Primates and primatologists: social contexts for interspecies pathogen transmission

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 primatologists, characterizing their occupational exposures to NHP. Of 116 individuals who participated in the study, 68.1% reported having worked with NHP in a field setting, 68.1% in a laboratory setting, and 24.1% at a zoo or animal sanctuary. Most subjects (N=98, 84.5%) reported having worked with multiple NHP taxa, including 46 (39.7%) who had worked with more than five distinct taxa. Sixty-nine subjects (59.5%) recalled having been scratched by a NHP and 48 (41.1%) had been bitten; 32 subjects reporting being bitten more than once. Eleven subjects (9.5%) reported having been injured by a needle containing NHP tissue or body fluids. We conclude that primatologists are at high risk for exposure to NHP-borne infectious agents. Furthermore, primatologists' varied occupational activities often bring them into contact with multiple NHP species in diverse contexts and geographic areas, over extended periods of time, making them a unique population with respect to zoonotic and anthropozoonotic disease risk.     

Modelling pathogen transmission: the interrelationship between local and global approaches

We describe two spatial (cellular automaton) host-pathogen models with contrasting types of transmission, where the biologically realistic transmission mechanisms are based entirely on 'local' interactions. The two models, fixed contact area (FCA) and fixed contact number (FCN), may be viewed as local 'equivalents' of commonly used global density- (and frequency-) dependent models. Their outputs are compared with each other and with the patterns generated by these global terms. In the FCN model, unoccupied cells are bypassed, but in the FCA model these impede pathogen spread, extending the period of the epidemic and reducing the prevalence of infection when the pathogen persists. Crucially, generalized linear modelling reveals that the global transmission terms betaSI and beta'SI/N are equally good at describing transmission in both the FCA and FCN models when infected individuals are homogeneously distributed and N is approximately constant, as at the quasi-equilibrium. However, when N varies, the global frequency-dependent term beta'SI/N is better than the density-dependent one, betaSI, at describing transmission in both the FCA and FCN models. Our approach may be used more generally to compare different local contact structures and select the most appropriate global transmission term.     

Assessing variation in the social behavior of stumptail macaques using thermal criteria

This paper reports a method for comparing the environments of nonhuman primates based on biophysical, thermal criteria. The method is applied to an analysis of behaviors exhibited by group-living stumptail macaques (Macaca arctoides), documented by a group-scan observation technique, to test the hypothesis that the expression of social behavior is dependent on thermal conditions. Thermal conditions are identified by considering sky cover and the relative cooling power of the environment. The results show that the rates of occurrence of affiliative, play, and solitary behaviors are altered significantly at a relative cooling power at or above 550 kcal/m2/hr under cloudy conditions and at or above 600 kcal/m2/hr under sunny conditions. In addition, the rates of occurrence of play, sexual, aggressive, and submissive behavioral states are also significantly different under cloudy, rather than sunny, conditions over particular ranges of cooling. It is possible to conclude that thermal criteria affect the expression of social behaviors by stumptail macaques. This is consistent with studies of huddling behavior exhibited by stumptail macaques and rhesus macaques (M. mulatta), and suggests that 1) certain changes in the expression of social behaviors may be thermoregulatory in at least some nonhuman primate species and 2) thermal criteria are likely to be useful tools when conducting comparative analyses of behavioral data collected on animals in outdoor environments.     

The MHC E locus in macaques is polymorphic and is conserved between macaques and humans

Although the functions of the molecules encoded by the classical MHC class I loci are well defined, no function has been ascribed to the molecules encoded by the non-classical MHC class I loci. To investigate the evolution and conservation of the non-classical loci, we cloned and sequenced HLA-E homologues in macaques. We isolated four E locus alleles from five rhesus monkeys and two E locus alleles from one cynomolgus monkey, which indicated that the E locus in macaques is polymorphic. We also compared the rate of nucleotide substitution in the second intron of the macaque and human E locus alleles with that of exons two and three. The rate of nucleotide substitution was significantly higher in the introns, which suggested that the E locus has evolved under selective pressure. Additionally, comparison of the rates of synonymous and non-synonymous substitutions in the peptide binding region versus the remainder of the molecule suggested that the codons encoding the amino acids in the peptide binding region had been conserved in macaques and humans over the 36 million years since macaques and humans last shared a common ancestor.The nucleotide sequence data reported in this paper have been submitted to the GenBank nucleotide sequence database and have been assigned the accession numbers UO2976–UO2981     

Assessing the spontaneous cage behavior of the squirrel monkey (Saimiri sciureus)

A Behavioral Activity Index for rapid assessment of spontaneous cage behavior of the squirrel monkey is described. Observing the behavior of six male squirrel monkeys, it was found that four readily identifiable behaviors accounted for 62% of the total activity during a 30 minutes observation period. The need for a technique to reliably assess changes in baseline behavior is discussed in relation to behavioral pharmacological investigations.This research was supported by a Grant from the Moody Foundation, Galveston, Texas, and by the Physiological Psychology Branch, Office of Naval Research, Contract 1598-06.     

Shoe soles as a potential vector for pathogen transmission: a systematic review

Shoe soles are possible vectors for infectious diseases. Although studies have been performed to assess the prevalence of infectious pathogens on shoe soles and decontamination techniques, no systematic review has ever occurred. The aim of this study was to perform a systematic review of the literature to determine the prevalence of infectious agents on shoe bottoms and possible decontamination strategies. Three electronic bibliographic databases were searched using a predefined search strategy evaluating prevalence of infectious pathogens on shoe bottoms and decontamination strategies. Quality assessment was performed independently by two reviews with disagreements resolved by consensus. Thirteen studies were identified that supported the hypothesis that shoe soles are a vector for infectious pathogens. Methicillin‐resistant Staphylococcus aureus, Clostridium difficile and multidrug‐resistant Gram‐negative species among other pathogens were documented on shoe bottoms in the health care setting, in the community and among food workers. Fifteen studies were identified that investigated decontamination strategies for shoe soles. A number of decontamination strategies have been studied of which none have been shown to be consistently successful at disinfecting shoe soles. In conclusion, a high prevalence of microbiological pathogens was identified from shoe soles studied in the health care, community and animal worker setting. An effective decontamination strategy for shoe soles was not identified. Studies are needed to assess the potential for contaminated shoes to contribute to the transmission of infectious pathogens.     

Evidence for carry-over effects of predator exposure on pathogen transmission potential

Accumulating evidence indicates that species interactions such as competition and predation can indirectly alter interactions with other community members, including parasites. For example, presence of predators can induce behavioural defences in the prey, resulting in a change in susceptibility to parasites. Such predator-induced phenotypic changes may be especially pervasive in prey with discrete larval and adult stages, for which exposure to predators during larval development can have strong carry-over effects on adult phenotypes. To the best of our knowledge, no study to date has examined possible carry-over effects of predator exposure on pathogen transmission. We addressed this question using a natural food web consisting of the human malaria parasite Plasmodium falciparum, the mosquito vector Anopheles coluzzii and a backswimmer, an aquatic predator of mosquito larvae. Although predator exposure did not significantly alter mosquito susceptibility to P. falciparum, it incurred strong fitness costs on other key mosquito life-history traits, including larval development, adult size, fecundity and longevity. Using an epidemiological model, we show that larval predator exposure should overall significantly decrease malaria transmission. These results highlight the importance of taking into account the effect of environmental stressors on disease ecology and epidemiology.     

Conserved MHC class I peptide binding motif between humans and rhesus macaques

Since the onset of the HIV pandemic, the use of nonhuman primate models of infection has increasingly become important. An excellent model to study HIV infection and immunological responses, in particular cell-mediated immune responses, is SIV infection of rhesus macaques. CTL epitopes have been mapped using SIV-infected rhesus macaques, but, to date, a peptide binding motif has been described for only one rhesus class I MHC molecule, Mamu-A*01. Herein, we have established peptide-live cell binding assays for four rhesus MHC class I molecules: Mamu-A*11, -B*03, -B*04, and -B*17. Using such assays, peptide binding motifs have been established for all four of these rhesus MHC class I molecules. With respect to the nature and spacing of crucial anchor positions, the motifs defined for Mamu-B*04 and -B*17 present unique features not previously observed for other primate species. The motifs identified for Mamu-A*11 and -B*03 are very similar to the peptide binding motifs previously described for human HLA-B*44 and -B*27, respectively. Accordingly, naturally processed peptides derived from HLA-B*44 and HLA-B*27 specifically bind Mamu-A*11 and Mamu-B*03, respectively, indicating that conserved MHC class I binding capabilities exist between rhesus macaques and humans. The definition of four rhesus MHC class I-specific motifs expands our ability to accurately detect and quantitate immune responses to MHC class I-restricted epitopes in rhesus macaques and to rationally design peptide epitope-based model vaccine constructs destined for use in nonhuman primates.     

Covariation between the physiological and behavioral components of pathogen transmission: host heterogeneity determines epidemic outcomes

Although heterogeneity in contact rate, physiology, and behavioral response to infection have all been empirically demonstrated in host–pathogen systems, little is known about how interactions between individual variation in behavior and physiology scale‐up to affect pathogen transmission at a population level. The objective of this study is to evaluate how covariation between the behavioral and physiological components of transmission might affect epidemic outcomes in host populations. We tested the consequences of contact rate covarying with susceptibility, infectiousness, and infection status using an individual‐based, dynamic network model where individuals initiate and terminate contacts with conspecifics based on their behavioral predispositions and their infection status. Our results suggest that both heterogeneity in physiology and subsequent covariation of physiology with contact rate could powerfully influence epidemic dynamics. Overall, we found that 1) individual variability in susceptibility and infectiousness can reduce the expected maximum prevalence and increase epidemic variability; 2) when contact rate and susceptibility or infectiousness negatively covary, it takes substantially longer for epidemics to spread throughout the population, and rates of epidemic spread remained suppressed even for highly transmissible pathogens; and 3) reductions in contact rate resulting from infection‐induced behavioral changes can prevent the pathogen from reaching most of the population. These effects were strongest for theoretical pathogens with lower transmissibility and for populations where the observed variation in contact rate was higher, suggesting that such heterogeneity may be most important for less infectious, more chronic diseases in wildlife. Understanding when and how variability in pathogen transmission should be modelled is a crucial next step for disease ecology.     

Risk assessment: A model for predicting cross-species transmission of simian foamy virus from macaques (M. fascicularis) to humans at a monkey temple in Bali, Indonesia

Contact between humans and nonhuman primates (NHPs) frequently occurs at monkey temples (religious sites that have become associated with free-ranging populations of NHPs) in Asia, creating the potential for NHP-human disease transmission. In March 2003 a multidisciplinary panel of experts participated in a workshop designed to model the risk of NHP-human pathogen transmission. The panel developed a risk assessment model to describe the likelihood of cross-species transmission of simian foamy virus (SFV) from temple macaques (Macaca fascicularis) to visitors at monkey temples. SFV is an enzootic simian retrovirus that has been shown to be transmitted from NHPs to humans. In operationalizing the model field data, laboratory data and expert opinions were used to estimate the likelihood of SFV transmission within this context. This model sets the stage for a discussion about modeling as a risk assessment tool and the kinds of data that are required to accurately predict transmission.     

Natural variation in host feeding behaviors impacts host disease and pathogen transmission potential

Animals ranging from mosquitoes to humans often vary their feeding behavior when infected or merely exposed to pathogens. These so‐called “sickness behaviors” are part of the innate immune response with many consequences, including avoiding orally transmitted pathogens. Fully understanding the role of this ubiquitous behavior in host defense and pathogen evolution requires a quantitative account of its impact on host and pathogen fitness across environmentally relevant contexts. Here, we use a zooplankton host and fungal pathogen as a case study to ask if infection‐mediated feeding behaviors vary across pathogen exposure levels and natural genetic variation in susceptibility to infection. Then, we connect these changes in behavior to pathogen transmission potential (spore yield) and fitness and growth costs to the host. Our results validate a protective effect of altered feeding behavior during pathogen exposure while also revealing significant variation in the magnitude of this response across host susceptibility and pathogen exposure levels. Across all four host genotypes, feeding rates were negatively correlated with susceptibility to infection and transmission potential. The most susceptible genotypes exhibited either strong anorexia, reducing food intake by 26%–42%, (“Standard”) or pronounced hyperphagia, increasing food intake by 20%–54% (“A45”). Together, these results suggest that infection‐mediated changes in host feeding behavior—which are traditionally interpreted as immunopathology— may in fact serve as crucial components of host defense strategies and warrant further investigation.     

Human vocal behavior within competitive and courtship contexts and its relation to mating success

Beyond the linguistic content of their speech, speakers of both sexes convey diverse biological and psychosocial information through their voices, which are important when assessing potential mates and competitors. However, studies investigating the relationships between mating success and acoustic inter-individual differences are scarce. In this study, we investigated such relationships in both sexes in courtship and competitive interactions—as they correspond to the two different types of sexual selection—using an experimental design based on a simulated dating game. We assessed which type of sexual selection best predicted mating success, here defined as the self-reported number of sexual partners within the past year. Our results show that only acoustic inter-individual differences in the courtship context for both men and women predicted their mating success. Men displaying faster articulation rate and louder voices reported significantly more sexual partners; in contrast, men displaying higher intonation reported a greater negative effect of roughness and breathiness on their mating success. Women who displayed relatively less breathy voices and shorter speech duration reported significantly fewer sexual partners. These novel findings are discussed in light of the mate choice context and the relative contribution of both types of sexual selection shaping acoustic features of speech.     

Human–wildlife conflict: Proximate predictors of aggression between humans and rhesus macaques in India

Macaques live in close contact with humans across South and Southeast Asia, and direct interaction is frequent. Aggressive contact is a concern in many locations, particularly among populations of rhesus and longtail macaques that co‐inhabit urbanized cities and towns with humans. We investigated the proximate factors influencing the occurrence of macaque aggression toward humans as well as human aggression toward macaques to determine the extent to which human behavior elicits macaque aggression and vice versa. We conducted a 3‐month study of four free‐ranging populations of rhesus macaques in Dehradun, India from October–December 2012, using event sampling to record all instances of human‐macaque interaction (N = 3120). Our results show that while human aggression was predicted by the potential for economic losses or damage, macaque aggression was influenced by aggressive or intimidating behavior by humans as well as recent rates of conspecific aggression. Further, adult female macaques participated in aggression more frequently than expected, whereas adult and subadult males participated as frequently as expected. Our analyses demonstrate that neither human nor macaque aggression is unprovoked. Rather, both humans and macaques are responding to one another's behavior. Mitigation of human‐primate conflict, and indeed other types of human‐wildlife conflict in such coupled systems, will require a holistic investigation of the ways in which each participant is responding to, and consequently altering, the behavior of the other. Am J Phys Anthropol 156:286–294, 2015. © 2014 Wiley Periodicals, Inc.     

Trade-off between virulence and vertical transmission and the maintenance of a virulent plant pathogen

The continuum hypothesis predicts that parasites should evolve reduced virulence if they have higher opportunity for vertical transmission. However, when there is a trade-off between virulence and vertical transmission, selection may favor horizontal transmission and higher virulence. Atkinsonella hypoxylon is a fungal pathogen that reduces Danthonia fitness by 50% or more when it completely castrates hosts' chasmogamous inflorescences, despite the high opportunity for vertical transmission through cleistogamous seeds. Sporadically, infected hosts with partially castrated inflorescences (which have higher fecundity than completely castrated hosts) are observed in natural populations. Why are partially castrated plants rare if selection favors reduced virulence? We investigated whether there was genetic diversity for virulence among A. hypoxylon genotypes and the relationship between virulence and vertical transmission. We found that the fungal genotype significantly affects the occurrence of partial castration in Danthonia compressa. The proportion of seedlings that were vertically infected by their maternal plant was lower for partially castrated than for completely castrated plants. Our results demonstrate a trade-off between virulence and vertical transmission, explaining the maintenance of more virulent, completely castrating fungal genotypes in natural populations, and suggest that vertical transmission in plants is more complex than what is considered in current models.     

Plasmodium knowlesi: reservoir hosts and tracking the emergence in humans and macaques

Plasmodium knowlesi, a malaria parasite originally thought to be restricted to macaques in Southeast Asia, has recently been recognized as a significant cause of human malaria. Unlike the benign and morphologically similar P. malariae, these parasites can lead to fatal infections. Malaria parasites, including P. knowlesi, have not yet been detected in macaques of the Kapit Division of Malaysian Borneo, where the majority of human knowlesi malaria cases have been reported. In order to extend our understanding of the epidemiology and evolutionary history of P. knowlesi, we examined 108 wild macaques for malaria parasites and sequenced the circumsporozoite protein (csp) gene and mitochondrial (mt) DNA of P. knowlesi isolates derived from macaques and humans. We detected five species of Plasmodium (P. knowlesi, P. inui, P. cynomolgi, P. fieldi and P. coatneyi) in the long-tailed and pig-tailed macaques, and an extremely high prevalence of P. inui and P. knowlesi. Macaques had a higher number of P. knowlesi genotypes per infection than humans, and some diverse alleles of the P. knowlesi csp gene and certain mtDNA haplotypes were shared between both hosts. Analyses of DNA sequence data indicate that there are no mtDNA lineages associated exclusively with either host. Furthermore, our analyses of the mtDNA data reveal that P. knowlesi is derived from an ancestral parasite population that existed prior to human settlement in Southeast Asia, and underwent significant population expansion approximately 30,000-40,000 years ago. Our results indicate that human infections with P. knowlesi are not newly emergent in Southeast Asia and that knowlesi malaria is primarily a zoonosis with wild macaques as the reservoir hosts. However, ongoing ecological changes resulting from deforestation, with an associated increase in the human population, could enable this pathogenic species of Plasmodium to switch to humans as the preferred host.     

Relationship between culture redox potential and culture fluorescence inCorynebacterium glutamicum

Summary Transient experiments were performed during a batch fermentation ofCorynebacterium glutamicum ATCC 14296 in which the flow of air to the reactor was cut off. The fluorescence of the culture was observed to vary linearly with the culture redox potential during the transient. This observation was made below the sensitivity limit of a dissolved oxygen probe. It appears that redox potential in conjunction with fluorescence measurements are of utility in studying extra- and intracellular reduction states, particularly in the microaerobic regime.