Dissecting a wildlife disease hotspot: the impact of multiple host species, environmental transmission and seasonality in migration, breeding and mortality

Brown, V. L.; Drake, John M.; Stallknecht, David E.; Brown, Justin D.; Pedersen, Kerri; Rohani, Pejman

doi:10.1098/rsif.2012.0804

Cited by 32 publications

(38 citation statements)

References 56 publications

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“…Influenza virus circulation and long-term maintenance in avian populations is probably determined by a combination of explosive, essentially direct transmission and episodic contributions from the environmental reservoir [19]. The precise impact of environmental transmission is thought to be determined by virus-specific durability under different abiotic conditions.…”

Section: Introductionmentioning

confidence: 99%

Trade-offs between and within scales: environmental persistence and within-host fitness of avian influenza viruses

et al. 2014

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Trade-offs between different components of a pathogen's replication and transmission cycle are thought to be common. A number of studies have identified trade-offs that emerge across scales, reflecting the tension between strategies that optimize within-host proliferation and large-scale population spread. Most of these studies are theoretical in nature, with direct experimental tests of such cross-scale trade-offs still rare. Here, we report an analysis of avian influenza A viruses across scales, focusing on the phenotype of temperaturedependent viral persistence. Taking advantage of a unique dataset that reports both environmental virus decay rates and strain-specific viral kinetics from duck challenge experiments, we show that the temperature-dependent environmental decay rate of a strain does not impact within-host virus load. Hence, for this phenotype, the scales of within-host infection dynamics and between-host environmental persistence do not seem to interact: viral fitness may be optimized on each scale without cross-scale trade-offs. Instead, we confirm the existence of a temperature-dependent persistence trade-off on a single scale, with some strains favouring environmental persistence in water at low temperatures while others reduce sensitivity to increasing temperatures. We show that this temperature-dependent trade-off is a robust phenomenon and does not depend on the details of data analysis. Our findings suggest that viruses might employ different environmental persistence strategies, which facilitates the coexistence of diverse strains in ecological niches. We conclude that a better understanding of the transmission and evolutionary dynamics of influenza A viruses probably requires empirical information regarding both within-host dynamics and environmental traits, integrated within a combined ecological and within-host framework.

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Section: Introductionmentioning

confidence: 99%

Trade-offs between and within scales: environmental persistence and within-host fitness of avian influenza viruses

et al. 2014

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“…IAV in waterfowl (Brown et al . ; Hénaux et al . ), cowpox and tuberculosis in voles Microtus agrestis (Cavanagh et al .…”

Section: Introductionmentioning

confidence: 99%

Capturing individual‐level parameters of influenza A virus dynamics in wild ducks using multistate models

Avril

Grosbois

Latorre‐Margalef

et al. 2016

Journal of Applied Ecology

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Disease prevalence in wildlife is governed by epidemiological parameters (infection and recovery rates) and response to infection, both of which vary within and among individual hosts. Studies quantifying these individual-scale parameters and documenting their source of variation in wild hosts are fundamental for predicting disease dynamics. Such studies do not exist for the influenza A virus (IAV), despite its strong impact on the global economy and public health. Using capture–recaptures of 3500 individual mallards Anas platyrhynchos during seven migration seasons at a stopover site in southern Sweden, we provide the first empirical description of the individual-based mechanisms of IAV dynamics in a wild reservoir host. For most years, prevalence and risk of IAV infection peaked at a single time during the autumn migration season, but the timing, shape and intensity of the infection curve showed strong annual heterogeneity. In contrast, the seasonal pattern of recovery rate only varied in intensity across years. Adults and juveniles displayed similar seasonal patterns of infection and recovery each year. However, compared to adults, juveniles experienced twice the risk of becoming infected, whereas recovery rates were similar across age categories. Finally, we did not find evidence that infection influenced the timing of emigration. Synthesis and applications. Our study provides robust empirical estimates of epidemiological parameters for predicting influenza A virus (IAV) dynamics. However, the strong annual variation in infection curves makes forecasting difficult. Prevalence data can provide reliable surveillance indicators as long as they catch the variation in infection risk. However, individual-based monitoring of infection is required to verify this assumption in areas where surveillance occurs. In this context, monitoring of captive sentinel birds kept in close contact with wild birds is useful. The fact that infection does not impact the timing of migration underpins the potential for mallards to spread viruses rapidly over large geographical scales. Hence, we strongly encourage IAV surveillance with a multistate capture–recapture approach along the entire migratory flyway of mallards. (Résumé d'auteur

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“…; Brown et al . ). Discerning the signal of chronic shedders operating in inter‐epidemic troughs from epidemic drivers operating through multiple epidemic cycles remains a challenge in wildlife systems [(Lloyd‐Smith et al .…”

Section: Introductionmentioning

confidence: 97%

Detecting signals of chronic shedding to explain pathogen persistence:Leptospira interrogansinCalifornia sea lions

Buhnerkempe

Prager

Strelioff

et al. 2017

Journal of Animal Ecology

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Identifying mechanisms driving pathogen persistence is a vital component of wildlife disease ecology and control. Asymptomatic, chronically infected individuals are an oft-cited potential reservoir of infection, but demonstrations of the importance of chronic shedding to pathogen persistence at the population-level remain scarce. Studying chronic shedding using commonly collected disease data is hampered by numerous challenges, including short-term surveillance that focuses on single epidemics and acutely ill individuals, the subtle dynamical influence of chronic shedding relative to more obvious epidemic drivers, and poor ability to differentiate between the effects of population prevalence of chronic shedding vs. intensity and duration of chronic shedding in individuals. We use chronic shedding of Leptospira interrogans serovar Pomona in California sea lions (Zalophus californianus) as a case study to illustrate how these challenges can be addressed. Using leptospirosis-induced strands as a measure of disease incidence, we fit models with and without chronic shedding, and with different seasonal drivers, to determine the time-scale over which chronic shedding is detectable and the interactions between chronic shedding and seasonal drivers needed to explain persistence and outbreak patterns. Chronic shedding can enable persistence of L. interrogans within the sea lion population. However, the importance of chronic shedding was only apparent when surveillance data included at least two outbreaks and the intervening inter-epidemic trough during which fadeout of transmission was most likely. Seasonal transmission, as opposed to seasonal recruitment of susceptibles, was the dominant driver of seasonality in this system, and both seasonal factors had limited impact on long-term pathogen persistence. We show that the temporal extent of surveillance data can have a dramatic impact on inferences about population processes, where the failure to identify both short- and long-term ecological drivers can have cascading impacts on understanding higher order ecological phenomena, such as pathogen persistence.

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Dissecting a wildlife disease hotspot: the impact of multiple host species, environmental transmission and seasonality in migration, breeding and mortality

Cited by 32 publications

References 56 publications

Trade-offs between and within scales: environmental persistence and within-host fitness of avian influenza viruses

Trade-offs between and within scales: environmental persistence and within-host fitness of avian influenza viruses

Capturing individual‐level parameters of influenza A virus dynamics in wild ducks using multistate models

Detecting signals of chronic shedding to explain pathogen persistence:Leptospira interrogansinCalifornia sea lions

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