Camille Lebarbenchon

The ecological significance of manipulative parasites.

The diversity of ways in which host manipulation by parasites interferes with ecological and evolutionary processes governing biotic interactions has been recently documented, and indicates that manipulative parasites are full participants in the functioning of ecosystems. Phenotypic alterations in parasitised hosts modify host population ecology, apparent competition processes, food web structure and energy and nutrient flow between habitats, as well as favouring habitat creation. As is usually the case in ecology, these phenomena can be greatly amplified by a series of secondary consequences (cascade effects). Here we review the ecological relevance of manipulative parasites in ecosystems and propose directions for further research.

Water-borne transmission drives avian influenza dynamics in wild birds: the case of the 2005-2006 epidemics in the Camargue area.

Transmission and persistence of avian influenza viruses (AIV) among wildlife remains an unresolved issue because it depends both on the ecology of the host (e.g. population density, migration) and on the environment (e.g. AIV persistence in water). We have developed a mathematical model that accounts for both AIV epidemics and bird community dynamics. The model is parameterized using bird counts and AIV prevalence data. Results suggest that the transmission patterns driving the dynamics of infection at our study site (Camargue, South of France) involved both a density-dependent and a water-borne transmission processes. Water-borne transmission is, however, the main determinant of the disease dynamics and observed prevalence level. This pattern of transmission highlights the importance of the persistence of viral particles in water in AIV dynamics in wild birds.

Evolution of pathogens in a man-made world

Human activities have resulted in substantial, large‐scale environmental modifications, especially in the past century. Ecologists and evolutionary biologists are increasingly coming to realize that parasites and pathogens, like free‐living organisms, evolve as the consequence of these anthropogenic changes. Although this area now commands the attention of a variety of researchers, a broad predictive framework is lacking, mainly because the links between human activities, the environment and parasite evolution are complex. From empirical and theoretical examples chosen in the literature, we give an overview of the ways in which humans can directly or indirectly influence the evolution of different traits in parasites (e.g. specificity, virulence, polymorphism). We discuss the role of direct and indirect factors as diverse as habitat fragmentation, pollution, biodiversity loss, climate change, introduction of species, use of vaccines and antibiotics, ageing of the population, etc. We also present challenging questions for further research. Understanding the links between anthropogenic changes and parasite evolution needs to become a cornerstone of public health planning, economic development and conservation biology.

Spread of Avian Influenza Viruses by Common Teal (Anas crecca) in Europe

Since the recent spread of highly pathogenic (HP) H5N1 subtypes, avian influenza virus (AIV) dispersal has become an increasing focus of research. As for any other bird-borne pathogen, dispersal of these viruses is related to local and migratory movements of their hosts. In this study, we investigated potential AIV spread by Common Teal (Anas crecca) from the Camargue area, in the South of France, across Europe. Based on bird-ring recoveries, local duck population sizes and prevalence of infection with these viruses, we built an individual-based spatially explicit model describing bird movements, both locally (between wintering areas) and at the flyway scale. We investigated the effects of viral excretion duration and inactivation rate in water by simulating AIV spread with varying values for these two parameters. The results indicate that an efficient AIV dispersal in space is possible only for excretion durations longer than 7 days. Virus inactivation rate in the environment appears as a key parameter in the model because it allows local persistence of AIV over several months, the interval between two migratory periods. Virus persistence in water thus represents an important component of contamination risk as ducks migrate along their flyway. Based on the present modelling exercise, we also argue that HP H5N1 AIV is unlikely to be efficiently spread by Common Teal dispersal only.

Do distantly related parasites rely on the same proximate factors to alter the behaviour of their hosts

Phylogenetically unrelated parasites often increase the chances of their transmission by inducing similar phenotypic changes in their hosts. However, it is not known whether these convergent strategies rely on the same biochemical precursors. In this paper, we explored such aspects by studying two gammarid species (Gammarus insensibilis and Gammarus pulex; Crustacea: Amphipoda: Gammaridae) serving as intermediate hosts in the life cycle of two distantly related parasites: the trematode, Microphallus papillorobustus and the acanthocephalan, Polymorphus minutus. Both these parasite species are known to manipulate the behaviour of their amphipod hosts, bringing them towards the water surface, where they are preferentially eaten by aquatic birds (definitive hosts). By studying and comparing the brains of infected G. insensibilis and G. pulex with proteomics tools, we have elucidated some of the proximate causes involved in the parasite-induced alterations of host behaviour for each system. Protein identifications suggest that altered physiological compartments in hosts can be similar (e.g. immunoneural connexions) or different (e.g. vision process), and hence specific to the host–parasite association considered. Moreover, proteins required to alter the same physiological compartment can be specific or conversely common in both systems, illustrating in the latter case a molecular convergence in the proximate mechanisms of manipulation.

Parasitological Consequences of Overcrowding in Protected Areas

For the past several years, there has been growing interest in understanding the dynamics of parasites in ecosystems, as well as the diversity of ways in which they interfere with conservation and health preoccupations. Although it is widely recognized that many conservation practices (e.g., wildlife translocations, species removal, food supplementation) may be associated with parasite-related problems, less attention has been devoted to exploring the parasitological consequences of the overcrowding of animals in protected wildlife areas. Here, we discuss this important ecological/epidemiological problem, presenting at the same time an overview of the main questions and challenges in this field. Using empirical and theoretical examples chosen from the literature, we focus particularly on the interactions between the overcrowding of free living species and parasite population dynamics, the evolution of parasite virulence, the indirect effects on the structure of invertebrate communities, as well as the nutritional value of prey species. We argue that conservation policies should be aware more than ever of this problem, especially given the serious health risks currently posed by the spread of virulent viruses (e.g., avian influenza).

Water-seeking behavior in worm-infected crickets and reversibility of parasitic manipulation

One of the most fascinating examples of parasite-induced host manipulation is that of hairworms, first, because they induce a spectacular “suicide” water-seeking behavior in their terrestrial insect hosts and, second, because the emergence of the parasite is not lethal per se for the host that can live several months following parasite release. The mechanisms hairworms use to increase the encounter rate between their host and water remain, however, poorly understood. Considering the selective landscape in which nematomorph manipulation has evolved as well as previously obtained proteomics data, we predicted that crickets harboring mature hairworms would display a modified behavioral response to light. Since following parasite emergence in water, the cricket host and parasitic worm do not interact physiologically anymore, we also predicted that the host would recover from the modified behaviors. We examined the effect of hairworm infection on different behavioral responses of the host when stimulated by light to record responses from uninfected, infected, and ex-infected crickets. We showed that hairworm infection fundamentally modifies cricket behavior by inducing directed responses to light, a condition from which they mostly recover once the parasite is released. This study supports the idea that host manipulation by parasites is subtle, complex, and multidimensional.

Hairworm anti-predator strategy: a study of causes and consequences.

One of the most fascinating anti-predator responses displayed by parasites is that of hairworms (Nematomorpha). Following the ingestion of the insect host by fish or frogs, the parasitic worm is able to actively exit both its host and the gut of the predator. Using as a model the hairworm, Paragordius tricuspidatus, (parasitizing the cricket Nemobius sylvestris) and the fish predator Micropterus salmoïdes, we explored, with proteomics tools, the physiological basis of this anti-predator response. By examining the proteome of the parasitic worm, we detected a differential expression of 27 protein spots in those worms able to escape the predator. Peptide Mass Fingerprints of candidate protein spots suggest the existence of an intense muscular activity in escaping worms, which functions in parallel with their distinctive biology. In a second step, we attempted to determine whether the energy expended by worms to escape the predator is traded off against its reproductive potential. Remarkably, the number of offspring produced by worms having escaped a predator was not reduced compared with controls.

The Potential Distance of Highly Pathogenic Avian Influenza Virus Dispersal by Mallard, Common Teal and Eurasian Pochard

Waterbirds represent the major natural reservoir for low pathogenic (LP) avian influenza viruses (AIV). Among the wide diversity of subtypes that have been described, two of them (H5 and H7) may become highly pathogenic (HP) after their introduction into domestic bird populations and cause severe outbreaks, as is the case for HP H5N1 in South-Eastern Asia. Recent experimental studies demonstrated that HP H5N1 AIV infection in ducks does not necessarily have significant pathological effects. These results suggest that wild migratory ducks may asymptomatically carry HP AIV and potentially spread viruses over large geographical distances. In this study, we investigated the potential spreading distance of HP AIV by common teal (Anas crecca), mallard (A. platyrhynchos), and Eurasian pochard (Aythya ferina). Based on capture-mark-recapture method, we characterized their wintering movements from a western Mediterranean wetland (Camargue, South of France) and identified the potential distance and direction of virus dispersal. Such data may be crucial in determining higher-risk areas in the case of HP AIV infection detection in this major wintering quarter, and may serve as a valuable reference for virus outbreaks elsewhere.