Effects of social and climatic factors on birth sex ratio in Macaca mulatta in Mount Taihangshan area

Sex allocation theory predicts the optimal investment to male and female offspring. However, a biased sex ratio requires explanations as to why the deviation occurs. Rhesus macaque (Macaca mulatta) is the most widely distributed nonhuman primate species and the Taihangshan macaque (Macaca mulatta tcheliensis) occupies the northern limit of all rhesus macaque natural populations worldwide. We observed one macaque troop (Wangwu‐1 [WW‐1]) inhabiting Taihangshan Macaque National Nature Reserve and recorded all birth events and the sex of newborn macaques from 2004 to 2013. Our aim was to apply the Trivers–Willard hypothesis to this free‐ranging rhesus macaque troop, and to understand the relationship between climatic parameters (precipitation and temperature) and birth sex ratio. We found that the total newborn macaques showed a female‐biased sex ratio at birth in the WW‐1 troop, but there were no significant biased birth sex ratios in all matriarchs and in high‐ranking and middle‐ranking matrilineal units. However, the low‐ranking macaque matrilineal unit was significantly female‐biased. Moreover, we found that the annual precipitation of the previous year was positively associated with the birth sex ratio, and there was an interactive effect of troop size and current winter temperature on the birth sex ratio. The underlying mechanisms for the effects of social and climatic factors on birth sex ratio could be complex, and we discuss several plausible explanations.     

Novel betapapillomavirus associated with hand and foot papillomas in a cynomolgus macaque

Betapapillomavirus is a genus of papillomaviruses (PVs) commonly found in human skin and associated with both benign and malignant skin lesions. Only 2 previous beta-PVs have been fully characterized in nonhuman species. This report describes a novel beta-PV, named Macaca fascicularis PV type 2 (MfPV2), isolated from exophytic skin papillomas on the hands and feet of a 2-year-old male cynomolgus monkey (M. fascicularis). On histology the papillomas were composed of diffusely thickened epidermis with superficial foci of cytomegaly, cytoplasmic pallor, marginalized chromatin, and rare eosinophilic intranuclear inclusion bodies. Positive immunostaining for p16 and the proliferation marker Ki67 was present multifocally within affected epidermis, most prominently within basal-type cells. Complete sequence identity (100%) was noted between PV genomes fully sequenced from hand and foot lesions. The MfPV2 genome was 7632 base pairs in length and included putative open reading frames (ORFs) for E1, E2, E4, E6, E7, L1, and L2 genes, similar to other PVs. The closest relatives to MfPV2 based on the L1 ORF sequence were all beta-PVs. These included human PV (HPV) 9, HPV115, HPV76, HPV75, and MfPV1 (60-70% pairwise identity for all), the latter of which was also isolated from hand and foot papillomas in a cynomolgus macaque. Phylogenetic analysis placed MfPV2 in a new species group (beta-6), distinct from HPVs (beta-1 to beta-5) and MfPV1 (beta-1). These findings characterize a new nonhuman beta-PV and provide additional support for the idea that tissue tropism among ancestral primate PVs developed prior to divergence of certain Old World primate lineages.     

Intestinal parasites of baboons (Papio cynocephalus anubis) and chimpanzees (Pan troglodytes) in Gombe National Park.

A survey of gastrointestinal parasites of nonhuman primates in Gombe National Park, Tanzania, was conducted during July and August 1989. Fresh fecal samples collected from 35 baboons (Papio cynocephalus anubis) and 20 chimpanzees (Pan troglodytes) were analyzed for intestinal parasites. Parasite identifications were based upon the size and appearance of eggs and larvae on both direct and fecal flotation examinations. Seven species of helminths and three species of protozoa were noted in the chimpanzees, and seven species of helminths, two species of trematodes, and one species of protozoa were noted in baboons. An unidentified parasite, with a thick egg shell similar to that of ascarids, was noted in both the chimpanzee and baboon population. Unfortunately a definitive identification of this parasite could not be made based upon egg size and morphology alone and insufficient numbers of larva were present to aid identification. One previously unreported parasite, Schistosoma mansoni, was identified in the baboon population. This is the first report of a schistosome in Gombe's nonhuman primate population.     

Simian immunodeficiency virus infections in vervet monkeys (Clorocebus aethiops) at an Australian zoo

A number of monkey species, including African green monkeys and African vervet monkeys (Chlorocebus aethiops), are frequently infected in the wild and in captivity with a Simian immunodeficiency virus strain, SIVagm, a primate lentivirus. Up to 50% of African green monkeys are estimated to be infected with SIVagm. SIV strains are very closely related to HIV-2 strains, which are a cause of AIDS in humans, predominantly in western Africa, although cases in Australia have also been reported. It is generally thought that SIV is non-pathogenic in several natural hosts, including African green monkeys. Nevertheless many SIV strains induce a profound immunodeficiency virtually identical to HIV-1 induced AIDS in humans when administered to Asian macaque species such as rhesus (Macaca mulatta) or pigtailed macaques (M nemestrina). SIV infection of Asian macaque species is frequently employed as an animal model for AIDS vaccine studies. In November 1996 a group of 10 African vervet monkeys were imported from the USA for display at Victoria's Open Range Zoo in Werribee. Two animals in this group of monkeys later developed a fatal gastroenteric illness. These diagnoses led us to initiate SIV testing of the colony.     

The use of a cathodic antigen in the immunoelectrophoretic serodiagnosis of Echinococcus granulosus in sheep

An antigen was prepared from purified sheep hydatid-cyst fluid by gelfiltration on Sephadex G-200 followed by chromatography on DEAE-cellulose. In each case the first-peak material was used. This antigen, which migrated cathodically, was concentrated and used in immunoelectrophoretic analyses of 4X concentrated sera from sheep experimentally and naturally infected with $\text{Echinococcus granulosus}$ and from uninfected sheep. Of 34 sheep with $\text{E. granulosus}$ infection 31 were positive with the cathodic antigen while of 85 sheep without $\text{E. granulosus}$ 8 were (falsely) positive. Many false positives appeared to be associated with heavy infections of $\text{Taenia ovis}$ or $\text{T. hydatigena}$ larvae. The “arc 5” immunoelectrophoresis test, which is the most specific immuno-diagnostic test for echinococcus infection in humans, was not able to specifically identify $\text{E. granulosus}$ infections in sheep.     

Genetic structure and recent population demographic history of Taihangshan macaque (Macaca mulatta tcheliensis), North China

Massive actions have been and are being taken into protecting the world's primates from extinction, while the study of the properties of genetic diversity, demographic history, and ecological relationships will benefit the understanding of the long-term survival of a species. The Taihangshan macaque (Macaca mulatta tcheliensis), a subspecies of rhesus macaque (Macaca mulatta), is endemic to China and currently restricted to southern Mt. Taihangshan area. Herein, we evaluated the genetic diversity, population structure, and demographic history of this subspecies using mitochondrial (Cytb and high variable region I: HVR I) and nuclear markers (microsatellite loci) of 131 individuals collected from 9 localities covering the distribution range of this subspecies. Both phylogenetic analyses and genetic assignment revealed that the wild populations of Taihangshan macaques could be divided into 2 major highly divergent clades, THS-east and THS-west. Low genetic diversity (π: 0.00266 ± 0.00016) but high haplotype diversity (H_d: 0.80352 ± 0.015) were detected in the Taihangshan macaques, particularly in THS-east. Analyses of demographic history suggested that the Taihangshan macaques experienced first a stable historical population size from Holocene to early 19th century but a subtle decline and then slight growth in the recent 200 years. We suggest that bridging the neighbor populations (i.e. setting corridors) would facilitate the male-mediated gene flow and subsequently increase the genetic diversity of the Taihangshan macaque populations.     

Pharmacokinetics of tramadol following intravenous and oral administration in male rhesus macaques (Macaca mulatta)

Recently, tramadol and its active metabolite, O‐desmethyltramadol (M1), have been studied as analgesic agents in various traditional veterinary species (e.g., dogs, cats, etc.). This study explores the pharmacokinetics of tramadol and M1 after intravenous (IV) and oral (PO) administration in rhesus macaques (Macaca mulatta), a nontraditional veterinary species. Rhesus macaques are Old World monkeys that are commonly used in biomedical research. Effects of tramadol administration to monkeys are unknown, and research veterinarians may avoid inclusion of this drug into pain management programs due to this limited knowledge. Four healthy, socially housed, adult male rhesus macaques (Macaca mulatta) were used in this study. Blood samples were collected prior to, and up to 10 h post‐tramadol administration. Serum tramadol and M1 were analyzed using liquid chromatography–mass spectrometry. Noncompartmental pharmacokinetic analysis was performed. Tramadol clearance was 24.5 (23.4–32.7) mL/min/kg. Terminal half‐life of tramadol was 111 (106–127) min IV and 133 (84.9–198) min PO. Bioavailability of tramadol was poor [3.47% (2.14–5.96%)]. Maximum serum concentration of M1 was 2.28 (1.88–2.73) ng/mL IV and 11.2 (9.37–14.9) ng/mL PO. Sedation and pruritus were observed after IV administration.     

Anti-complementary activity for guinea-pig and sheep complement in serum and Mg2+-EGTA plasma from various animals

Serum and Mg²⁺-ethyleneglycoltetraacetic acid (EGTA) plasma from 14 domestic or laboratory animal species had no anti-complementary activity for sheep complement (C). Serum samples from 8 species and all 14 Mg²⁺-EGTA plasma samples were anti-complementary towards guinea-pig C. Thus, use of sheep C in a warm complement fixation text (with human erythrocytes sensitized with sheep antiserum, IgM, slow or fast γ-globulin antibody), in the presence or absence of Mg²⁺-EGTA, may be a satisfactory method of eliminating anticomplementary activity.     

Diet and dietary-niche breadth of diurnal rain forest primates in the Central Western Ghats, India

We studied the feeding ecology of 3 sympatric primate species, the lion-tailed macaque (Macaca silenus), bonnet macaque (Macaca radiata) and Hanuman langur (Semnopithecus entellus), in a tropical rain forest of the Central Western Ghats, India. Since the availability of leaves is much higher than that of fruits, we expected that the primarily folivorous langurs would use a larger number of resources than the primarily frugivorous macaques. Since fruits are a relatively total resource, unlike leaves, of which only selected parts are consumed, we expected that the primarily frugivorous macaques would use resources more proportionately than the folivorous langurs, resulting in a wider food niche breadth in macaques. We collected data on these primate species over a period of 2 years using scan sampling in a contiguous rain forest. We calculated Levin's standardised food niche breadth for each species. Langurs used a larger number of tree species than macaques, but their niche breadth was narrower than that of macaques. The majority of their diet (over 50%) came from only a few trees in the case of all three primate species. Long-term data are provided herein for the first time on the feeding ecology of bonnet macaques and Hanuman langurs in a tropical rain forest.     

Distribution of helper and suppressor/cytotoxic T-lymphocytes in subsets of rhesus macaque peripheral blood T-lymphocytes as determined by monoclonal antibodies: Tγ, Tμ, T-null,and histamine receptor bearing T-cells

Rhesus macaque ($\text{Macaca mulatta}$) peripheral blood T-lymphocyte subpopulations were assessed for the distribution of helper and suppressor/cytotoxic cells using the T-cell subset specific monoclonal antibodies T4 and T8 respectively. Highly purified T-lymphocytes (> 90% E-rosetted) were separated into subpopulations by rosetting with IgG (Tγ) and Igm (Tμ) sensitized bovine red blood cells, or by adsorption with insolubilized histamine. In this study, rhesus peripheral blood T-lymphocytes were found to express cell-surface determinates recognized by T4 and T8 monoclonal antibodies. Subset frequencies were found to be comparable to that found in humans (50% T4 and 33% T8). The helper subpopulation, Tμ, contained 30% T4 and 2% T8 type cells. These results suggest Tγ helper activity may be due to a selective depletion of suppressor cells, rather than an enrichment of helper T-cells. The suppressor subpopulations, Tγ, contained 9% T4 and 2% T8 type cells. These results suggest Tγ cells may represent either an undifferentiated suppressor cell or, perhaps, a separate suppressor subpopulation which does not express T8 differentiation antigens. The Tγ-subpopulation (depleted of cells with Fc-IgG receptors) was rich in helper T-cells (52% T4) and depleted of suppressor T-cells (6% T8). T-cells depleted of cells expressing IgM or IgG receptors, T-null, contained 47% T4 and 12% T8 type cells. Further, T-cells adsorbed with insolubilized histamine were selectively depleted (70% reduction) of T8 type cells, while the frequency of T4 type cells remained unaffected by histamine absorption. The majority of suppressor/cytotoxic T-cells (T8), therefore, appear to express cell-surface receptors for histamine.     

A newly‐found pattern of social relationships among adults within one‐male units of golden snub‐nosed monkeys (Rhinopithecus roxenalla) in the Qinling Mountains,China

Group living provides various advantages to individuals in regards to protection avoidance, intergroup competition, productive success and social information. Stable one‐male units (OMUs) consist of relationships between the adult females and the resident male as well as the relationships among adult females. Based on continuous observation of a reproductive group of golden snub‐nosed monkeys (Rhinopithecus roxellana) in the Qinling Mountains, we analyzed the relationships among adult individual dyads within 4 OMUs. The results indicated that in golden snub‐nosed monkey societies, females not only had no strong tendency to build a relationship with the resident male in the OMU but also had no strong tendency to build relationships with other females in the OMU. In comparison with hamadryas (Papio hamadryas) and gelada baboons (Theropithecus gelada), the relationships within golden snub‐nosed monkeys OMUs showed neither the star‐shaped pattern observed in hamadryas baboons nor the net‐shaped pattern observed in gelada baboons. We concluded that the relationships within golden snub‐nosed monkey OMUs indicated a third pattern in nonhuman primate societies. Future research is required to determine the potential mechanisms for such a pattern.     

Bovine babesiosis: The immunization of cattle with fractions of erythrocytes infected with Babesia bovis (syn B. argentina)

Soluble antigen which protected susceptible cattle against challenge with $\text{Babesia bovis}$ was extracted from $\text{B. bovis}$-infected erythrocytes by sonic disintegration and separation of the soluble from the insoluble matter by ultracentrifugation. The material was then fractionated by the precipitation of fibrinogen-like proteins. The precipitate contained the babesial antigens that were located on the stroma of the infected erythrocytes. Antigen originally located on the parasite remained in solution. Both fractions conferred protection on splenectomized calves against challenge with $\text{B. bovis}$. However, the fraction containing the parasite antigens appeared to have more potential for development as a killed vaccine because it was not heavily contaminated with antigenic material from bovine erythrocytes.     

A comparative study of natural killer cell activity, lymphoproliferation, and cell phenotypes in nonhuman primates.

Three different species of nonhuman primates (baboons [Papio hamadryas], rhesus monkeys [Macaca mulatta], and African green monkeys [Cercopithecus aethiops]) were evaluated for their natural killer cell activity, and for the ability of their peripheral blood mononuclear cells to proliferate in response to known mitogens (concanavalin A, phytohemagglutinin, and pokeweed mitogen) and to react with a panel of mouse monoclonal antibodies directed against human leukocyte surface antigens. Rhesus monkeys displayed the highest natural killer cell cytotoxic activity (185.7 +/- 33 lytic units) compared with those of baboons (83.8 +/- 19 lytic units) and of African green monkeys from West Africa (39.08 +/- 8 lytic units) and from the Caribbean basin (37.9 +/- 9 lytic units). No correlation was observed between the natural killer cell cytotoxic activity and the percentage of CD16+ natural killer cells among the three species studied. High spontaneous proliferative capacity was observed in African green monkeys obtained from West Africa compared with those of the other species studied. Although no significant differences were noted in T and B cell mitogen-induced in vitro proliferation, baboon mononuclear cells were less responsive to concanavalin A (stimulation index of 16 +/- 3 [mean +/- standard error of mean]) than to phytohemagglutinin (stimulation index of 47 +/- 12). However, rhesus and African green monkey cells proliferated more efficiently in response to concanavalin A. Unlike in human beings where the ratio between helper-inducer (CD4+) and cytotoxic-suppressor (CD8+) T-lymphocytes is generally greater than 1, the CD4+/CD8+ ratios in baboons and rhesus and African green monkeys were 0.58, 0.69, and 0.35, respectively.(ABSTRACT TRUNCATED AT 250 WORDS)     

Adult‐onset,chronic, cyclic thrombocytopenia in a Rhesus macaque (Macaca mulatta) after dengue virus vaccination and viral challenge

An 8‐year‐old, male Rhesus macaque (Macaca mulatta), previously used for dengue virus (DENV) vaccine research with viral challenge, was presented with adult‐onset, chronic, cyclic thrombocytopenia. Platelet number, morphology, and function were evaluated by automated hematology, peripheral blood smears, electron microscopy, flow cytometry, and impedance aggregometry. Bone marrow was evaluated by cytology. Both serum anti‐dengue nonstructural protein 1 (NS1) antibodies and anti‐platelet antibodies were detected by ELISA. Platelet characterization showed a lack of aggregation to all agonists (ADP, ASP, and collagen), increased activation with increased expression of surface marker (HLA‐ABC), and an absence of surface receptor GPIX during clinical episodes of petechiae and ecchymoses, even in the presence of normal platelet counts. Bone marrow aspirates identified potential mild megakaryocytic hypoplasia. All platelet functions and morphologic attributes were within normal limits during clinically normal phases. Presence of anti‐dengue NS1 serum antibodies confirmed a positive DENV titer 8 years postvaccination. Based on the history and clinical findings, a primary differential diagnosis for this chronic, cyclic platelet pathology was autoimmune platelet destruction with potential bone marrow involvement.     

Serological relationship of a Japanese Babesia species and Babesia bigemina by the complement fixation and capillary-tube agglutination tests

The complement fixation (CF) test and the capillary-tube agglutination (CA) test were used to study the antigenic relationship between Babesia bigemina and the large Babesia species frequently infecting cattle in Japan. The CF antigen was prepared from parasitized erythrocytes by extraction with distilled water. The CA antigen was prepared from parasitized erythrocytes by mild sonification of mixtures of Babesia and erythrocyte stroma, following lysis of the erythrocytes with hypotonic saline solution. All the sera used were collected from experimentally-infected cattle. Cross reaction was demonstrated between the Japanese Babesia species and B. bigemina. There was, however, a difference of two dilutions in titer between homologous and heterologous antibody in the CF test, and a difference of more than three tubes in titer between both antibodies in the CA test. It was possible, therefore, to distinguish the Japanese Babesia species from B. bigemina by the CF and CA tests.     

实验猴间日疟原虫感染的血清学调查

为了解实验猴间日疟原虫感染的基本情况,为猕猴属动物或其他非人类灵长类实验动物间日疟原虫病的防治提供参考。通过酶联免疫吸附试验(ELISA)的检测方法,对采自云南昆明某灵长类研究中心的3种实验猴(恒河猴、豚尾猴、食蟹猴)的血清样品进行间日疟原虫抗原检测。结果,3种实验猴的间日疟原虫血清阳性率平均为1. 62%,其中,豚尾猴的血清阳性率最高为5. 62%,其次恒河猴的血清阳性率为0. 94%,食蟹猴的血清阳性率为0%,3种实验猴的血清阳性率有显著差异(P=0. 004 <0. 05);从性别分析,公猴(2. 89%)和母猴(0. 94%)的血清阳性率之间无显著差异(P=0. 101> 0. 05);从年龄分析,青年猴(≤4岁)血清阳性率为3. 07%,成年猴(> 4岁)血清阳性率为0%,也存在显著性差异(P=0. 007 <0. 05)。从回归分析结果来看,品种因素是引起实验猴感染间日疟原虫的主要风险因子(P=0. 004 <0. 05)。结果表明,该灵长类研究中心的实验猴存在间日疟原虫感染,带虫猴会成为潜在的内部感染源。饲养人员需要加强对实验猴的饲养管理及间日疟原虫的防治工作,提高实验猴质量。     

NONHUMAN PRIMATE EXCRETORY UROGRAPHY*

Survey radiographs have not accurately identified renal contour or location in nonhuman primates. Excretory urography using 786 to 1193 mg iodinelkg body weight resulted in dense opacification of the renal parenchyma and pelvis. Abdominal compression improved visu- alization of the renal pelvis. Interpretation of the nonhuman primate excretory urogram was compromised by several anatomic characteristics of this animal group. Superimposition of the kidneys on the lateral radiograph limited evaluation of the renal contour. Since the renal pelvis in most species of nonhuman primates does not possess diverticula (as in the dog and cat) or a caliceal system (as in the pig and man), the diagnosis of pyelonephritis or renal mass lesions was difficult. Severe irregularities in the renal contour, size of the renal pelvis, or areas of deficient concentrating ability were identifiable in nonhuman primate excretory urograms, but the diagnosis of small cysts was not possible in smaller nonhuman primates. The presence of a caliceal collecting system in the spider monkey (Ateles sp.) suggests this animal as a potential model for the evaluation of human renal disease.     

The effects of Leptospira serotype pomona in sheep of different haemoglobin types

A warm complement fixation test that will detect antibody in sheepserum in the virtual absence of anti-complementary activity is described. Sheep antibody-antigen complexes were detected by fixation of sheep complement. Sheep serum, heparinized or Mg⁺⁺—EGTA plasma was used as the source of sheep complement. Sheep-antibody-sensitized human erythrocytes were used as the haemolytic indicator cells for sheep complement. As the modified complement-fixation test was performed in the presence of Mg⁺⁺—EGTA, sheep C probably reacts with sheep Ab-Ag complexes by a different mechanism than does guinea-pig complement.     

Studies on degradation and outflow rate of protein supplements in the rumen of sheep and cattle

The rates of disappearance (p) of protein from fish-meal, meat-and-bone meal, soya-bean meal, cottonseed meal, linseed-meal and groundnut-meal were described when nylon bags were incubated in the rumens of sheep and cattle given either barley or dried grass. The exponential equation p = a + b (1 ? e^?ct),where a, b and c are constants, e is the natural logarithm, and p the amount disappearing in time, t, was used. There was no consistent difference between the degradabilities determined with sheep and cattle. Degradation was finally combined with different outflow rate (k) and the effective degradability (P) was described as the equation $\text{P}\text{=}\text{a + (bc)}\text{(c + k)}$.     

Campylobacter-induced fetal death in a rhesus monkey

A pregnant 4-year-old rhesus monkey (Macaca mulatta) was presented with a history of acute vaginal bleeding. Physical examination revealed an open cervix. An ultrasound scan demonstrated a viable early third-trimester fetus, approximately 16 weeks of gestational age. Hematology results showed that the monkey was anemic, with a normal leukogram and D?hle bodies. A subsequent cervical culture was positive for Campylobacter fetus. The fetus died 3 days later, and a necropsy of the fetus and placenta was performed. Microscopic examination of the placenta revealed villitis, perivillitis, and deciduitis with S-shaped and gull wing-shaped bacteria. C. fetus was considered the cause of the placental lesions and fetal death; however, the pathogenesis of the infection (hematogenous vs. ascending from the maternal genital tract) was not clear. This is the first report of a Campylobacter-induced fetal death in the rhesus monkey. Because macaques can be asymptomatic carriers and Campylobacter-induced diarrhea is common, this finding has implications for breeding success in nonhuman primate breeding colonies.