Rhesus Macaque Macaca mulatta (Mammalia: Primates: Cercopithecidae) in a human-modified landscape: population, activity budget, and societal perceptions in Bangladesh

Rhesus Macaques are widely distributed and ecologically diverse primate species that attract special focus from the research and conservation approaches. We studied population, activity budget, and societal perceptions of Rhesus Macaque at Old Dhaka City, Bangladesh from March 2015 to February 2016. Total count was used to determine the group size and composition. Daily activity budgets of Rhesus Macaques were studied using scan sampling method. Questionnaire survey was conducted to know the attitudes of local people towards monkey conservation in the area. Seven groups with a total of 169 individuals were recorded. The population density was 15.5 individuals/ km² and group size ranged from 8 to 63 individuals. Rhesus Macaque spent most of their time in resting (38.5%) followed by feeding (25.7%), moving (18.4%), grooming (12.8%), and playing or object manipulation (4.6%). There was a significant variation in each behavioral activity among the age-sex classes. Questionnaire survey revealed that property damage was the main problem created by the monkeys. A significant majority of people (83.4%) held a positive outlook toward conservation of this species. Variables such as religion, education, and occupation of the respondents significantly influenced their opinion about conservation. These findings have implications for not only conservation and management interventions of Rhesus Macaque but also helpful for minimizing human-monkey interactions in urban areas.

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Spondyloarthritis in Taihangshan Macaques (Macaca mulatta tcheliensis)

Folia Primatologica ◽

10.1159/000519338 ◽

2021 ◽

pp. 1-8

Author(s):

Ke-Li Pang ◽

Qin-Qin Jin ◽

Zan-An Yuan ◽

Zhen-Jing Kuang ◽

Ji-Qi Lu ◽

...

Keyword(s):

Ankylosing Spondylitis ◽

Rhesus Macaque ◽

Macaca Mulatta ◽

Nature Reserve ◽

Rhesus Macaques ◽

Pubic Symphysis ◽

Primate Species ◽

Human Beings ◽

Captive Populations ◽

Nonhuman Primate Species

The rhesus macaque (<i>Macaca mulatta</i>) is the most widely distributed nonhuman primate species, and captive populations play an important role in biomedical research due to close phylogenetic and physiological similarity to human beings. However, to our best knowledge, the spondyloarthritis (SpA) in rhesus macaques has been exclusively reported in captive or semicaptive populations rather than wild counterparts. In the present study, we report 2 cases of SpA observed in Taihangshan macaques (<i>Macaca mulatta tcheliensis</i>) inhabiting the Taihangshan Macaque National Nature Reserve, Henan Province, China. Among these 2 cases, one can be diagnosed as ankylosing spondylitis (AS) following accepted medical criteria, and another case showed evident fusion at the pubic symphysis which could be specific to rhesus macaque AS. We discuss the potential causes leading directly or indirectly to the development of SpA.

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The Antiviral Activity of the Cellular Glycoprotein LGALS3BP/90K Is Species Specific

Journal of Virology ◽

10.1128/jvi.00226-18 ◽

2018 ◽

Vol 92 (14) ◽

Cited By ~ 7

Author(s):

Veronika Lodermeyer ◽

George Ssebyatika ◽

Vânia Passos ◽

Aparna Ponnurangam ◽

Angelina Malassa ◽

...

Keyword(s):

Amino Acid ◽

Antiviral Activity ◽

Rhesus Macaque ◽

Rhesus Macaques ◽

Single Amino Acid ◽

Primate Species ◽

Target Cells ◽

Amino Acid Exchange ◽

Hiv 1 ◽

Acid Exchange

ABSTRACT Cellular antiviral proteins interfere with distinct steps of replication cycles of viruses. The galectin 3 binding protein (LGALS3BP, also known as 90K) was previously shown to lower the infectivity of nascent human immunodeficiency virus type 1 (HIV-1) virions when expressed in virus-producing cells. This antiviral effect was accompanied by impaired gp160Env processing and reduced viral incorporation of mature Env glycoproteins. Here, we examined the ability of 90K orthologs from primate species to reduce the particle infectivity of distinct lentiviruses. We show that 90K's ability to diminish the infectivity of lentiviral particles is conserved within primate species, with the notable exception of 90K from rhesus macaque. Comparison of active and inactive 90K orthologs and variants uncovered the fact that inhibition of processing of the HIV-1 Env precursor and reduction of cell surface expression of HIV-1 Env gp120 are required, but not sufficient, for 90K-mediated antiviral activity. Rather, 90K-mediated reduction of virion-associated gp120 coincided with antiviral activity, suggesting that 90K impairs the incorporation of HIV-1 Env into budding virions. We show that a single “humanizing” amino acid exchange in the BTB (broad-complex, tramtrack, and bric-à-brac)/POZ (poxvirus and zinc finger) domain is sufficient to fully rescue the antiviral activity of a shortened version of rhesus macaque 90K, but not that of the full-length protein. Comparison of the X-ray structures of the BTB/POZ domains of 90K from rhesus macaques and humans point toward a slightly larger hydrophobic patch at the surface of the rhesus macaque BTB domain that may modulate a direct interaction with either a second 90K domain or a different protein. IMPORTANCE The cellular 90K protein has been shown to diminish the infectivity of nascent HIV-1 particles. When produced in 90K-expressing cells, particles bear smaller amounts of the HIV-1 Env glycoprotein, which is essential for attaching to and entering new target cells in the subsequent infection round. However, whether the antiviral function of 90K is conserved across primates is unknown. Here, we found that 90K orthologs from most primate species, but, surprisingly, not from rhesus macaques, inhibit HIV-1. The introduction of a single amino acid exchange into a short version of the rhesus macaque 90K protein, consisting of the two intermediate domains of 90K, resulted in full restoration of antiviral activity. Structural elucidation of the respective domain suggests that the absence of antiviral activity in the rhesus macaque factor may be linked to a subtle change in protein-protein interaction.

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Serotonin pathway gene–gene and gene–environment interactions influence behavioral stress response in infant rhesus macaques

Development and Psychopathology ◽

10.1017/s0954579409990241 ◽

2010 ◽

Vol 22 (1) ◽

pp. 35-44 ◽

Cited By ~ 28

Author(s):

Erin L. Kinnally ◽

Genesio M. Karere ◽

Leslie A. Lyons ◽

Sally P. Mendoza ◽

William A. Mason ◽

...

Keyword(s):

Stress Response ◽

High Risk ◽

Emotional Reactivity ◽

Rhesus Macaques ◽

Behavioral Activity ◽

Risk Alleles ◽

Behavioral Stress ◽

Gene Environment ◽

Social Separation ◽

Infant Rhesus

AbstractA subset of serotonin (5-HT) pathway polymorphisms has been shown to confer risk for psychological dysfunction, particularly in individuals who experience early adversity. Understanding the developmental processes underlying these Gene × Environment interactions will strengthen the search for risk factors for behavioral dysfunction. We investigated the combined influence of two serotonin pathway polymorphisms and species-atypical, and possibly adverse, rearing (nursery rearing [NR]) on two dimensions of behavioral stress response in infant rhesus macaques. We hypothesized that the experience of NR and possession of both “high-risk” genotypes (genotypes that are thought to confer low 5-HT function) would predict the greatest behavioral stress response to maternal/social separation. Using a matched-pair design, the impact of early experience and the serotonin transporter (rh5-HTTLPR) and monoamine oxidase A (rhMAO-A-LPR) promoter polymorphisms on behavioral reactivity of 136 infant rhesus macaques (90–120 days of age) during a 25-hr social separation/relocation procedure was assessed. Each pair included one infant reared with mother in a large, outdoor field enclosure (field rearing) and one infant reared in a nursery (NR). Pairs were matched for putative gene activity of each polymorphism, sex, age, and weight at testing. Behavioral responses in a “human intruder” test were recorded, and activity and emotional reactivity composites were created to detect different aspects of psychological adaptation to stress. Our hypothesis that high-risk groups would be the most reactive to stress was not entirely borne out. Rh5-HTTLPR × rhMAOA-LPR interactions predicted emotional reactivity and tended to predict behavioral activity scores. Carriers of the two “low-risk” alleles exhibited the lowest behavioral activity, as might be predicted, but carriers of both “high-risk” alleles were two of four genotype groups exhibiting the highest observed Emotional Reactivity. Gene × Gene interactions were exacerbated by the experience of nursery rearing, as predicted, however. Finally, we suggest that genetic or environmental factors may mitigate the risk for behavioral dysregulation illustrated in the patterns of behavioral activity and emotional reactivity displayed by infants.

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Ecological aspects of black-pincelled marmoset (Callithrix penicillata) in the cerradão and dense cerrado of the Brazilian Central Plateau

Brazilian Journal of Biology ◽

10.1590/s1519-69842001000300008 ◽

2001 ◽

Vol 61 (3) ◽

pp. 397-404 ◽

Cited By ~ 37

Author(s):

G. H. B. de MIRANDA ◽

D. S. de FARIA

Keyword(s):

Home Range ◽

Group Size ◽

Rainy Season ◽

Botanical Garden ◽

Primate Species ◽

Ecological Data ◽

Central Plateau ◽

Bird Eggs ◽

Different Seasons ◽

Gallery Forests

Ecological data about three free-ranging groups of C. penicillata (black-pincelled marmoset) were observed between March and December 1996, in one cerradão patch (in the Ecological Reserve of Brazilian Institute of Geography and Statistics, RECOR) and two patches of dense cerrado (one in the Recor and another in the Botanical Garden of Brasília, JBB), situated in the APA (area of environmental protection) of the Gama/Cabeça-de-Veado, Distrito Federal. Each area was visited weekly during three periods of two months -- end of the rainy season (01/04 to 31/05), dry season (16/06 to 15/08) and beginning of the rainy season (14/10 to 15/12) -- and instantaneous scan records at fifteen minute intervals were made for the vertical and horizontal position of each visible individual of the target group. The group size ranged between 4 and 11 elements. In September, the birth of twins in both groups of the Recor was observed. Home-range varied from 8.25 to 18.5 hectares, while density ranged from 0.4 to 0.82 ind/ha. Twenty two species of nine tree families were identified as exudate sources. Qualea grandiflora (Vochysiaceae), Vochysia thyrsoidea (Vochysiaceae), Scheflera macrocarpum (Araliaceae) and Qualea parviflora (Vochysiaceae) were more explored. Fruits (14 species, two of which were exotics), nectar, honey, arthropods (mainly orthopterans) and bird eggs complete their diet. The main sleep-tree species was Emmotum nitens (Icacinaceae). Data from different seasons and studied groups/areas were compared along previous data from this primate species in gallery forests. In the cerradão and dense cerrado areas C. penicillata had a similar group size, however a larger home-range and smaller density than in gallery forests were observed in this study.

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Age-Related Changes in the Rhesus Macaque Eye

10.1101/2021.07.14.452427 ◽

2021 ◽

Author(s):

Kira Lin ◽

Tu Tran ◽

Soohyun Kim ◽

Sangwan Park ◽

Jiajia Chen ◽

...

Keyword(s):

Optical Coherence Tomography ◽

Intraocular Pressure ◽

Rhesus Macaque ◽

Axial Length ◽

Rhesus Macaques ◽

Anterior Segment ◽

Optical Coherence ◽

Lens Thickness ◽

Age Related ◽

Age Related Changes

Purpose: To assess age-related changes in the rhesus macaque eye and evaluate them to corresponding human age-related eye disease. Methods: Data from eye exams and imaging tests including intraocular pressure (IOP), lens thickness, axial length, and retinal optical coherence tomography (OCT) images were evaluated from 142 individuals and statistically analyzed for age-related changes. Quantitative autofluorescence (qAF) was measured as was the presence of macular lesions as related to age. Results: Ages of the 142 rhesus macaques ranged from 0.7 to 29 years (mean=16.4 years, stdev=7.5 years). Anterior segment measurements such as IOP, lens thickness, and axial length were acquired. Advanced retinal imaging in the form of optical coherence tomography and qAF were obtained. Quantitative assessments were made and variations by age groups were analyzed to compare with established age-related changes in human eyes. Quantitative analysis of data revealed age-related increase in intraocular pressure, ocular biometry (lens thickness and axial length), and presence of macular lesions. Age-related changes in thicknesses of retinal layers on OCT were observed and quantified. Age was correlated with increased qAF. Conclusions: The rhesus macaque has age-related ocular changes similar to humans. IOP increases with age while retinal ganglion cell layer thickness decreases. Macular lesions develop in some aged animals. Our findings support the concept that rhesus macaques may be useful for the study of important age-related diseases such as glaucoma, macular diseases, and cone disorders, and for development of therapies for these diseases.

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Isolation, Maintenance and Differentiation of Primary Tracheal Basal Cells from Adult Rhesus Macaque

Methods and Protocols ◽

10.3390/mps2040079 ◽

2019 ◽

Vol 2 (4) ◽

pp. 79

Author(s):

Anna E. Engler ◽

Gustavo Mostoslavsky ◽

Lisa Miller ◽

Jason R. Rock

Keyword(s):

Rhesus Macaque ◽

Rhesus Macaques ◽

Enzymatic Digestion ◽

Basal Cells ◽

Early Passage ◽

Long Term Storage ◽

Air Liquid Interface ◽

Nonadherent Cells ◽

Level 2

In this report, we describe methodologies for the isolation and culture of primary rhesus macaque tracheal basal cells, their cryopreservation, long term storage and differentiation. These are comparable to state-of-the-art protocols that have been developed for mouse and human airway basal cells. This method is based on the use of proprietary media, providing an easily reproducible and applicable protocol for usage in biosafety level 2 (BSL2) settings. Tracheas from rhesus macaques were isolated after animal euthanasia and subjected to enzymatic digestion overnight. Cells of the epithelial layer were scraped off of the trachea for cell culture. Twenty-four hours after plating basal cells had attached and nonadherent cells were removed. First passages of basal cells can be frozen for early passage storage in liquid nitrogen or propagated and differentiated on an air–liquid interface and in a tracheosphere assay up to passage seven. This protocol provides a platform for the analysis of basal cells from a close evolutionary relative to humans.

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Effect of Group Size and Individual Characteristics on Intergroup Encounters in Primates

International Journal of Primatology ◽

10.1007/s10764-019-00119-5 ◽

2020 ◽

Vol 41 (2) ◽

pp. 325-341 ◽

Cited By ~ 6

Author(s):

Bonaventura Majolo ◽

Aurora deBortoli Vizioli ◽

Laura Martínez-Íñigo ◽

Julia Lehmann

Keyword(s):

Group Size ◽

Dominance Rank ◽

Individual Characteristics ◽

Primate Species ◽

New World Monkeys ◽

Older Individuals ◽

Data Set ◽

Unequal Distribution ◽

Intergroup Encounters ◽

Group 2

AbstractIntergroup encounters are common in nonhuman primates and can vary from affiliative to aggressive. We extracted data from the literature to test five different hypotheses: 1) where there are group size differences between opposing groups, whether the larger group is more likely to win an intergroup encounter than the smaller group; 2) whether the likelihood of a group engaging in aggressive intergroup encounters increases with group size; and 3–5) whether dominant, older individuals, and/or males are more likely to participate aggressively in intergroup encounters than subordinate, younger individuals and/or females. Our data set comprised 52 studies on 31 primate species (3 lemur species, 5 New World monkeys, 19 Old World monkeys, and 4 apes). We found that the larger group is more likely to win an encounter against a smaller group than vice versa. We found no significant relationship between group size and propensity to be aggressive during intergroup encounters. We found weak/no support for the effect of age, dominance rank, and sex on the frequency of aggression displayed toward outgroup individuals during intergroup encounters. Species- and population-specific differences in inter- and intragroup competition and in the degree of the unequal distribution of resources across group members may explain why age, dominance rank, and sex are not strong predictors of aggression during intergroup encounters.

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Anti-α4β7 monoclonal antibody–conjugated nanoparticles block integrin α4β7 on intravaginal T cells in rhesus macaques

Science Advances ◽

10.1126/sciadv.abb9853 ◽

2020 ◽

Vol 6 (34) ◽

pp. eabb9853

Author(s):

Sidi Yang ◽

Geraldine Arrode-Bruses ◽

Ines Frank ◽

Brooke Grasperge ◽

James Blanchard ◽

...

Keyword(s):

Monoclonal Antibody ◽

T Cells ◽

Single Dose ◽

Side Effects ◽

Rhesus Macaque ◽

Rhesus Macaques ◽

Vaginal Infection ◽

Macaque Model ◽

Immunodeficiency Virus ◽

Vaginal Tract

Intravenous administration of anti-α4β7 monoclonal antibody in macaques decreases simian immunodeficiency virus (SIV) vaginal infection and reduces gut SIV loads. Because of potential side effects of systemic administration, a prophylactic strategy based on mucosal administration of anti-α4β7 antibody may be safer and more effective. With this in mind, we developed a novel intravaginal formulation consisting of anti-α4β7 monoclonal antibody–conjugated nanoparticles (NPs) loaded in a 1% hydroxyethylcellulose (HEC) gel (NP-α4β7 gel). When intravaginally administered as a single dose in a rhesus macaque model, the formulation preferentially bound to CD4+ or CD3+ T cells expressing high levels of α4β7, and occupied ~40% of α4β7 expressed by these subsets and ~25% of all cells expressing α4β7. Blocking of the α4β7 was restricted to the vaginal tract without any changes detected systemically.

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128 MITOCHONDRIAL DNA DELETIONS IN RHESUS MACAQUE OOCYTES, EMBRYOS, AND ADULT AND EMBRYONIC STEM CELLS

Reproduction Fertility and Development ◽

10.1071/rdv18n2ab128 ◽

2006 ◽

Vol 18 (2) ◽

pp. 173

Author(s):

T. Gibson ◽

T. Quebedeaux ◽

S. Rajasekaran ◽

C. Brenner

Keyword(s):

Skeletal Muscle ◽

Stem Cells ◽

Mitochondrial Dna ◽

Embryonic Stem Cells ◽

Rhesus Macaque ◽

Rhesus Macaques ◽

Embryonic Stem ◽

Immature Oocytes ◽

Mtdna Deletions ◽

Common Deletion

Mitochondria are the most abundant organelles in mammalian oocytes and early embryos. Previous data have shown that mitochondrial DNA (mtDNA) deletions are present both in human oocytes and in embryos from in vitro fertilization (IVF) patients and suggest that accumulation of these deletions may contribute to mitochondrial dysfunction and impaired ATP production. In addition, high levels of mitochondrial mutations are present in skeletal muscle fibers from aged rhesus macaques. The specific aims of this study were to determine whether the mitochondrial common deletion is present in non-human primate oocytes and embryos generated by IVF and to determine whether mtDNA mutations are already present in immature oocytes from rhesus ovaries. Using a nested primer polymerase chain reaction (PCR) strategy, we determined the frequency of the rhesus common deletion in immature oocytes compared with stimulated oocytes and embryos. There was a low incidence (21%) of the rhesus common deletion present in immature, unstimulated oocytes derived from necropsied ovaries of 2 to 10-yr-old rhesus macaques. However, there was >3-fold increase (71.4%) in the frequency of deleted mtDNA in stimulated oocytes and IVF embryos from age-matched fertile monkeys. We postulated that, in addition to skeletal muscle, a similar time-dependent accumulation of mtDNA deletions occurs in fertile rhesus macaque oocytes and embryos. We are now investigating the effects of culture and passage number on mtDNA deletions in primate adult and embryonic stem cells. We propose the rhesus monkey to be an excellent model to assess the quality of gametes and embryos, as well as stem cells, and their developmental competence in human and non-human primates. This study was supported by National Institutes of Health grants RR15395 and HD045966.

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The multinomial index: a robust measure of reproductive skew

Proceedings of The Royal Society B Biological Sciences ◽

10.1098/rspb.2020.2025 ◽

2020 ◽

Vol 287 (1936) ◽

pp. 20202025

Author(s):

Cody T. Ross ◽

Adrian V. Jaeggi ◽

Monique Borgerhoff Mulder ◽

Jennifer E. Smith ◽

Eric Alden Smith ◽

...

Keyword(s):

Group Size ◽

Social Evolution ◽

Natural Populations ◽

R Package ◽

Reproductive Skew ◽

Primate Species ◽

Highly Sensitive ◽

Highly Nonlinear ◽

Population Comparisons ◽

Negative Effect

Inequality or skew in reproductive success (RS) is common across many animal species and is of long-standing interest to the study of social evolution. However, the measurement of inequality in RS in natural populations has been challenging because existing quantitative measures are highly sensitive to variation in group/sample size, mean RS, and age-structure. This makes comparisons across multiple groups and/or species vulnerable to statistical artefacts and hinders empirical and theoretical progress. Here, we present a new measure of reproductive skew, the multinomial index, M , that is unaffected by many of the structural biases affecting existing indices. M is analytically related to Nonacs’ binomial index, B , and comparably accounts for heterogeneity in age across individuals; in addition, M allows for the possibility of diminishing or even highly nonlinear RS returns to age. Unlike B , however, M is not biased by differences in sample/group size. To demonstrate the value of our index for cross-population comparisons, we conduct a reanalysis of male reproductive skew in 31 primate species. We show that a previously reported negative effect of group size on mating skew was an artefact of structural biases in existing skew measures, which inevitably decline with group size; this bias disappears when using M . Applying phylogenetically controlled, mixed-effects models to the same dataset, we identify key similarities and differences in the inferred within- and between-species predictors of reproductive skew across metrics. Finally, we provide an R package, SkewCalc , to estimate M from empirical data.

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