Lisa Jones-Engel

University of Washington Seattle | UW · Washington National Primate Research Center

The global trade in nonhuman primates represents a substantial threat to ecosystem health, human health, and primate conservation worldwide. Most of the primate trade involves trade for pet-keeping, consumption, or biomedical experimentation. We present an overview of international primate trade through five case studies; each describes a different...

In 2022, long-tailed macaques (Macaca fascicularis), a once ubiquitous primate species, was elevated to Endangered on the International Union for Conservation of Nature (IUCN) Red List of Threatened Species. In 2023, recognizing that the long-tailed macaque is threatened by multiple factors: (1) declining native habitats across Southeast Asia; (2)...

Measles infections can cause significant morbidity and mortality in human and monkey populations. The endemicity of measles in human populations and viral circulation within populations of free-living monkeys may have important repercussions for potential zoonotic transmission events and for the long-term health of monkey populations. Yet, there ha...

The IUCN Red List assessment of Macaca fascicularis 2022

From foraging patterns in a single tree to social interactions across a home range, how primates use space is a key question in the field of primate behavioral ecology. Drawing on the latest advances in spatial analysis tools, this book offers practical guidance on applying geographic information systems (GIS) to central questions in primatology. A...

Oral swabs are emerging as a non-invasive sample type for diagnosing infectious diseases including Ebola, tuberculosis (TB), and COVID-19. To assure proper sample collection, sample adequacy controls (SACs) are needed that detect substances indicative of samples collected within the oral cavity. This study evaluated two candidate SACs for this purp...

Oral swabs are emerging as a non-invasive sample type for diagnosing infectious diseases including Ebola, tuberculosis (TB), and COVID-19. To assure proper sample collection, sample adequacy controls (SACs) are needed that detect substances indicative of samples collected within the oral cavity. This study evaluated two candidate SACs for this purp...

In the original publication of the article, figure 1 was wrongly published as a duplication.

Over the past 20 years, GPS collars have emerged as powerful tools for the study of nonhuman primate (hereafter, "primate") movement ecology. As the size and cost of GPS collars have decreased and performance has improved, it is timely to review the use and success of GPS collar deployments on primates to date. Here we compile data on deployments a...

There is mounting evidence to suggest that short telomere length (TL) increases an organism’s susceptibility to disease and accelerates aging. However, it is not well understood why these effects do not select for longer telomeres. The ‘thrifty telomere’ hypothesis suggests one possibility: while longer telomeres improve an organism’s ability to re...

Diagnostic tests for tuberculosis (TB) usually require collection of sputum, a viscous material derived from human airways. Sputum can be difficult and hazardous to collect and challenging to process in the laboratory. Oral swabs have been proposed as alternative sample types that are non-invasive and easy to collect. This study evaluated the biolo...

The H9N2 influenza viruses that have become established in Bangladeshi live poultry markets possess five gene segments of the highly pathogenic H7N3 avian influenza virus. We assessed the replication, transmission, and disease potential of three H9N2 viruses in chickens and New World quail. Each virus replicated to high titers and transmitted by th...

Highly pathogenic avian influenza H5N1 viruses were first isolated in Bangladesh in February 2007. Subsequently, clades 2.2.2, 2.3.4.2 and 2.3.2.1a were identified in Bangladesh, and our previous surveillance data revealed that by the end of 2014, the circulating viruses exclusively comprised clade 2.3.2.1a. We recently determined the status of cir...

Highly pathogenic avian influenza A(H5N8) clade 2.3.4.4 virus emerged in 2016 and spread to Russia, Europe, and Africa. Our analysis of viruses from domestic ducks at Tan-guar haor, Bangladesh, showed genetic similarities with other viruses from wild birds in central Asia, suggesting their potential role in the genesis of A(H5N8). © 2017, Centers f...

Influenza viruses isolated from wild birds and free-ranging domestic ducks in the Tanguar haor region of Bangladesh, February 2015–February 2016, and phylogenetic trees for the genes of these viruses.

Objectives: Cyclical submergence and re-emergence of the Sunda Shelf throughout the Pleistocene served as a dynamic biogeographic landscape, across which long-tailed macaques (Macaca fascicularis) have migrated and evolved. Here, we tested the integrity of the previously reported continental-insular haplotype divide reported among Y and mitochondr...

The global increase in urbanization is leading to heavier interface between humans and wildlife. Within these anthropogenic landscapes, little is known about ranging patterns, particularly with regard to urban primates. Here we present the results of the first long-term deployment of multiple GPS collars on two species of macaques to investigate th...

Survey results showed treponemal infection among pet macaques in Southeast Asia, a region with a high prevalence of human yaws. This finding, along with studies showing treponemal infection in nonhuman primates in Africa, should encourage a One Health approach to yaws eradication and surveillance activities, possibly including monitoring of nonhuma...

Highly pathogenic avian influenza (HPAI) H5N1 and low pathogenic avian influenza (LPAI) H9N2 viruses have been recognized as threats to public health in Bangladesh since 2007. Although live bird markets (LBMs) have been implicated in the transmission, dissemination, and circulation of these viruses, an in-depth analysis of the dynamics of avian tra...

In 2011, avian influenza surveillance at the Bangladesh live bird markets (LBMs) showed complete replacement of the highly pathogenic avian influenza (HPAI) H5N1 virus of clade 2.2.2 (Qinghai-like H5N1 lineage) by the HPAI H5N1 clade 2.3.2.1. This clade, which continues to circulate in Bangladesh and neighboring countries, is an intra-and interclad...

H9N2 avian influenza viruses are continuously monitored by the World Health Organization because they are endemic; they continually reassort with H5N1, H7N9 and H10N8 viruses; and they periodically cause human infections. We characterized H9N2 influenza viruses carrying internal genes from highly pathogenic H7N3 viruses, which were isolated from ch...

The acquisition and training of monkeys to perform is a centuries-old tradition in South Asia, resulting in a large number of rhesus macaques kept in captivity for this purpose. The performing monkeys are reportedly collected from free-ranging populations, and may escape from their owners or may be released into other populations. In order to deter...

Avian influenza A(H9N2) is an agricultural and public health threat. We characterized an H9N2 virus from a pet market in Bangladesh and demonstrated replication in samples from pet birds, swine tissues, human airway and ocular cells, and ferrets. Results implicated pet birds in the potential dissemination and zoonotic transmission of this virus.

Methods for influenza-specific laboratory procedures; primary cell and tissue culture; inoculation and exposure of donor and contact animals; and statistical methods to determine the replication capacity of avian influenza A (H9N2) virus in pet birds and mammals in Bangladesh.

Astroviruses (AstVs) are positive sense, single-stranded RNA viruses transmitted to a wide range of hosts via the fecal-oral route. The number of AstV-infected animal hosts has rapidly expanded in recent years with many more likely to be discovered because of the advances in viral surveillance and next generation sequencing. Yet no study to date ha...

Simian Foamy viruses (SVF) are ubiquitous in non-human primates (NHP). SFV can be zoonotically transmitted to humans, who either work with, or live commensally with NHP. We analyzed the blood of 45 Bangladeshi performing monkey owners (an ethnic group called the Bedey) for SFV infection. Surprisingly, PCR failed to detect SFV infection in any of th...

Diagnosis of pulmonary tuberculosis (TB) usually includes laboratory analysis of sputum, a viscous material derived from deep in the airways of patients with active disease. As a diagnostic sample matrix, sputum can be difficult to collect and analyze. An alternative, less invasive sample matrix could greatly simplify TB diagnosis. We hypothesized...

Diagnosis of pulmonary tuberculosis (TB) usually includes laboratory analysis of sputum, a viscous material derived from deep in the airways of patients with active disease. As a diagnostic sample matrix, sputum can be difficult to collect and analyze by microbiological and molecular techniques. An alternative, less invasive sample matrix could gre...

Avian influenza subtype H9N2 is endemic in many bird species in Asia and the Middle East and has contributed to the genesis of H5N1, H7N9 and H10N8, which are potential pandemic threats. H9N2 viruses that have spread to Bangladesh have acquired multiple gene segments from highly pathogenic (HP) H7N3 viruses that are presumably in Pakistan and curre...

Monkey performance is a centuries’ old tradition in Bangladesh. Monkey performers catch monkey, train and rear them for street show or any other gatherings to earn their livelihood. The study was conducted on performing monkey population in Bangladesh between January 2012 and June 2013. Monkey species, age-sex and other demographic features were re...

The Mycobacterium tuberculosis complex causes tuberculosis in humans and nonhuman primates and is a global public health concern. Standard diagnostics rely upon host immune responses to detect infection in nonhuman primates and lack sensitivity and specificity across the spectrum of mycobacterial infection in these species. We have previously shown...

While studies of rhesus macaques (Macaca mulatta) in the eastern (e.g., China) and western (e.g., India) parts of their geographic range have revealed major genetic differences that warrant the recognition of two different subspecies, little is known about genetic characteristics of rhesus macaques in the transitional zone extending from eastern In...

Author Summary Simian Foamy Virus (SFV) is a very common retrovirus in monkeys. When an infected monkey bites a human it can transmit the virus to the human; however, there are no documented cases of human to human transmission. There also appear to be significant differences between infection in monkey and human hosts. The reason for these differe...

Highly pathogenic H5N1 and low pathogenic H9N2 influenza viruses are endemic to poultry markets in Bangladesh and have cocirculated since 2008. H9N2 influenza viruses circulated constantly in the poultry markets, whereas highly pathogenic H5N1 viruses occurred sporadically, with peaks of activity in cooler months. Thirty highly pathogenic H5N1 infl...

Foamy viruses (FV) are complex retroviruses that naturally infect all nonhuman primates (NHP) studied to date. Zoonotic transmission of Old World NHP simian foamy viruses (SFV) has been documented, leading to nonpathogenic persistent infections. To date, there have been no reports concerning zoonotic transmission of New World monkey (NWM) SFV to hu...

Simian foamy viruses (SFV) are complex retroviruses that are ubiquitous in nonhuman primates (NHP) and are zoonotically transmitted to humans, presumably through NHP saliva, by licking, biting, and other behaviors. We have studied SFV in free-ranging rhesus macaques in Bangladesh. It has been previously shown that SFV in immunocompetent animals rep...

Human infection with avian influenza A(H9N2) virus was identified in Bangladesh in 2011. Surveillance for influenza viruses in apparently healthy poultry in live-bird markets in Bangladesh during 2008-2011 showed that subtype H9N2 viruses are isolated year-round, whereas highly pathogenic subtype H5N1 viruses are co-isolated with subtype H9N2 prima...

Simian foamy viruses (SFVs) are ubiquitous in non-human primates (NHPs). As in all retroviruses, reverse transcription of SFV leads to recombination and mutation. Because more humans have been shown to be infected with SFV than with any other simian borne virus, SFV is a potentially powerful model for studying the virology and epidemiology of virus...

Genes of influenza A(H9N2) viruses from Bangladesh that were not sequenced or only partially sequenced, amino acid substitutions in hemagglutinin and neuraminidase gene products and in internal genes that determine host specificity of the viruses, and phylogenetic relations of key internal genes of the virus isolates.

Much of the primatology literature on stable isotope ratios of carbon (δ13C) and nitrogen (δ15N) has focused on African and New World species, with comparatively little research published on Asian primates. Here we present hair δ13C and δ15N isotope values for a sample of 33 long-tailed macaques from Singapore. We evaluate the suggestion by a previ...

Foamy viruses are complex retroviruses that have been shown to be transmitted from nonhuman primates to humans. In Bangladesh, infection with simian foamy virus (SFV) is ubiquitous among rhesus macaques, which come into contact with humans in diverse locations and contexts throughout the country. We analyzed microsatellite DNA from 126 macaques at...

In Bangladesh rhesus macaques (Macaca mulatta) are found in forested habitats and urban areas. From 2005 to 2010, we investigated the distribution of rhesus macaques throughout the country. Populations were estimated by line transect, point sampling and direct counting. A total of 37 groups in 16 localities were recorded in urban areas. Overall, gr...

Conditions in densely populated Bangladesh favor picornavirus transmission, resulting in a high rate of infection in the human population. Data suggest nonhuman primates (NHP) may play a role in the maintenance and transmission of diverse picornaviruses in Bangladesh. At the Dhaka Zoo, multiple NHP species are caged in close proximity. Their proxim...

The term synanthropic describes organisms that thrive in human-altered habitats. Where synanthropic nonhuman primates (NHP) share an ecological niche with humans, cross-species transmission of infectious agents can occur. In Bangladesh, synanthropic NHP are found in villages, densely populated cities, religious sites, and protected forest areas. NH...

To determine whether nonhuman primates are infected with influenza viruses in nature, we conducted serologic and swab studies among macaques from several parts of the world. Our detection of influenza virus and antibodies to influenza virus raises questions about the role of nonhuman primates in the ecology of influenza.

Here we present a case series from a primate research facility. The index case, a 4-year-old pig-tailed macaque (Macaca nemestrina) experimentally infected with chimeric simian-human immunodeficiency virus (SHIVSF162 P4), developed weight loss and was euthanized. Based on necropsy results the animal was diagnosed with opportunistic atypical mycobac...

Although the Mycobacterium tuberculosis complex (MTBC) infects a third of all humans, little is known regarding the prevalence of mycobacterial infection in nonhuman primates (NHP). For more than a century, tuberculosis has been regarded as a serious infectious threat to NHP species. Advances in the detection of MTBC open new possibilities for inve...

Biomedical research in the 21st century increasingly relies on pathogen-free nonhuman primates (NHPs) to model human pathophysiology. Despite adherence to protocols designed to maintain pathogen-free colonies, reports of tuberculosis regularly appear. We hypothesize that, undetected by standard screening protocols, mycobacteria of the Mycobacterium...

Humans and nonhuman primates (NHP) interact in a variety of contexts. The frequency, duration, and intensity of interspecies interaction influence the likelihood that contact results in cross-species transmission of infectious agents. In this study, we present results of a cross-sectional survey of attendees at a national conference of primatologis...

Recent findings of Plasmodium in African apes have changed our perspectives on the evolution of malarial parasites in hominids. However, phylogenetic analyses of primate malarias are still missing information from Southeast Asian apes. In this study, we report molecular data for a malaria parasite lineage found in orangutans. We screened twenty-fou...

BEAST node numbers for the Plasmodium phylogeny as used in Table 5 and 6. (TIF)

Cultural and ecological interactions between non-human primates (NHPs) and humans occur in a variety of contexts in Peru, and human population growth and economic development has increased human-NHP interactions through habitat encroachment, hunting, wildlife trade, and through access to zoos and sanctuaries. Additionally, harboring exotic pets in...

Timing the origin of human malarias has been a focus of great interest. Previous studies on the mitochondrial genome concluded that Plasmodium in primates, including those parasitic to humans, radiated relatively recently during a process where host switches were common. Those investigations, however, assumed constant rate of evolution and tightly...

Divergence times of major splits in the malarial tree. Divergence times of major splits in the malarial tree as estimated by MultiDivTime and BEAST. Point time estimates and 95% credibility intervals (CrIs) are shown in millions of years (Mya). Three calibration scenarios are shown with different minimum-maximum boundaries. The absolute maximum (AB...

Node numbers for the malarial phylogeny including lemurs. MultiDivTime and BEAST node numbers for the lemur phylogeny.

Phylogenetic tree of lemur Plasmodium, including the partial sequences obtained from the Propithecus verrauxi isolate, based on mitochondrial genomes. In the Bayesian phylogenetic tree presented, the values above branches are posterior probabilities. The accession numbers of the sequences derived from the parasites found in lemurs and other species...

Timetree of major malarial splits using a conservative calibration. Divergence times in MultiDivTime and CrIs for major splits in the malarial phylogeny (MultiDivTime: filled bars; BEAST: empty bars). A single conservative calibration was used (6-8 Mya).

Separate saturation plots for complete mitochondrial genome and each gene. Saturation plots for complete mitochondrial genome (top left), cox3 (top right), cox1 (bottom left), and cytb (bottom right). Green dots represent the observed data for transitions, blue dots for transversions; while the light green and light blue lines are smoothing connect...

Node numbers for the malarial phylogeny including gorilla species. Node numbers as used in Table 4. This phylogeny includes recently published gorilla species (see main text for details).

Timetree of major malarial splits using an inclusive calibration. Divergence times in MultiDivTime and CrIs for major splits in the malarial phylogeny (MultiDivTime: filled bars; BEAST: empty bars). The calibration point used includes the maximum molecular time estimate for the Papio/Macaca divergence.

Long-tailed macaques are an edge species, preferring to live along the forest borders of many habitat types (Gumert, Chapter 1). The result of this preference is that long-tailed macaques are adaptable generalists that are frequently found along the edges of human settlements across Southeast Asia. Another consequence is that long-tailed macaques c...

Long-tailed macaques (Macaca fascicularis) have a wide geographical distribution and extensively overlap with human societies across southeast Asia, regularly utilizing the edges of secondary forest and inhabiting numerous anthropogenic environments, including temple grounds, cities and farmlands. Yet despite their apparent ubiquity across the regi...

Avian influenza surveillance in Bangladesh has been passive, relying on poultry farmers to report suspected outbreaks of highly pathogenic H5N1 influenza. Here, the results of an active surveillance effort focusing on the live-bird markets are presented. Prevalence of influenza infection in the birds of the live bird markets is 23.0%, which is simi...

Long-tailed macaques (Macaca fascicularis) have a wide geographical distribution and extensively overlap with human societies across southeast Asia, regularly utilizing the edges of secondary forest and inhabiting numerous anthropogenic environments, including temple grounds, cities and farmlands. Yet despite their apparent ubiquity across the regi...

Twenty years ago it was generally considered unthinkable (as well as unfundable and unpublishable) to carry out research on non-human primates (hereafter ‘primates’) that were in contact with human populations. Such contexts were seen as abnormal/aberrant situations, which distorted ‘natural’ primate behaviour and ecology. In the last decade this b...

Humans and nonhuman primates have coexisted and interacted for millennia in Asia. Interspecies interaction is particularly intensive at religious sites that are commonly referred to by Westerners as “monkey temples” or “monkey forests”. These monkey temples are found throughout South and Southeast Asia, and some have evolved into significant touris...

The retroviral restriction factor TRIMCyp, which is a fusion protein derived from the TRIM5 gene, blocks replication at a post-entry step. Among Old World primates, TRIMCyp has been found in four species of Asian macaques, but not in African monkeys. To further define the evolutionary origin of Old World TRIMCyp, we examined two species of baboons...

The cardiothoracic ratio is often used as a proxy measure of cardiovascular pathophysiology in humans but less frequently in nonhuman primates, for whom little published data are available to establish normal values. The present study is the first to examine relative cardiac size in a feral population of primates. This report presents estimates of...

The relative size of the heart, as measured by the cardiothoracic ratio, is often used as an index of ventricular hypertrophy—an important measure of myocardial pathophysiology in human primates. Despite its widespread use in human medicine, use of the cardiothoracic ratio in nonhuman primate veterinary medicine has been poorly documented. This rep...

The long-tailed macaque (Macaca fascicularis) population of the island-state of Singapore consists of ca. 1,218–1,454 individuals. About seventy percent of the population (ca. 1,027 individuals) is concentrated in both Bukit Timah and Central Catchment Nature Reserves, a system of reservoirs and forest reserves located in the center of Singapore. T...

Humans and long-tailed macaques (Macaca fascicularis) interface in several locations in Singapore. We investigated six of these interface zones to assess the level of conflict between the two species. We observed macaque-to-human interactions and distributed questionnaires to residents and visitors of nature reserves. We observed an average of two...

Macaques are similar to humans both physiologically and behaviorally. In South and Southeast Asia they are also synanthropic, ecologically associated with humans. Synanthropy with humans raises the possibility that macaques come into contact with anthropogenic toxicants, such as lead and mercury, and might be appropriate sentinels for human exposur...

In Asia, contact between persons and nonhuman primates is widespread in multiple occupational and nonoccupational contexts. Simian foamy viruses (SFVs) are retroviruses that are prevalent in all species of nonhuman primates. To determine SFV prevalence in humans, we tested 305 persons who lived or worked around nonhuman primates in several South an...

Previous studies have noted substantial human-macaque interactions involving physical contact in Bali, Indonesia; Gibraltar; and Mt. Emei, China [Fuentes, American Journal of Primatology 68:880-896, 2006; Zhao, Tibetan macaques, visitors, and local people at Mt. Emei: problems and countermeasures. In: Paterson and Wallis, editor. Commensalism and c...

Because Gibraltar's macaques (Macaca sylvanus) have frequent contact with humans, we assayed 79 macaques for antibodies to enzootic primate viruses. All macaques were seronegative for herpesvirus B, simian T-cell lymphotropic virus, simian retrovirus, simian immunodeficiency virus, and rhesus cytomegalovirus. Seroprevalence of simian foamy virus re...

This report describes the results from a study of thoracic radiographs taken on a sample (n = 20) of pet macaque monkeys (Macaca) on the Indonesian island of Sulawesi. We present findings relating to general thoracic health, as well as describe our field methods and outline some of the challenges of conducting thoracic radiography in remote areas o...

Crab-eating, or long-tailed, macaques [Macaca fascicularis (Raffles, 1821)] have been studied extensively throughout their distribution in South and South-east Asia. Despite this extensive body of research, the island population of long-tailed macaques from Singapore remains virtually undescribed. In the present study, we compare the morphometric v...