing antibodies for ZIKV as indicated by PRNT were in direct or close contact with animals positive for qRT-PCR and these antibodies may constitute additional evidence for virus circulation. Conclusion: These results demonstrate the occurrence of natural ZIKV infection in neotropical primates and the temporal detection suggests that virus detection in animals accompanied the epidemic period in humans. However since some positive animals were free raging, a continuous surveillance is necessary to exclude the possibility of virus circulation and transmission in wild environments.

Parasites of Neotropical Primates: A Review

The study of parasites is of great relevance to primatology given their ecological significance and their effects on primate demography, behavior, and evolution. Moreover, assessing the vulnerability of endangered species to parasitic infections is important in developing appropriate conservation strategies. We conducted an intensive bibliographical search to synthesize the available information about the parasites of Neotropical primates. We analyzed the host and parasite taxonomic coverage of the available studies, examined the advantages and disadvantages of the diagnostic techniques employed, identified information gaps that need to be addressed, and recommend future directions in the parasitological research of Neotropical primates. Researchers have reported 276 parasite taxa, including endo- and ectoparasites, in 21 of the 22 genera of Neotropical primates. Of these, 42 parasite species have also been reported in humans, although this number may be inaccurate owing to misidentification. The parasites of 50% of Neotropical primate species are completely unknown, and 32% of the parasites recorded in these hosts have not been identified to the species level. Information regarding ectoparasites is particularly limited. We need to develop methods that enhance parasite diagnosis accuracy when using noninvasive samples, and the incorporation of molecular techniques in routine procedures should be a priority in parasitological studies of Neotropical primates. An integrative approach in which veterinarians, primatologists, and parasitologists collaborate in the identification and treatment of parasites of Neotropical primates is essential to achieve significant progress in this field.

Experimental Zika Virus Infection of Neotropical Primates.

The establishment of a sylvatic reservoir of Zika virus (ZIKV) in the Americas is dependent on the susceptibility of primates of sufficient population density, the duration and magnitude of viremia, and their exposure to the human mosquito-borne transmission cycle. To assess the susceptibility of squirrel (Saimiri sp.) and owl monkeys (Aotus sp.) to infection, we inoculated four animals of each species with ZIKV from the current epidemic. Viremia in the absence of detectible disease was observed in both species and seroconversion occurred by day 28. ZIKV was detected in the spleen of three owl monkeys: one at 7 days postinoculation (dpi) and two at 14 dpi. This study confirms the susceptibility to ZIKV infection of two Neotropical primate species that live in close proximity to humans in South America, suggesting that they could support a widespread sylvatic ZIKV cycle there. Collectively, establishment of a ZIKV sylvatic transmission cycle in South America would imperil eradication efforts and could provide a mechanism for continued exposure of humans to ZIKV infection and disease.

Seasonality, richness and prevalence of intestinal parasites of three neotropical primates (Alouatta seniculus, Ateles hybridus and Cebus versicolor) in a fragmented forest in Colombia.

Studies on parasites infecting non-human primates are essential to better understand the potential threat to humans of zoonoses transmission, particularly under the current processes of pervasive land use change and biodiversity loss. The natural ecosystems in the Middle Magdalena river basin in Colombia have suffered a dramatic reduction and transformation into pastures and agroindustrial monocultures, threatening their biodiversity, and probably affecting the dynamics between parasites and their hosts, as well as altering the disease transmission cycles between wild populations and humans. This study evaluated seasonality, prevalence and richness of intestinal parasites in three species of neotropical primates: Cebus versicolor, Ateles hybridus and Alouatta seniculus, in a fragmented forest in the Middle Magdalena river valley, Colombia. One hundred and eighty five faecal samples were collected between 2010 and 2015. Direct faecal smears were performed with saline solution (0.85%) and iodine solution (1%), in order to identify larvae and eggs based on their morphology. A large proportion of the samples examined (72.9%) was positive for intestinal parasites; seven families of nematodes were identified: Trichuridae, Trichostrongylidae, Oxyuridae, Strongyloididae, Ancylostomatidae, Ascarididae and Gnathostomatidae, two of protozoans: Entamoebidae and Balantiididae, as well as some eggs of trematodes, cestodes and acanthocephalans. Additionally, DNA extraction and sequencing were conducted on 30 faecal samples in order to identify Giardia sp. and Blastocystis hominis, two parasite species also present in humans. Molecular testing for Giardia sp. was negative and Blastocystis hominis was identified in a single sample of Alouatta seniculus. No clear patterns were observed for prevalence of intestinal parasites according to the season; nonetheless, parasite species richness was higher during the dry season. This study builds on our current understanding of intestinal parasites infecting wild neotropical primates and provides novel information on the patterns of intestinal parasites in primate communities exposed to anthropogenic disturbance.

Mycoplasma sp. infection in captive Marcgrave's capuchin monkeys (Sapajus flavius).

Three species of hemoplasmas are known to infect monkeys, 'Candidatus Mycoplasma kahanei', 'Candidatus Mycoplasma haemomacaque' and 'Candidatus Mycoplasma aoti'. Marcgrave's capuchin monkey (Sapajus flavius) is a critically endangered neotropical primate species of the Brazilian Atlantic Forest, and thus, sustained efforts are needed to protect the health and well-being of these animals. This study has aimed to screen 12 captive S. flavius from the State of Paraíba, northeastern Brazil, for hemoplasma infection. Packed cell volume (PCV) was measured and a pan-hemoplasma PCR protocol performed. A total of 8/12 (66.6%) monkeys were positive for the 16S rDNA gene of Mycoplasma sp., showing an identity of 99% to Mycoplasma sp. previously detected in Sapajus apella and Sapajus sp. monkeys from the Brazilian Amazon. Further studies should be conducted in order to elucidate whether this potentially novel Mycoplasma sp. is able to cause anemia in Sapajus sp. monkeys from Brazil.

Long-term consistency in spatial patterns of primate seed dispersal.

Seed dispersal is a key ecological process in tropical forests, with effects on various levels ranging from plant reproductive success to the carbon storage potential of tropical rainforests. On a local and landscape scale, spatial patterns of seed dispersal create the template for the recruitment process and thus influence the population dynamics of plant species. The strength of this influence will depend on the long‐term consistency of spatial patterns of seed dispersal. We examined the long‐term consistency of spatial patterns of seed dispersal with spatially explicit data on seed dispersal by two neotropical primate species, Leontocebus nigrifrons and Saguinus mystax (Callitrichidae), collected during four independent studies between 1994 and 2013. Using distributions of dispersal probability over distances independent of plant species, cumulative dispersal distances, and kernel density estimates, we show that spatial patterns of seed dispersal are highly consistent over time. For a specific plant species, the legume Parkia panurensis, the convergence of cumulative distributions at a distance of 300 m, and the high probability of dispersal within 100 m from source trees coincide with the dimension of the spatial–genetic structure on the embryo/juvenile (300 m) and adult stage (100 m), respectively, of this plant species. Our results are the first demonstration of long‐term consistency of spatial patterns of seed dispersal created by tropical frugivores. Such consistency may translate into idiosyncratic patterns of regeneration.

Ulcerative and granulomatous enteritis associated with Molineus torulosus parasitism in neotropical primates

ABSTRACT: This paper reports eleven cases of ulcerative and granulomatous enteritis associated with Molineus torulosus parasitism in different species of neotropical primates of the Sapajus genus. All of the affected monkeys had been apprehended by the environmental police and were being treated in a rehabilitation center for wild animals. The clinical history was weight loss and debility. During the necropsy, several nodules were found on the duodenum and proximal jejunum wall, with ulcers on the adjacent intestinal mucosa, including the nodules in the pancreas of four monkeys. Histologically, eosinophilic granulomas were observed in the small intestine, associated with fibrosis, eggs and adult models of Trichostrongylidae, etiology consistent with Molineus torulosus. This study describes the first cases of parasitism in Sapajus flavius, a species previously considered extinct, but recently rediscovered, and presents the occurrence of M. torulosus in two other species, Sapajus libidinosus and Sapajus apella.

Sperm Morphology Assessment in Captive Neotropical Primates.

The main objective of this study was to evaluate sperm morphology in four neotropical primate species to compare the sperm morphological traits and the sperm morphometric parameters as a basis for establishing normative sperm standards for each species. Data from 80 ejaculates collected from four primate species, Callithrix jacchus, Callimico goeldii, Alouatta caraya and Ateles geoffroyi, were analysed for detection of sperm morphological alterations using subjective World Health Organization (WHO-2010) standards and Sperm Deformity Index (SDI) criteria, objective computer-assisted sperm morphometry analysis (CASMA) and subpopulation sperm determination (SSD) methods. There were multiple differences (p<0.01) observed among primate species in values obtained from WHO-2010, SDI, CASMA and SSD sperm analysis methods. In addition, multiple significant positive and negative correlations were observed between the sperm morphological traits (SDI, Sperm Deformity Index Head Defects, Sperm Deformity Index Midpiece Defects, Sperm Deformity Index Tail Defects, Normal Sperm, Head Defects, Midpiece Defects and Tail Defects) and the sperm morphometric parameters (SSD, Area (A), Perimeter (P), Length (L), Width (W), Ellipticity, Elongation and Rugosity) (p≤0.046). In conclusion, our findings using different evaluation methods indicate that pronounced sperm morphological variation exists among these four neotropical primate species. Because of the strong relationship observed among morphological and morphometric parameters, these results suggest that application of objective analysis methods could substantially improve the reliability of comparative studies and help to establish valid normative sperm values for neotropical primates.