Extensive diversity of intestinal trichomonads of non-human primates

Despite the fact that the non-human primates are our closest relatives and represent a species-rich mammalian group, little is known about their intestinal protistan parasites/commensals. Particularly, the intestinal trichomonads represent a neglected part of the fauna of the primate digestive system. We have established 30 trichomonad strains isolated from feces of 11 primate species kept in 3 Czech zoos and performed an analysis of their SSU rDNA and ITS1-5·8S rDNA-ITS2. Our results showed that intestinal trichomonads are rather common among non-human primates. Molecular phylogenetic analysis showed that the strains are unexpectedly diversified, belonging to 8 or 9 distinct species. Interestingly, the vast majority of the strains from non-human primates belonged to the genus Tetratrichomonas while no member of this genus has been found in the human intestine so far. In addition, hominoid and non-hominoid primates differed in their intestinal trichomonads. Our results suggest that captive primates possibly may be infected by intestinal trichomonads of other vertebrates such as pigs, cattle, birds, tortoises and lizards.     

Spontaneous rat bite fever in non-human primates: a review of two cases

Rat bite fever is a worldwide zoonotic, non-reportable disease. This entity encompasses similar, yet distinct, disease syndromes caused by Streptobacillus moniliformis or Spirillum minus. Naturally occurring rat bite fever has not been previously described in non-human primates. This report describes two cases of non-human primate rat bite fever caused by S. moniliformis; a rhesus macaque (Macaca mullata) with valvular endocarditis, and a titi monkey (Callicebus sp.) with septic arthritis. Potential sources of infection included direct contact, and ingestion of surface water or feed contaminated with rodent feces.     

Complete Mitochondrial Genomes of Chimpanzee- and Gibbon-Derived Ascaris Isolated from a Zoological Garden in Southwest China

Roundworms (Ascaridida: Nematoda), one of the most common soil-transmitted helminths (STHs), can cause ascariasis in various hosts worldwide, ranging from wild to domestic animals and humans. Despite the veterinary and health importance of the Ascaridida species, little or no attention has been paid to roundworms infecting wild animals including non-human primates due to the current taxon sampling and survey bias in this order. Importantly, there has been considerable controversy over the years as to whether Ascaris species infecting non-human primates are the same as or distinct from Ascaris lumbricoides infecting humans. Herein, we first characterized the complete mitochondrial genomes of two representative Ascaris isolates derived from two non-human primates, namely, chimpanzees (Pan troglodytes) and gibbons (Hylobates hoolock), in a zoological garden of southwest China and compared them with those of A. lumbricoides and the congeneric Ascaris suum as well as other related species in the same order, and then used comparative mitogenomics, genome-wide nucleotide sequence identity analysis, and phylogeny to determine whether the parasites from chimpanzees and gibbons represent a single species and share genetic similarity with A. lumbricoides. Taken together, our results yielded strong statistical support for the hypothesis that the chimpanzee- and gibbon-derived Ascaris represent a single species that is genetically similar to A. lumbricoides, consistent with the results of previous morphological and molecular studies. Our finding should enhance public alertness to roundworms originating from chimpanzees and gibbons and the mtDNA data presented here also serves to enrich the resource of markers that can be used in molecular diagnostic, systematic, population genetic, and evolutionary biological studies of parasitic nematodes from either wild or domestic hosts.     

Leishmaniasis in non-human primates: Clinical and pathological manifestations and potential as reservoirs

Although the domestic dog is the most important reservoir of visceral leishmaniasis in urban areas, there have been an increasing number of reports of naturally occurring leishmaniasis in non-human primates. Reported cases affecting neotropical and Old World non-human primates as well as their potential role as reservoirs were reviewed.     

Cockroaches as vectors of Sarcocystis muris and of other coccidia in the laboratory.

To assess the roles of the German cockroach (Blatella germanica) and the American cockroach (Periplaneta americana) in the transmission of Sarcocystis muris and of 3 other coccidia of cats-Toxoplasma gondii, Isospora felis, and Isospora rivolta, cockroaches exposed to feces containing these coccidia were periodically fed to mice, as was a portion of the fecal matter. Sarcocystis muris sporocysts, which in feces remained infectious for at least 20 days, were also transmitted to mice by P. americana for at least 20 days and by B. germanica for 5 days after exposure to infectious feces. Toxoplasma gondii oocysts were transmitted by P. americana intermittently up to 10 days, but by B. germanica only immediately after exposure to feces. Oocysts of 2 species of Isospora, when associated with fecal matter, remained infectious for 20 days. Those of I. rivolta were transmitted by both cockroach species for 10 days, but I. felis was transmitted only by by B. germanica, and for only 2 days.     

Economic behaviours among non-human primates

Do we have any valid reasons to affirm that non-human primates display economic behaviour in a sufficiently rich and precise sense of the phrase? To address this question, we have to develop a set of criteria to assess the vast array of experimental studies and field observations on individual cognitive and behavioural competences as well as the collective organization of non-human primates. We review a sample of these studies and assess how they answer to the following four main challenges. (i) Do we see any economic organization or institutions emerge among groups of non-human primates? (ii) Are the cognitive abilities, and often biases, that have been evidenced as underlying typical economic decision-making among humans, also present among non-human primates? (iii) Can we draw positive lessons from performance comparisons among primate species, humans and non-humans but also across non-human primate species, as elicited by canonical game-theoretical experimental paradigms, especially as far as economic cooperation and coordination are concerned? And (iv) in which way should we improve models and paradigms to obtain more ecological data and conclusions? Articles discussed in this paper most often bring about positive answers and promising perspectives to support the existence and prevalence of economic behaviours among non-human primates.This article is part of the theme issue ‘Existence and prevalence of economic behaviours among non-human primates’.     

Zoonotic schistosomiasis in non-human primates: past, present and future activities at the human-wildlife interface in Africa

Schistosomiasis is one of the world's most widely distributed and prevalent parasitic diseases. Less widely recognized is that some species of Schistosoma, including several that commonly affect humans, also cause disease in other mammalian species; in particular, infections in non-human primates are known. With interest increasing in emerging zoonotic diseases, the status of schistosomiasis as a zoonotic infection is in need of re-appraisal, especially in light of advances in application of molecular screening and epidemiological tools where newly reported infections raise general animal welfare and conservation concerns. Focusing on Africa, this review provides a summary of the occurrence of schistosomiasis in non-human primates and discusses new ways in which surveillance for schistosomiasis should be integrated into more effective conservation management and disease control strategies. Emphasis is on the more common forms of human schistosomiasis, their clinical manifestations and epidemiological significance in terms of infection reservoir potential.     

Mitochondrial and Nuclear Ribosomal DNA Evidence Supports the Existence of a New Trichuris Species in the Endangered Fran?ois’ Leaf-Monkey

The whipworm of humans, Trichuris trichiura, is responsible for a neglected tropical disease (NTD) of major importance in tropical and subtropical countries of the world. Whipworms also infect animal hosts, including pigs, dogs and non-human primates, cause clinical disease (trichuriasis) similar to that of humans. Although Trichuris species are usually considered to be host specific, it is not clear whether non-human primates are infected with T. trichiura or other species. In the present study, we sequenced the complete mitochondrial (mt) genome as well as the first and second internal transcribed spacers (ITS-1 and ITS-2) of Trichuris from the François’ leaf-monkey (langur), and compared them with homologous sequences from human- and pig-derived Trichuris. In addition, sequence comparison of a conserved mt ribosomal gene among multiple individual whipworms revealed substantial nucleotide differences among these three host species but limited sequence variation within each of them. The molecular data indicate that the monkey-derived whipworm is a separate species from that of humans. Future work should focus on detailed population genetic and morphological studies (by electron microscopy) of whipworms from various non-humans primates and humans.     

Host range characteristics of the primate coccidian, Isospora arctopitheci Rodhain 1933 (Protozoa: Eimeriidae).

Studies were conducted on 35 primates, 12 carnivores, and 2 marsupials to determine their susceptibility to the primate coccidian, Isospora arctopitheci. Patent oocyst infections resulted in 12 of the 14 species of animals investigated. These included 6 genera of New World primates native to Panama: Saguinus geoffroyi, Aotus trivirgatus, Ateles fusciceps, Cebus capucinus, Alouatta villosa, and Saimiri sciureus. In addition 4 families of carnivores (2 domestic and 2 sylvatic) and 1 species of marsupial became infected following experimental exposure. These animals are represented respectively by the following 6 genera and species: Canis familiaris; Felis catus; Nasua nasua, and Potos flavus; Eiria barbara; and Didelphis marsupialis. Four Old World rhesus monkeys, Macaca mulatta, and 1 carnivore, Bassaricyon gabbii, did not become oocyst positive. This unusually large host range makes this isosporan unique among the coccidia that have been investigated to date.     

Corvids can decide if a future exchange is worth waiting for

Evidence for time-dependent calculations about future rewards is scarce in non-human animals. In non-human primates, only great apes are comparable with humans. Still, some species wait for several minutes to obtain a better reward in delayed exchange tasks. Corvids have been shown to match with non-human primates in some time-related tasks. Here, we investigate a delay of gratification in two corvid species, the carrion crow (Corvus corone) and the common raven (Corvus corax), in an exchange task. Results show that corvids success decreases quickly as delay increases, with a maximal delay of up to 320 s (more than 5 min). The decision to wait rests both on the quality of the prospective reward and the time required to obtain it. Corvids also apply tactics (placing the reward on the ground or caching it) that probably alleviate costs of waiting and distract their attention during waiting. These findings contrast previous results on delayed gratification in birds and indicate that some species may perform comparably to primates.     

Combinatorial Communication in Bacteria: Implications for the Origins of Linguistic Generativity

Combinatorial communication, in which two signals are used together to achieve an effect that is different to the sum of the effects of the component parts, is apparently rare in nature: it is ubiquitous in human language, appears to exist in a simple form in some non-human primates, but has not been demonstrated in other species. This observed distribution has led to the pair of related suggestions, that (i) these differences in the complexity of observed communication systems reflect cognitive differences between species; and (ii) that the combinations we see in non-human primates may be evolutionary pre-cursors of human language. Here we replicate the landmark experiments on combinatorial communication in non-human primates, but in an entirely different species, unrelated to humans, and with no higher cognition: the bacterium Pseudomonas aeruginosa. Using the same general methods as the primate studies, we find the same general pattern of results: the effect of the combined signal differs from the composite effect of the two individual signals. This suggests that advanced cognitive abilities and large brains do not necessarily explain why some species have combinatorial communication systems and others do not. We thus argue that it is premature to conclude that the systems observed in non-human primates are evolutionarily related to language. Our results illustrate the value of an extremely broad approach to comparative research.     

Failure to detect simian immunodeficiency virus infection in a large Cameroonian cohort with high non-human primate exposure

Hunting and butchering of wildlife in Central Africa are known risk factors for a variety of human diseases, including HIV/AIDS. Due to the high incidence of human exposure to body fluids of non-human primates, the significant prevalence of simian immunodeficiency virus (SIV) in non-human primates, and hunting/butchering associated cross-species transmission of other retroviruses in Central Africa, it is possible that SIV is actively transmitted to humans from primate species other than mangabeys, chimpanzees, and/or gorillas. We evaluated SIV transmission to humans by screening 2,436 individuals that hunt and butcher non-human primates, a population in which simian foamy virus and simian T-lymphotropic virus were previously detected. We identified 23 individuals with high seroreactivity to SIV. Nucleic acid sequences of SIV genes could not be detected, suggesting that SIV infection in humans could occur at a lower frequency than infections with other retroviruses, including simian foamy virus and simian T-lymphotropic virus. Additional studies on human populations at risk for non-human primate zoonosis are necessary to determine whether these results are due to viral/host characteristics or are indicative of low SIV prevalence in primate species consumed as bushmeat as compared to other retroviruses in Cameroon.     

An effort to use human-based exome capture methods to analyze chimpanzee and macaque exomes

Non-human primates have emerged as an important resource for the study of human disease and evolution. The characterization of genomic variation between and within non-human primate species could advance the development of genetically defined non-human primate disease models. However, non-human primate specific reagents that would expedite such research, such as exon-capture tools, are lacking. We evaluated the efficiency of using a human exome capture design for the selective enrichment of exonic regions of non-human primates. We compared the exon sequence recovery in nine chimpanzees, two crab-eating macaques and eight Japanese macaques. Over 91% of the target regions were captured in the non-human primate samples, although the specificity of the capture decreased as evolutionary divergence from humans increased. Both intra-specific and inter-specific DNA variants were identified; Sanger-based resequencing validated 85.4% of 41 randomly selected SNPs. Among the short indels identified, a majority (54.6%-77.3%) of the variants resulted in a change of 3 base pairs, consistent with expectations for a selection against frame shift mutations. Taken together, these findings indicate that use of a human design exon-capture array can provide efficient enrichment of non-human primate gene regions. Accordingly, use of the human exon-capture methods provides an attractive, cost-effective approach for the comparative analysis of non-human primate genomes, including gene-based DNA variant discovery.     

Human is a unique species among primates in terms of telomere length.

TRF (terminal restriction fragments) length in various tissues of non-human primates such as Macaca mulatta (rhesus monkey), Macaca fuscata (Japanese monkey), Macaca fascicularis (crab-eating monkey), Pan troglodytes (common chimpanzee), and Pongo pygmaeus (orangutan) was at least 23 kb without exception, which was quite different from that of human somatic tissues (smaller than 10 kb). The distribution pattern of telomerase activity among tissues was similar between human and non-human primates, while the activity level showed some differences such as that strong telomerase activity was observed in gastrointestinal and lymphocytic tissues from non-human primates. The human appears to be a unique species among primates in terms of telomere length.     

The use of non-human primates in biological and medical research: evidence submitted by FRAME to the Academy of Medical Sciences/Medical Research Council/Royal Society/Wellcome Trust Working Group

The Academy of Medical Sciences, the Medical Research Council, the Royal Society and the Wellcome Trust are undertaking a study into the use of non-human primates in biological and medical research. An independent working group of scientific experts, led by Sir David Weatherall, aims to produce a report summarising the findings of this study, early in 2006. The trends in primate research, and the nature and effects of recent and proposed changes in the global use of non-human primates in research, will be investigated. The associated ethical, welfare and regulatory issues, and the role and impact of the Three Rs principles of refinement, reduction and replacement will also be reviewed. As part of this study, a call for evidence was made. The evidence submitted by FRAME emphasised that the use of non-human primates for fundamental research or for regulatory testing still fails to take into account the fact that, although non-human primates are anatomically and physiologically similar to humans, they are not necessarily relevant models for studies on human disease or human physiology. FRAME continues to believe that we have a duty to ensure that these animals are not used without overwhelming evidence that they are the only suitable and relevant models for use in work of undeniable significance.     

结核分枝杆菌在动物中的流行与传播

结核分枝杆菌(Mycobacterium tuberculosis)是一种重要的人兽共患病病原菌,人类是其主要宿主。千百年来,由于动物与人类关系密切,动物也成为结核分枝杆菌的重要宿主,且感染结核分枝杆菌的动物还能成为传染源,将其传播至人类和其他动物。关于动物感染结核分枝杆菌已有大量报道,包括大象、非人灵长类动物、貘、海狮、犬、猫、牛、鸟等。本文就结核分枝杆菌在野生动物、家畜中的流行与传播进行介绍,总结其在动物间传播的主要途径。     

Characterization of the fecal microbiome from non-human wild primates reveals species specific microbial communities

Background

Host-associated microbes comprise an integral part of animal digestive systems and these interactions have a long evolutionary history. It has been hypothesized that the gastrointestinal microbiome of humans and other non-human primates may have played significant roles in host evolution by facilitating a range of dietary adaptations. We have undertaken a comparative sequencing survey of the gastrointestinal microbiomes of several non-human primate species, with the goal of better understanding how these microbiomes relate to the evolution of non-human primate diversity. Here we present a comparative analysis of gastrointestinal microbial communities from three different species of Old World wild monkeys.

Methodology/Principal Findings

We analyzed fecal samples from three different wild non-human primate species (black-and-white colobus [Colubus guereza], red colobus [Piliocolobus tephrosceles], and red-tailed guenon [Cercopithecus ascanius]). Three samples from each species were subjected to small subunit rRNA tag pyrosequencing. Firmicutes comprised the vast majority of the phyla in each sample. Other phyla represented were Bacterioidetes, Proteobacteria, Spirochaetes, Actinobacteria, Verrucomicrobia, Lentisphaerae, Tenericutes, Planctomycetes, Fibrobacateres, and TM7. Bray-Curtis similarity analysis of these microbiomes indicated that microbial community composition within the same primate species are more similar to each other than to those of different primate species. Comparison of fecal microbiota from non-human primates with microbiota of human stool samples obtained in previous studies revealed that the gut microbiota of these primates are distinct and reflect host phylogeny.

Conclusion/Significance

Our analysis provides evidence that the fecal microbiomes of wild primates co-vary with their hosts, and that this is manifested in higher intraspecies similarity among wild primate species, perhaps reflecting species specificity of the microbiome in addition to dietary influences. These results contribute to the limited body of primate microbiome studies and provide a framework for comparative microbiome analysis between human and non-human primates as well as a comparative evolutionary understanding of the human microbiome.     

Serum leptin in nonpregnant and pregnant women and in old and new world nonhuman primates

Leptin is a hormone that is produced during mammalian pregnancy in the placental trophoblast and other tissues, including! fetal and maternal adipocytes. Synthesis of the polypeptide and the presence of its specific receptors throughout the human maternal fetoplacental unit suggest direct effects on conceptus growth and development. However, both the physiologic roles of leptin and the mechanisms regulating leptin synthesis in human pregnancy differ from those in laboratory and domestic species, necessitating the development of non-human primate research models. Therefore, we compared serum leptin concentrations in nonpregnant and pregnant women with those in both old world nonhuman primates (i.e., baboon, rhesus monkey, cynomolgus monkey) and new world nonhuman primates (i.e., squirrel monkey, titi monkey). As expected, maternal leptin levels were elevated in human and baboon pregnancies (P < 0.05 and P < 0.001, respectively). Levels in both species of old world monkeys were also greatly enhanced (P < 0.001). Although maternal serum concentrations were slightly elevated compared to nonpregnant levels in both species of new world monkeys, overall concentrations were dramatically lower than for either old world primates or humans. Results provide comparisons of serum leptin concentrations in pregnant and nonpregnant humans and baboons with those in both old and new world monkeys and further characterize these nonhuman primates as models for the investigation of leptin dynamics in pregnancy.     

Corvids avoid odd evaluation by following simple rules in a risky exchange task

In their natural environment, animals often make decisions crucial for survival, such as choosing the best patch or food, or the best partner to cooperate. The choice can be compared to a gamble with an outcome that is predictable but not certain, such as rolling a dice. In economics, such a situation is called a risky context. Several models show that although individuals can generally evaluate the odds of each potential outcome, they can be subject to errors of judgment or choose according to decision-making heuristics (simple decision rules). In non-human primates, similar errors of judgment have been reported and we have recently shown that they also use a decisional heuristics when confronted with a risky choice in an exchange task. This suggests a common evolutionary origin to the mechanisms underlying decision-making under risk in primates. However, whether the same mechanisms are also present in more distantly related taxa needs to be further investigated. Other social species, like corvids, are renowned for their advanced cognitive skills and may show similar responses. Here, we analyse data on corvids (carrion crows, hooded crows, common ravens and rooks) tested in a risky exchange task comparable to the one used in non-human primates. We investigated whether corvids could exchange according to the odds of success or, alternatively, whether they used a heuristic similar to the one used by non-human primates. Instead, most corvids chose a course of action (either a low or high exchange rate) that remained constant throughout the study. In general, corvids’ mean exchange rates were lower compared to non-human primates, indicating that they were either risk-adverse or that they do not possess the cognitive capabilities to evaluate odds. Further studies are required to evaluate the flexibility in exchange abilities of these birds in exchange abilities of these birds.     

非人灵长类饲养与管理过程中的福利保障

实验动物饲养管理和福利保障的问题已越来越被国际社会所关注.与发达国家相比,中国对实验动物福利的研究及大众化意识则相对滞后.中国作为世界上最大的实验灵长类动物的饲养与出口国,每年遭受的国际贸易损失始终位居全球首位.为此,本文引入了实验灵长类福利的"5个自由"理论:1)动物有避免干渴、饥饿和营养不良等不利因素影响的自由;2)动物有获得舒适生活条件的自由;3)动物有脱离痛苦、受伤和疾病骚扰的自由;4)动物有表达自然行为的自由;5)动物有脱离恐惧和心理压力的自由.在上述理论的基础上,提高实验动物福利应具体从饲养的物理环境、营养供给、饲养管理、繁殖管理及饲养环境的多样性等几方面着手.通过总结国际与此相关的研究进展,旨为中国相关研究提供素材和为完善国内现行的法规及标准提出一些思路.