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Exploring the influence of competition on arbovirus invasion risk in communities

Exploring the influence of competition on arbovirus invasion risk in communities

Afonso Dimas Martins, Quirine ten Bosch and J. A. P. Heesterbeek

Arbovirus outbreaks in communities are affected by how vectors, hosts and non-competent species interact. In this study, we investigate how ecological interactions between species and epidemiological processes influence the invasion potential of a vector-borne disease. We use an eco-epidemiological model to explore the basic reproduction number R0 for a range of interaction strengths in key processes, using West Nile virus infection to parameterize the model. We focus our analysis on intra and interspecific competition between vectors and between hosts, as well as competition with non-competent species. We show that such ecological competition has non-linear effects on R0 and can greatly impact invasion risk. The presence of multiple competing vector species results in lower values for R0 while host competition leads to the highest values of risk of disease invasion. These effects can be understood in terms of how the competitive pressures influence the vector-to-host ratio, which has a positive relationship with R0. We also show numerical examples of how vector feeding preferences become more relevant in high competition conditions between hosts. Under certain conditions, non-competent hosts, which can lead to a dilution effect for the pathogen, can have an amplification effect if they compete strongly with the competent hosts, hence facilitating pathogen invasion in the community.

1. Introduction

Vector-borne diseases are infections that result from pathogens that are transmitted by vectors to hosts. Mosquito vectors feed on animals as they require blood for completing their life cycle. During feeding, pathogens may be transmitted, causing infections in suitable hosts. West Nile Virus (WNV) is a neuroinvasive vector-borne disease transmitted by mosquitoe species, mainly of the Culex genus, to a range of animals, such as birds, horses, and humans. The symptoms in humans range from headaches and fever to death in critical situations [1]. The virus is maintained in circulation through enzootic amplification in transmission cycles between mosquito species and bird species. Other species, such as horses and humans, are only incidental hosts and are non-competent for the virus, i.e., they do not produce enough viremia to further contribute to transmission [1].

The dynamics of a pathogen in multi-species communities depend on the transmission routes available, as well as on the direct and indirect ecological interactions within and between species [24]. One type of interaction is competition, which in the case of vector-borne diseases can occur at different levels: between the vectors, the hosts, and potentially also between different pathogens. These competitive forces are characterized in different ways depending on the species involved. For example, at the level of the vectors, mosquitoes compete mostly during early larval stages when the resources are more limited [5]. At the host level, birds compete mostly for food, territory, and mating opportunities [67]. At the within-host level, pathogens can interact, for example, by releasing toxic compounds or otherwise interfere with the growth of their competitors [8]. All the species in their different roles affect the others in some way: pathogens are dependent on the vectors and the vertebrate hosts to be maintained in transmission; vectors rely on hosts for blood-feeding; and hosts suffer from fitness loss due to the vector-transmitted infections. Therefore, any changes in the species abundances or interaction strengths in the community can influence the network of pathogen transmission, and have impact on the probability of pathogen emergence.

Host species differ in their competence [9] with respect to the pathogen. Species that we will collectively refer to as ‘non-competent species’ abound in the natural habitat of any pathogen, for example the dead-end host species and species that are not susceptible. Such non-competent species interact ecologically with host species of various degrees of competence and influence the abundance and dynamics of host species. Non-competent species may therefore influence pathogen dynamics indirectly and also affect invasion risk upon introduction, potentially both positively and negatively. For vector-borne pathogens, additional interactions become relevant, for example related to blood meals necessary for completion of the vector life cycle. This may involve host species of different competence with respect to the pathogen in question, as well as dead-end host species and species not susceptible to the pathogen. It is known that vector-borne pathogens are sensitive to biodiversity [10], however whether pathogens end up benefiting from changes in biodiversity depends on many factors [11]. For example, non-competent species or very weakly competent host species can dilute mosquito bites on competent host species. These bites do not contribute to maintaining the pathogen cycle. It is, therefore, important to explore a more diverse collection of species in a community to better understand outbreak risk in complex natural environments.

Our aim here is to show that ecological interactions may influence host, vector and pathogen dynamics in commonly adopted modelling descriptions of mosquito-borne pathogen systems. We focus on invasion dynamics. In this study, we use WNV as a motivating case study for the exploration of invasion risk of a mosquito-borne virus in a multi-species setting. Like many other vector-borne infections, WNV is expanding its range, with small outbreaks in areas that are at the borders of the current endemic range. For such small outbreaks it is important to understand how local conditions can be conducive to onward transmission. For these reasons, we focus in this study on invasion risk, rather than on long-term dynamics. We construct a low-dimensional model that captures explicit competition acting at different levels. The focus is on intra- and interspecific competition as the main ecological interaction. Marini et al. 2017 [12], for example, studied the effects of competition at the host level on the invasion risk of WNV. In our study, we include not only competition between hosts, but also competition between mosquito species. This is also further extended to more complex scenarios such as the presence of non-competent vectors and non-competent vertebrate species, and their respective competitive pressures on the competent species. This approach allows us to study the potential effects of species interactions that are difficult to quantify in the field, such as competition at different trophic levels and vector feeding preferences. The invasion risk is quantified by the basic reproduction number R0 [13]. Because our interest is in showing the effects of ecological interactions in common settings for the pathogen, we consider situations where, apart from those interactions, there are no impediments to invasion. The steps taken here to obtain insight into R0 can be generalized to other systems with multiple vector, host and non-host species, as well as to additional types of ecological interaction.

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Source: PLOS ONE

Date: October 25th 2022

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This project 'Preparing for vector-borne virus outbreaks in a changing world: a One Health Approach' (NWA. 1160.1S.210) is (partly) financed by the Dutch Research Council (NWO).

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