An official website of the United States government
Abstract Models of host–pathogen interactions help to explain infection dynamics in wildlife populations and to predict and mitigate the risk of zoonotic spillover. Insights from models inherently depend on the way contacts between hosts are modelled, and crucially, how transmission scales with animal density.Bats are important reservoirs of zoonotic disease and are among the most gregarious of all mammals. Their population structures can be highly heterogeneous, underpinned by ecological processes across different scales, complicating assumptions regarding the nature of contacts and transmission. Although models commonly parameterise transmission using metrics of total abundance, whether this is an ecologically representative approximation of host–pathogen interactions is not routinely evaluated.We collected a 13‐month dataset of tree‐roostingPteropusspp. from 2,522 spatially referenced trees across eight roosts to empirically evaluate the relationship between total roost abundance and tree‐level measures of abundance and density—the scale most likely to be relevant for virus transmission. We also evaluate whether roost features at different scales (roost level, subplot level, tree level) are predictive of these local density dynamics.Roost‐level features were not representative of tree‐level abundance (bats per tree) or tree‐level density (bats per m2or m3), with roost‐level models explaining minimal variation in tree‐level measures. Total roost abundance itself was either not a significant predictor (tree‐level 3D density) or only weakly predictive (tree‐level abundance).This indicates that basic measures, such as total abundance of bats in a roost, may not provide adequate approximations for population dynamics at scales relevant for transmission, and that alternative measures are needed to compare transmission potential between roosts. From the best candidate models, the strongest predictor of local population structure was tree density within roosts, where roosts with low tree density had a higher abundance but lower density of bats (more spacing between bats) per tree.Together, these data highlight unpredictable and counterintuitive relationships between total abundance and local density. More nuanced modelling of transmission, spread and spillover from bats likely requires alternative approaches to integrating contact structure in host–pathogen models, rather than simply modifying the transmission function.
more »
« less
Food availability leads to more connected contact networks among peridomestic zoonotic reservoir hosts
The North American deermouse (Peromyscus maniculatus) is a reservoir host for many zoonotic pathogens. Deermice have been well studied, but few studies have attempted to understand social interactions within the species despite these interactions being key to understanding disease transmission. We performed an experiment to determine if supplemental food or nesting material affected social interactions of deermice and tested if interactions increased with increasing population density. We constructed three simulated buildings that received one of three treatments: food, nesting material, or control. Mice were tagged with passive integrated transponder (PIT) tags, and their movement in and out of buildings was monitored with PIT tag readers. PIT tag readings were used to create contact networks, assuming a contact if two deermice were in the same building at the same time. We found that buildings with food led to contact networks that were approximately 10 times more connected than buildings with nesting material or control buildings. We also saw a significant effect of population density on the average number of contacts per individual. These results suggest that food supplementation which is common in peridomestic settings, can significantly increase contacts between reservoir hosts, potentially leading to increased transmission of zoonotic viruses within the reservoir host and from reservoir hosts to humans.
more »
« less
- Award ID(s):
- 2109828
- PAR ID:
- 10478458
- Publisher / Repository:
- Royal Society Publishing
- Date Published:
- Journal Name:
- Royal Society Open Science
- Volume:
- 10
- Issue:
- 11
- ISSN:
- 2054-5703
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
ABSTRACT To explain patterns between anthropogenic loss of species diversity and the rise in the number of novel zoonotic diseases, the “dilution effect” hypothesis predicts that with lower species diversity, infection risk will increase. The underlying mechanisms have been largely investigated in systems where pathogen transmission is vector‐borne or environmental. Relatively less research has been conducted in systems where transmission is direct, such as with orthohantaviruses (hereafter hantaviruses) and their rodent reservoir hosts. These systems are commonly cited as supporting a negative diversity‐disease pattern. To motivate empirical research on underlying mechanisms driving this pattern, we extend a mechanistic framework that links species diversity and infection prevalence of directly transmitted zoonotic pathogens by using rodent‐hantavirus systems in the Americas as models. Additionally, we summarize empirical studies, synthesize mechanistic evidence, and identify knowledge gaps. Our findings suggest that host regulation is a key mechanism likely to drive diversity‐disease patterns in rodent‐hantavirus systems of the Americas. Other mechanisms have received less empirical support but also less attention. Although host regulation likely functions via density‐dependent transmission, and can thus change contact rates among hosts, consequences to other mechanisms have been neglected. As observed in rodent‐hantavirus systems in the Americas, we propose that for a negative diversity‐disease pattern to manifest, the primary reservoir host species should be resilient to anthropogenic disturbance but also vulnerable to competition, predation, or both, and the “diversity” measure should be associated with host density.more » « less
-
ABSTRACT Microbial transmission is hypothesised to be a major benefit of sociality, facilitated by affiliative behaviours such as grooming and communal nesting in group‐living animals. Whether microbial transmission is also present in animals that do not form groups because territoriality limits interactions and prevents group formation remains unknown. Here, we investigate relationships among gut microbiota, population density and dynamic behavioural and spatial measures of territoriality in wild North American red squirrels (Tamiasciurus hudsonicus). Periods of high population density predicted population‐level gut microbial homogeneity but individual‐level diversification, alongside changes in obligately anaerobic, non‐sporulating taxa indicative of social transmission. Microbial alpha‐diversity increased with more frequent territorial intrusions, and pairs with stronger intrusion‐based social associations had more similar gut microbiota. As some of the first evidence for social microbial transmission in a solitary system, our findings suggest that fluctuations in density and territorial behaviours can homogenise and diversify host microbiomes among otherwise non‐interacting animals.more » « less
-
Abstract ObjectivesUnderstanding disease transmission is a fundamental challenge in ecology. We used transmission potential networks to investigate whether a gastrointestinal protozoan (Blastocystisspp.) is spread through social, environmental, and/or zoonotic pathways in rural northeast Madagascar. Materials and MethodsWe obtained survey data, household GPS coordinates, and fecal samples from 804 participants. Surveys inquired about social contacts, agricultural activity, and sociodemographic characteristics. Fecal samples were screened forBlastocystisusing DNA metabarcoding. We also tested 133 domesticated animals forBlastocystis. We used network autocorrelation models and permutation tests (networkk‐test) to determine whether networks reflecting different transmission pathways predicted infection. ResultsWe identified six distinctBlastocystissubtypes among study participants and their domesticated animals. Among the 804 human participants, 74% (n = 598) were positive for at least oneBlastocystissubtype. Close proximity to infected households was the most informative predictor of infection with any subtype (model averaged OR [95% CI]: 1.56 [1.33–1.82]), and spending free time with infected participants was not an informative predictor of infection (model averaged OR [95% CI]: 0.95 [0.82–1.10]). No human participant was infected with the same subtype as the domesticated animals they owned. DiscussionOur findings suggest thatBlastocystisis most likely spread through environmental pathways within villages, rather than through social or animal contact. The most likely mechanisms involve fecal contamination of the environment by infected individuals or shared food and water sources. These findings shed new light on human‐pathogen ecology and mechanisms for reducing disease transmission in rural, low‐income settings.more » « less
-
Identifying the key vector and host species that drive the transmission of zoonotic pathogens is notoriously difficult but critical for disease control. We present a nested approach for quantifying the importance of host and vectors that integrates species’ physiological competence with their ecological traits. We apply this framework to a medically important arbovirus, Ross River virus (RRV), in Brisbane, Australia. We find that vertebrate hosts with high physiological competence are not the most important for community transmission; interactions between hosts and vectors largely underpin the importance of host species. For vectors, physiological competence is highly important. Our results identify primary and secondary vectors of RRV and suggest two potential transmission cycles in Brisbane: an enzootic cycle involving birds and an urban cycle involving humans. The framework accounts for uncertainty from each fitted statistical model in estimates of species’ contributions to transmission and has has direct application to other zoonotic pathogens.more » « less
- Free Publicly Accessible Full Text
-
Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1098/rsos.230809
