Discussion
Deciphering arboviral emergence within insular ecosystems

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Abstract

The spatial dynamics of zoonotic arthropod-borne viruses is a fashionable though challenging topic. Inter-human local transmission of a given arbovirus during an outbreak and its spread over large distances are considered as key parameters of emergence. Here, we suggest that insular ecosystems provide ideal natural “laboratory” conditions to uncouple local transmission from long distance spread, and differentiate these two processes. Due to geographic isolation, often-limited land surface area and relatively homogenous ecosystems, oceanic islands display low species richness and often-high levels of endemism. These aspects provide the means for comprehensive entomological surveys and investigations of original host/pathogen interactions. In addition, islands are interconnected through discrete anthropogenic and non-anthropogenic exchanges: whilst islands maintain a substantial level of human and domestic animal exchange with other neighbouring or distant territories, they also comprise dispersal and migratory pathways of volant organisms (insects, birds and bats). Hence, both anthropogenic and non-anthropogenic exchanges in island systems are easier to identify and investigate than in continuous, continental systems. Finally, island ecosystems tend to be notably simpler, more prone to invasive taxa and, therefore, easier to document the colonization or displacement of vector species. These different aspects are presented and overlaid upon the spread of arboviruses within two distinct insular systems: islands of Polynesia and the south-western Indian Ocean. The former have been repeatedly affected by Dengue fever epidemics, while the latter recently suffered four successive epidemics, probably of east African origin, three of which involved the emerging viruses Chikungunya, Rift Valley and Dengue fever. Here, we review some new insights into arboviral spread and evolution associated with investigations that followed these epidemics, as well as several aspects that make insular ecosystems favourable to the investigation of arboviral transmission and spread.

Highlights

► We explore the properties of oceanic islands that simplify emergence investigation. ► Islands host low species richness facilitating vector and reservoir species surveys. ► Islands are prone to species invasion allowing the monitoring of vector displacement. ► Limited inter island connections facilitate pathogens/vectors gene flow studies.

Introduction

There are several driving factors that can be involved in the emergence of an arthropod-borne viral disease (Woolhouse and Gowtage-Sequeria, 2005). These drivers include environmental changes, which can augment local transmission by modifying reservoirs and vector abundance and directly modify contact between the vector and humans. Alternatively, a virus may spread over a large area, or be transmitted between two geographically distant ecosystems by processes such as human/cattle transportation or animal migration. Hence, local transmission and long distance spread are two key considerations when investigating a viral outbreak, though they are both often difficult to address. Deciphering epidemic emergence ultimately requires the surveillance of virtually all biological participants, which is not an easy task when facing a large number of putatively involved species. Tracking a pathogen around the world is also challenging although phylogeographic approaches can be both informative and insightful in this regard. Here, we propose that insular ecosystems (particularly true oceanic islands, i.e. small land areas formed de novo and surrounded by major bodies of water) provide an ideal natural laboratory for the investigation of arboviral emergence, as they allow the influence of local viral transmission to be distinguished from long distance geographical spread (either natural or anthropogenic). Importantly, the unique ecological properties of insular ecosystems, which are reviewed herein, allow for independent experimental observation of these two distinct processes. Finally, these insular particularities are associated with epidemiological specificities as shown by the two chosen island case studies described below.

The ability of zoonotic arboviruses to cause human epidemics or outbreaks relies primarily on the concomitant presence of a naïve human population and of an arthropod-species able to ensure efficient inter-human transmission. These sometimes-explosive episodes require a timely and efficient epidemiological investigation to understand the basic parameters of transmission, which are critical to orient effective control measures. One key question is the origin of the incriminated arbovirus, which might have been maintained for considerable time within a local animal species, acting as a reservoir. In this case, its emergence in humans may result from a decrease in immunity of the exposed human population, as suggested by cyclic patterns of Chikungunya epidemics observed in southeast Asia (Pialoux et al., 2007). The entire local human population may be otherwise naïve for the pathogen but an unprecedented contact may be facilitated by anthropogenic environmental changes. Ecological changes associated with land use and economic development (including deforestation/reforestation, flood/drought or climate change) are known drivers of emergence; they can facilitate direct or indirect contacts between humans and reservoirs, and/or impact on the biology and abundance of both vector and reservoir taxa (Morse, 1995). In these cases, viral emergence (or re-emergence) relies solely on biological actors already present in a limited geographical zone.

Alternatively, the pathogen may have been recently introduced through human activities into the geographical area in question or naturally dispersed into the region via a number of different means. Hence, the mode of dispersal can be schematically separated in two distinct classes: human-dependent and human-independent. The first category includes, for example, virus importation through infected travellers or international animal trade. In addition, one must consider the human-mediated displacements of putative reservoirs. There is a substantial body of evidence for early historical translocations of commensal rodents by humans across the planet (Matisoo-Smith and Robins, 2004, Whisson et al., 2007) and the on-going human-mediated transportation of rodents in the millions of containers that are shipped worldwide each year is a large-scale potential precursor to viral emergence. The second category involves natural movements of animals associated with annual or regular migration or dispersal that is more irregular.

These aspects have been much less investigated despite being highlighted more than 50 years ago by the late Hoogstraal (1961). He proposed that migrating birds, which displace over long distances irrespective of international borders, might transport pathogens. In recent years, this notion has been widely supported following the H5N1 epidemics (Gilbert et al., 2006, Keawcharoen et al., 2008). In addition, Hoogstraal specifically proposed that infected ticks carried by migrating hosts, could be carried across considerable distances and between continents. Subsequently, these air-borne tick displacements were proposed to be associated with the long distance dispersal of the Crimean-Congo hemorrhagic fever virus (Morikawa et al., 2007). With the acumen typical of this researcher, Hoogstraal stated the importance of multidisciplinary investigations to unravel zoonotic processes; an aspect we discuss below. New technologies have clearly revealed the extent of dispersal for certain animals. For example, a satellite monitored radio-collar study of large fruit bats (Family Pteropodidae), which are known reservoirs of numerous viruses (Gilbert et al., 2006, Keawcharoen et al., 2008), showed that they can travel hundreds of kilometres each year between roosting and feeding sites and cross international borders (Epstein et al., 2009).

It is important to consider what can happen following an emergence episode. The arbovirus under consideration can (i) vanish in the absence of a suitable reservoir, (ii) be maintained locally for a relatively long inter-epidemic period in the presence of a permissive reservoir (endemization), or (iii) be displaced to another region where its transmission to susceptible human populations will rely on the presence of a competent (i.e. capable of replicating and transmitting a given parasite) arthropod vector. Several intermediate scenarios can be proposed beside the three mentioned above. For instance, in a new ecological context, a virus may at first be poorly replicated and inefficiently transmitted by a local vector species until it adapts to the local environment or finds an alternative vector species more capable of supporting efficient viral replication. Such an intermediate situation occurred on the islands of the south-western Indian Ocean (SWIO) during the Chikungunya epidemics of 2005 and 2006 (de Lamballerie et al., 2008, Schuffenecker et al., 2006).

We provide here a simplified scheme for the emergence and spread of viruses since several other key parameters, including, for example, temperature, alteration of vectorial competence or feeding behaviour as highlighted by West Nile Virus epidemic that occurred in North America (Dohm et al., 2002, Kilpatrick et al., 2006, Moudy et al., 2007, Rosenberg, 2011), may also be important to take into consideration. Information on the movements and biology of the organisms involved in viral transmission is critical to understand fully the driving factors behind a viral outbreak and this is best investigated using a multidisciplinary approach, allowing the integration of data from ecological, microbiological and epidemiological studies.

The classical interpretation of pathogen transmission processes is based on Newtonian physics: no matter how complex a transmission chain may be, one should investigate it by dissecting each simple interaction while ignoring or neglecting the system as a whole (Wulff, 1999). The investigation of complex systems has slowly evolved as a new paradigm in contemporary epidemiology. Epidemic phenomena are complex as the systems involved continuously change in response to exogenous (e.g., seasonal variation in the contact rate, life cycles) as well as endogenous factors (e.g., herd immunity, prevalence of cases). One method for understanding aspects of the associated complexity is to investigate regions of the globe where hypotheses can be tested within a relatively simplified or limited biological system. Insular ecosystems such as those of oceanic islands are optimal zones for these investigations.

Islands are discrete units with clear boundaries, resting in a matrix of open water, which is normally an inhospitable barrier for vectors and possible reservoir organisms to pass through. Hence, islands are ideal natural laboratories for the study of evolution and ecology (Emerson, 2002) and, in particular facilitate, the biogeographical study of host–parasite interactions. The ecological specificities of oceanic islands, in many cases a direct result of their geographical isolation, make them attractive models for the investigation of arboviral dynamics.

First, it has long been recognized that islands, with rare exceptions, have relatively fewer species of plants, amphibians, reptiles, birds or mammals than adjacent continental regions (Abbott, 1978). This relatively low-species richness depends on several factors including the degree of isolation (distance for source populations and geological history), island area, climate (tropical vs. temperate), and level of human activity. MacArthur and Wilson (1967) built on early principles of population ecology and genetics to explain how in combination distance (from a source-island or continent) and surface area regulate the balance between immigration and extinction of island populations. Extinction rates on islands would be higher than in continental areas, as average population size is smaller and, thus, more prone to drastic declines. In addition, the chance of recolonization of island populations after initial extinction, particularly on small oceanic islands, would be notably less than in equivalent continental zones of the same surface area. Hence, geologically recent, small, and human-modified oceanic islands are expected to shelter a low number of species, which in turn facilitates the investigation of entire community assemblages. For example, it is possible to screen virtually all vector and reservoir species that are potentially involved in local viral transmission.

Second, true oceanic islands have speciation rates that are greater than the rate of immigration; hence, their biota contains many endemic species and in turn, a high level of microbial endemism is also expected, although this has been poorly investigated. The low-species richness combined with the higher rate of endemism provides a notably simplified study of native taxa (including parasite, host, and reservoir or vector species). We predict that, given the differences outlined above between island and continental regions, the locally occurring parasite communities will show different trajectories associated with co-evolution processes. These could provide new insights into the general principles of multilayered interactions.

Finally, oceanic islands are prone to biological invasion: species introductions (either deliberate or accidental) are disproportionately more pervasive on islands than on continental areas (Elton, 2000). These invasive species, including parasite, reservoir, and vector taxa, may affect the local biota. Monitoring of introduced animal populations and identification of known and unknown sheltered pathogens may help to understand diffusion and potentially the emergence of arboviral diseases. McKinney proposes an active surveillance of (i) domestic and laboratory animals, (ii) animals from the pet trade and meat markets, (iii) pest species and managed game species, and (iv) the so-called urban adapters and exploiters (McKinney, 2002). Introduced species have a considerable chance of being sources of emerging vector-borne and zoonotic pathogens. The active monitoring of potential emerging pathogens would be greatly facilitated by focusing on oceanic islands, which typically have limited international airport and harbour services.

In addition to the properties of insular ecosystems outlined above, the strong influence of oceanic currents and the low elevation of oceanic islands make them disproportionately more sensitive to climate change than continental areas. Indeed, natural and anthropogenic perturbations deeply affect island biodiversity, which in turn has been proposed to impact the emergence and transmission of infectious diseases (Keesing et al., 2010). Altogether, the particularities of host–parasite co-evolution on islands may lead to and help maintain idiosyncratic changes of both insular-parasite virulence and transmission. The last decade has provided some scarce but informative data on arboviral spread within insular ecosystems, which are the subject of the following two case studies.

Section snippets

The spread of dengue in French Polynesia

Dengue virus (DENV) is a major public-health concern on many islands in the Pacific Ocean (Singh et al., 2005). French Polynesia (FP), composed of more than one hundred remote islands and islets, has experienced successive dengue epidemic episodes involving all four DENV serotypes. In 2000, outbreaks of DENV in countries of the south Pacific were caused by DENV-1 (Cao-Lormeau et al., 2011). DENV-I reintroduction in FP in 2001, where the population had not been exposed for over 20 years, resulted

Conclusions

As detailed here, oceanic islands are isolated landmasses generally displaying low-species richness, high endemism and often-heterogeneous distributions of vector species; these different aspects facilitate the investigation of arboviral transmission. In addition, islands generally have a limited number of international harbours and airports, which also simplifies the identification of sites where viruses have passed through and been introduced. Investigations carried out in both Polynesian and

Acknowledgements

We are thankful to Christian Devaux for stimulating this paper, to Coralie Foray for preparing Fig. 1 and to David Wilkinson for critical comments on the manuscript. This work was supported by FEDER Réunion, Programme Opérationnel de Coopération Territoriale (2007–2013) Faune Sauvage Océan Indien #31189 and European Community FP7 Capacity RegPot Run-Emerge.

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