skip to main content


Title: Feline immunodeficiency virus in puma: Estimation of force of infection reveals insights into transmission
Abstract

Determining parameters that govern pathogen transmission (such as the force of infection, FOI), and pathogen impacts on morbidity and mortality, is exceptionally challenging for wildlife. Vital parameters can vary, for example across host populations, between sexes and within an individual's lifetime.

Feline immunodeficiency virus (FIV) is a lentivirus affecting domestic and wild cat species, forming species‐specific viral–host associations. FIV infection is common in populations of puma (Puma concolor), yet uncertainty remains over transmission parameters and the significance of FIV infection for puma mortality. In this study, the age‐specific FOI of FIV in pumas was estimated from prevalence data, and the evidence for disease‐associated mortality was assessed.

We fitted candidate models to FIV prevalence data and adopted a maximum likelihood method to estimate parameter values in each model. The models with the best fit were determined to infer the most likely FOI curves. We applied this strategy for female and male pumas from California, Colorado, and Florida.

When splitting the data by sex and area, our FOI modeling revealed no evidence of disease‐associated mortality in any population. Both sex and location were found to influence the FOI, which was generally higher for male pumas than for females. For female pumas at all sites, and male pumas from California and Colorado, the FOI did not vary with puma age, implying FIV transmission can happen throughout life; this result supports the idea that transmission can occur from mothers to cubs and also throughout adult life. For Florida males, the FOI was a decreasing function of puma age, indicating an increased risk of infection in the early years, and a decreased risk at older ages.

This research provides critical insight into pathogen transmission and impact in a secretive and solitary carnivore. Our findings shed light on the debate on whether FIV causes mortality in wild felids like puma, and our approach may be adopted for other diseases and species. The methodology we present can be used for identifying likely transmission routes of a pathogen and also estimating any disease‐associated mortality, both of which can be difficult to establish for wildlife diseases in particular.

 
more » « less
Award ID(s):
1654609
NSF-PAR ID:
10459260
Author(s) / Creator(s):
 ;  ;  ;  ;  ;  ;  ;  
Publisher / Repository:
Wiley Blackwell (John Wiley & Sons)
Date Published:
Journal Name:
Ecology and Evolution
Volume:
9
Issue:
19
ISSN:
2045-7758
Page Range / eLocation ID:
p. 11010-11024
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract

    Host sex is an important source of heterogeneity in the severity of epidemics. Pinpointing the mechanisms causing this heterogeneity can be difficult because differences in behaviour among sexes (e.g. greater territorial aggression in males) can bias exposure risk, obfuscating the role of immune function, which can lead to differences in pathology, in driving differential susceptibility between sexes. Thus, sex‐biased transmission driven by differences in immune function independent of behaviour is poorly understood, especially in non‐mammalian systems.

    Here we examine the previously unexplored potential for male‐biased pathology to affect transmission using an avian host–pathogen system. We employ a sex‐dependent multistate transmission model parameterized with isolated, individual‐based experimental exposures of domestic canaries and experimental transmission data of house finches.

    The experiment revealed that male birds have shorter incubation periods, longer recovery periods, higher pathogen burdens and greater disease pathology than females. Our model revealed that male‐biased pathology led to epidemic size rapidly increasing with the proportion of male birds, with a nearly 10‐fold increase in total epidemic size from an all‐female to an all‐male simulation.

    Our results demonstrate that female‐biased resistance, independent of male behaviour, can drive sex‐dependent transmission in wildlife, indicating that sex‐based differences in immune function, not just differences in exposure risk, can shape epidemic dynamics.

     
    more » « less
  2. Abstract

    Controlling persistent infectious disease in wildlife populations is an ongoing challenge for wildlife managers and conservationists worldwide, and chronic diseases in particular remain a pernicious problem.

    Here, we develop a dynamic pathogen transmission model capturing key features ofMycoplasma ovipneumoniaeinfection, a major cause of population declines in North American bighorn sheepOvis canadensis. We explore the effects of model assumptions and parameter values on disease dynamics, including density‐ versus frequency‐dependent transmission, the inclusion of a carrier class versus a longer infectious period, host survival rates, disease‐induced mortality and recovery rates and the epidemic growth rate. Along the way, we estimate the basic reproductive ratio,R0, forM. ovipneumoniaein bighorn sheep to fall between approximately 1.36 and 1.74.

    We apply the model to compare efficacies across a suite of management actions following an epidemic, including test‐and‐remove, depopulation‐and‐reintroduction, range expansion, herd augmentation and density reduction.

    Our results suggest that test‐and‐remove, depopulation‐and‐reintroduction and range expansion could help persistently infected bighorn sheep herds recovery following an epidemic. By contrast, augmentation could lead to worse outcomes than those expected in the absence of management. Other management actions that improve host survival or reduce disease‐induced mortality are also likely to improve population size and persistence of chronically infected herds.

    Synthesis and applications. Dynamic transmission models like the one employed here offer a structured, logical approach for exploring hypotheses, planning field experiments and designing adaptive management. We find that management strategies that removed infected animals or isolated them within a structured metapopulation were most successful at facilitating herd recovery from a low‐prevalence, chronic pathogen. Ideally, models like ours should operate iteratively with field experiments to triangulate on better approaches for managing wildlife diseases.

     
    more » « less
  3. Abstract

    Pathogen spread rates are determined, in part, by the performance of pathogens under altered environmental conditions and their ability to persist while switching among hosts and vectors.

    To determine the effects of new conditions (host, vector, and nutrient) on pathogen spread rate, we introduced a vector‐borne viral plant pathogen, Barley Yellow Dwarf Virus PAV (BYDV‐PAV) into hosts, vectors, and host nutrient supplies that it had not encountered for thousands of viral generations. We quantified pathogen prevalence over the course of two serial inoculations under the new conditions. Using individual‐level transmission rates from this experiment, we parameterized a dynamical model of disease spread and projected spread across host populations through a growing season.

    A change in nutrient conditions (increased supply of phosphorus) reduced viral transmission whereas shifting to a new vector or host species had no effect on infection prevalence. However, the reduction in the new nutrient environment was only temporary; infection prevalence recovered after the second inoculation.

    Synthesis. These results highlight how robust the pathogen, BYDV‐PAV, is to changes in its biotic and abiotic environment. Our study also highlights the need to quantify longitudinal infection information beyond snapshot assessments to project disease risk for pathogens in new environments.

     
    more » « less
  4. Abstract

    Heterogeneities in infections among host populations may arise through differences in environmental conditions through two mechanisms. First, environmental conditions may alter host exposure to pathogens via effects on survival. Second, environmental conditions may alter host susceptibility, making infection more or less likely if contact between a host and pathogen occurs. Further, host susceptibility might be altered through acquired resistance, which hosts can develop, in some systems, through exposure to dead or decaying pathogens and their metabolites. Environmental conditions may alter the rates of pathogen decomposition, influencing the likelihood of hosts developing acquired resistance.

    The present study primarily tests how environmental context influences the relative contributions of pathogen survival and per capita transmission on host infection prevalence using the amphibian chytrid fungus (Batrachochytrium dendrobatidis; Bd) as a model system. Secondarily, we evaluate how environmental context influences the decomposition of Bd because previous studies have shown that dead Bd and its metabolites can illicit acquired resistance in hosts. We conducted Bd survival and infection experiments and then fit models to discern how Bd mortality, decomposition and per capita transmission rates vary among water sources [e.g. artificial spring water (ASW) or water from three ponds].

    We found that infection prevalence differed among water sources, which was driven by differences in mortality rates of Bd, rather than differences in per capita transmission rates. Bd mortality rates varied among pond water treatments and were lower in ASW compared to pond water.

    These results suggest that variation in Bd infection dynamics could be a function of environmental factors in waterbodies that result in differences in exposure of hosts to live Bd. In contrast to the persistence of live Bd, we found that the rates of decomposition of dead Bd did not vary among water sources, which may suggest that exposure of hosts to dead Bd or its metabolites might not commonly vary among nearby sites. Ultimately, a mechanistic understanding of the environmental dependence of free‐living pathogens could lead to a deeper understanding of the patterns of outbreak heterogeneity, which could inform surveillance and management strategies.

     
    more » « less
  5. Abstract

    World‐wide, infectious diseases represent a major source of mortality in humans and livestock. For wildlife populations, disease‐induced mortality is likely even greater, but remains notoriously difficult to estimate—especially for endemic infections. Approaches for quantifying wildlife mortality due to endemic infections have historically been limited by an inability to directly observe wildlife mortality in nature.

    Here we address a question that can rarely be answered for endemic pathogens of wildlife: what are the population‐ and landscape‐level effects of infection on host mortality? We combined laboratory experiments, extensive field data and novel mathematical models to indirectly estimate the magnitude of mortality induced by an endemic, virulent trematode parasite (Ribeiroia ondatrae) on hundreds of amphibian populations spanning four native species.

    We developed a flexible statistical model that uses patterns of aggregation in parasite abundance to infer host mortality. Our model improves on previous approaches for inferring host mortality from parasite abundance data by (i) relaxing restrictive assumptions on the timing of host mortality and sampling, (ii) placing all mortality inference within a Bayesian framework to better quantify uncertainty and (iii) accommodating data from laboratory experiments and field sampling to allow for estimates and comparisons of mortality within and among host populations.

    Applying our approach to 301 amphibian populations, we found that trematode infection was associated with an average of between 13% and 40% population‐level mortality. For three of the four amphibian species, our models predicted that some populations experienced >90% mortality due to infection, leading to mortality of thousands of amphibian larvae within a pond. At the landscape scale, the total number of amphibians predicted to succumb to infection was driven by a few high mortality sites, with fewer than 20% of sites contributing to greater than 80% of amphibian mortality on the landscape.

    The mortality estimates in this study provide a rare glimpse into the magnitude of effects that endemic parasites can have on wildlife populations and our theoretical framework for indirectly inferring parasite‐induced mortality can be applied to other host–parasite systems to help reveal the hidden death toll of pathogens on wildlife hosts.

     
    more » « less