Robert Poulin

University of Otago, Taieri, Otago, New Zealand

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Publications (450)1358.37 Total impact

  • Robert Poulin, Clément Lagrue
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    ABSTRACT: SUMMARY The fundamental assumption underpinning the evolution of numerous adaptations shown by parasites with complex life cycles is that huge losses are incurred by infective stages during certain transmission steps. However, the magnitude of transmission losses or changes in the standing crop of parasites passing from upstream (source) to downstream (target) hosts have never been quantified in nature. Here, using data from 100 pairs of successive upstream-downstream life stages, from distinct populations representing 10 parasite species, we calculated the total density per m2 of successive life stages. We show that clonal amplification of trematodes in their first intermediate host leads to an average 4-fold expansion of numbers of individuals at the next life stage, when differences in the longevity of successive life stages are taken into account. In contrast, trophic transmission to the definitive host results in almost no numerical change for trematodes, but possibly in large decreases for acanthocephalans and nematodes, though a correction for longevity was not possible for the latter groups. Also, we only found a positive association between upstream and downstream stage densities for transmission involving free-swimming cercariae in trematodes, suggesting a simple output-recruitment process. For trophic transmission, there was no coupling between downstream and upstream parasite densities. These first quantitative estimates of ontogenetic rises and falls in numbers under natural conditions provide new insights into the selective pressures acting on parasites with complex cycles.
    Parasitology 01/2015; · 2.36 Impact Factor
  • Clément Lagrue, Robert Poulin, Joel E Cohen
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    ABSTRACT: How do the lifestyles (free-living unparasitized, free-living parasitized, and parasitic) of animal species affect major ecological power-law relationships? We investigated this question in metazoan communities in lakes of Otago, New Zealand. In 13,752 samples comprising 1,037,058 organisms, we found that species of different lifestyles differed in taxonomic distribution and body mass and were well described by three power laws: a spatial Taylor's law (the spatial variance in population density was a power-law function of the spatial mean population density); density-mass allometry (the spatial mean population density was a power-law function of mean body mass); and variance-mass allometry (the spatial variance in population density was a power-law function of mean body mass). To our knowledge, this constitutes the first empirical confirmation of variance-mass allometry for any animal community. We found that the parameter values of all three relationships differed for species with different lifestyles in the same communities. Taylor's law and density-mass allometry accurately predicted the form and parameter values of variance-mass allometry. We conclude that species of different lifestyles in these metazoan communities obeyed the same major ecological power-law relationships but did so with parameters specific to each lifestyle, probably reflecting differences among lifestyles in population dynamics and spatial distribution.
    Proceedings of the National Academy of Sciences 12/2014; · 9.81 Impact Factor
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    ABSTRACT: Despite their very different historical origins as scientific disciplines, parasitology and marine ecology have already combined successfully to make important contributions to our understanding of the functioning of natural ecosystems. For example, robust assessments of the contribution of parasites to ecosystem biomass and energetics, and of their impact on community-wide biodiversity and food web structure, have all been made for the first time in marine systems. Nevertheless, for the marriage between parasitology and marine ecology to remain fruitful, several challenges must first be overcome. We discuss seven such challenges on the road to a greater synergy between these disciplines: (1) Raising awareness of parasitism as an ecological force by increasing the proportion of articles about parasites and diseases in marine ecology journals; (2) Making greater use of theory and conceptual frameworks from marine ecology to guide parasitological research; (3) Speeding up or at least maintaining the current rate at which marine parasites are found and described; (4) Elucidating a greater proportion of life cycles in all major groups of marine parasites; (5) Increasing the number of host-parasite model systems on which our knowledge is based; (6) Extending parasitological research offshore and into ocean depths; (7) Developing, as needed, new epidemiological theory and transmission models for the marine environment. None of these challenges is insurmountable, and addressing just a few of them should guarantee that parasitology and marine ecology will continue to join forces and make further substantial contributions.
    Journal of Sea Research 11/2014; in press(on-line). · 1.86 Impact Factor
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    ABSTRACT: 1. Meta-analysis has become a standard way of summarizing empirical studies in many fields, including ecology and evolution. In ecology and evolution, meta-analyses comparing two groups (usually experimental and control groups) have almost exclusively focused on comparing the means, using standardized metrics such as Cohen's / Hedges’ d or the response ratio.2. However, an experimental treatment may not only affect the mean but also the variance. Investigating differences in the variance between two groups may be informative, especially when a treatment influences the variance in addition to or instead of the mean.3. In this paper, we propose the effect size statistic, lnCVR (the natural logarithms of the ratio between the coefficients of variation, CV, from two groups), which enables us to meta-analytically compare differences between the variability of two groups. We illustrate the use of lnCVR with examples from ecology and evolution.4. Further, as an alternative approach to the use of lnCVR, we propose the combined use of (the log standard deviation) and (the log mean) in a hierarchical (linear mixed) model. The use of with overcomes potential limitations of lnCVR and it provides a more flexible, albeit more complex, way to examine variation beyond two group comparisons. Relevantly, we also refer to the potential use of and lnCV (the log CV) in the context of comparative analysis.5. Our approaches to compare variability could be applied to already published meta-analytic datasets that compare two-group means to uncover potentially overlooked effects on the variance. Additionally, our approaches should be applied to future meta-analyses, especially when one suspects a treatment has an effect not only on the mean, but also on the variance. Notably, the application of the proposed methods extends beyond the fields of ecology and evolution.This article is protected by copyright. All rights reserved.
    Methods in Ecology and Evolution 11/2014; 6(2). · 5.32 Impact Factor
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    ABSTRACT: Littorinid snails are one particular group of gastropods identified as important intermediate hosts for a wide range of digenean parasite species, at least throughout the Northern Hemisphere. However nothing is known of trematode species infecting these snails in the Southern Hemisphere. This study is the first attempt at cataloguing the digenean parasites infecting littorinids in New Zealand. Examination of over 5,000 individuals of two species of the genus Austrolittorina Rosewater, A. cincta Quoy & Gaimard and A. antipodum Philippi, from intertidal rocky shores, revealed infections with four digenean species representative of a diverse range of families: Philophthalmidae Looss, 1899, Notocotylidae Lühe, 1909, Renicolidae Dollfus, 1939 and Microphallidae Ward, 1901. This paper provides detailed morphological descriptions of the cercariae and intramolluscan stages of these parasites. Furthermore, partial sequences of the 28S rRNA gene and the mitochondrial gene cytochrome c oxidase subunit 1 (cox1) for varying numbers of isolates of each species were obtained. Phylogenetic analyses were carried out at the superfamily level and along with the morphological data were used to infer the generic affiliation of the species.
    Systematic Parasitology 10/2014; 89(2). · 1.04 Impact Factor
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    Katie O’Dwyer, Aaron Lynch, Robert Poulin
    Journal of Experimental Marine Biology and Ecology 09/2014; 458:1–5. · 2.48 Impact Factor
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    ABSTRACT: SUMMARY Host specificity is a fundamental component of a parasite's life history. However, accurate assessments of host specificity, and the factors influencing it, can be obscured by parasite cryptic species complexes. We surveyed two congeneric species of intertidal snail intermediate hosts, Zeacumantus subcarinatus and Zeacumantus lutulentus, throughout New Zealand to identify the number of genetically distinct echinostome trematodes infecting them and determine the levels of snail host specificity among echinostomes. Two major echinostome clades were identified: a clade consisting of an unidentified species of the subfamily Himasthlinae and a clade consisting of five species of the genus Acanthoparyphium. All five Acanthoparyphium species were only found in a single snail species, four in Z. subcarinatus and one in Z. lutulentus. In contrast, the Himasthlinae gen. sp. was found in both hosts, but was more prevalent in Z. lutulentus (97 infections) than Z. subcarinatus (10 infections). At least two of the Acanthoparyphium spp. and the Himasthlinae gen. sp. are widespread throughout New Zealand, and can therefore encounter both snail species. Our results suggest that host specificity is determined by host-parasite incompatibilities, not geographic separation, and that it can evolve in different ways in closely related parasite lineages.
    Parasitology 08/2014; 142(02):1-10. · 2.36 Impact Factor
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    ABSTRACT: Climates are changing worldwide, and populations are under selection to adapt to these changes. Changing temperature, in particular, can directly impact ectotherms and their parasites, with potential consequences for whole ecosystems. The potential of parasite populations to adapt to climate change largely depends on the amount of genetic variation they possess in their responses to environmental fluctuations. This study is, to our knowledge, the first to look at differences among parasite genotypes in response to temperature, with the goal of quantifying the extent of variation among conspecifics in their responses to increasing temperature. Snails infected with single genotypes of the trematode Maritrema novaezealandensis were sequentially acclimatized to two different temperatures, 'current' (15° C) and 'elevated' (20° C), over long periods. These temperatures are based on current average field conditions in the natural habitat and those predicted to occur during the next few decades. The output and activity of cercariae (free-swimming infective stages emerging from snails) were assessed for each genotype at each temperature. The results indicate that, on average, both cercarial output and activity are higher at the elevated acclimation temperature. More importantly, the output and activity of cercariae are strongly influenced by a genotype-by-temperature interaction, such that different genotypes show different responses to increasing temperature. Both the magnitude and direction (increase or decrease) of responses to temperature varied widely among genotypes. Therefore, there is much potential for natural selection to act on this variation, and predicting how the trematode M. novaezealandensis will respond to the climate changes predicted for the next century will prove challenging.
    International Journal for Parasitology 07/2014; · 3.40 Impact Factor
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    ABSTRACT: Complexes of cryptic species are rapidly being discovered in many parasite taxa, including trematodes. However, after they are found, cryptic species are rarely distinguished from each other with respect to key ecological or life history traits. In this study, we applied an integrative taxonomic approach to the discovery of cryptic species within Stegodexamene anguillae, a facultatively progenetic trematode common throughout New Zealand. The presence of cryptic species was determined by the genetic divergence found in the mitochondrial cytochrome c oxidase I (COI) gene, the 16S rRNA gene and the nuclear 28S gene, warranting recognition of two distinct species and indicating a possible third species. Speciation was not associated with geographic distribution or microhabitat within the second intermediate host; however frequency of the progenetic reproductive strategy (and the truncated life cycle associated with it) was significantly greater in one of the lineages. Therefore, two lines of evidence, molecular and ecological, support the distinction between these two species and suggest scenarios for their divergence.
    International Journal for Parasitology 07/2014; · 3.40 Impact Factor
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    ABSTRACT: Statistical correlations of biodiversity patterns across multiple trophic levels have received considerable attention in various types of interacting assemblages, forging a universal understanding of patterns and processes in free-living communities. Host–parasite interactions present an ideal model system for studying congruence of species richness among taxa as obligate parasites are strongly dependent upon the availability of their hosts for survival and reproduction while also having a tight coevolutionary relationship with their hosts. The present meta-analysis examined 38 case studies on the relationship between species richness of hosts and parasites, and is the first attempt to provide insights into the patterns and causal mechanisms of parasite biodiversity at the community level using meta-regression models. We tested the distinct role of resource (i.e. host) availability and evolutionary co-variation on the association between biodiversity of hosts and parasites, while spatial scale of studies was expected to influence the extent of this association. Our results demonstrate that species richness of parasites is tightly correlated with that of their hosts with a strong average effect size (r= 0.55) through both host availability and evolutionary co-variation. However, we found no effect of the spatial scale of studies, nor of any of the other predictor variables considered, on the correlation. Our findings highlight the tight ecological and evolutionary association between host and parasite species richness and reinforce the fact that host–parasite interactions provide an ideal system to explore congruence of biodiversity patterns across multiple trophic levels.
    Ecography 07/2014; · 4.21 Impact Factor
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    ABSTRACT: Male dimorphism has been reported across different taxa and is usually expressed as the coexistence of a larger morph with exaggerated male traits and a smaller one with reduced traits. The evolution and maintenance of male dimorphism are still poorly understood for several of the species in which it has been observed. Here, we analyse male dimorphism in several species of reptile parasitic nematodes of the genus Spauligodon, in which a major male morph (exaggerated morph), which presents the traditional male morphological traits reported for this taxon, coexists with a minor morph with reduced morphological traits (i.e. reduced genital papillae) resembling more closely the males of the sister genus Skrjabinodon than Spauligodon major males. Because of the level of uncertainty in the results of ancestral state reconstruction, it is unclear if the existence of male dimorphism in this group represents independent instances of convergent evolution or an ancestral trait lost multiple times. Also, although the number of major males per host was positively correlated with the number of females, the same did not hold true for minor males, whose presence was not associated with any other ecological factor. Nevertheless, the existence of male dimorphism in Spauligodon nematodes is tentatively interpreted as resulting from alternative reproductive tactics, with differences in presence and number of individuals as indicators of differences in fitness, with the lower numbers of minor males per host likely maintained by negative frequency-dependent selection.
    Journal of Evolutionary Biology 05/2014; · 3.48 Impact Factor
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    ABSTRACT: Trematode communities often consist of different species exploiting the same host population, with two or more trematodes sometimes co-occuring in the same host. A commonly used diagnostic method to detect larval trematode infections in snails has been based on cercarial shedding, though it is often criticized as inaccurate. In the present study we compare infection prevalences determined by cercarial emission with those determined, for the first time, by molecular methods, allowing us to quantify the underestimation of single and double infections based on cercarial emission. We thus developed a duplex PCR for two host-parasite systems, to specifically differentiate between single and double infections. The Ebro samples include two morphologically similar opecoelids, whereas the Otago samples include two morphologically different larval trematodes.
    Parasites & Vectors 05/2014; 7(1):243. · 3.25 Impact Factor
    This article is viewable in ResearchGate's enriched format
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    ABSTRACT: For conspecific parasites sharing the same host, kin recognition can be advantageous when the fitness of one individual depends on what another does; yet, evidence of kin recognition among parasites remains limited. Some trematodes, like Coitocaecum parvum, have plastic life cycles including two alternative life-history strategies. The parasite can wait for its intermediate host to be eaten by a fish definitive host, thus completing the classical three-host life cycle, or mature precociously and produce eggs while still inside its intermediate host as a facultative shortcut. Two different amphipod species are used as intermediate hosts by C. parvum, one small and highly mobile and the other larger, sedentary, and burrow dwelling. Amphipods often harbour two or more C. parvum individuals, all capable of using one or the other developmental strategy, thus creating potential conflicts or cooperation opportunities over transmission routes. This model was used to test the kin recognition hypothesis according to which cooperation between two conspecific individuals relies on the individuals' ability to evaluate their degree of genetic similarity. First, data showed that levels of intrahost genetic similarity between co-infecting C. parvum individuals differed between host species. Second, genetic similarity between parasites sharing the same host was strongly linked to their likelihood of adopting identical developmental strategies. Two nonexclusive hypotheses that could explain this pattern are discussed: kin recognition and cooperation between genetically similar parasites and/or matching genotypes involving parasite genotype-host compatibility filters.
    Journal of Evolutionary Biology 05/2014; · 3.48 Impact Factor
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    ABSTRACT: The global biodiversity of some taxonomic groups is poorly described, but thought to be decreasing rapidly. Surprisingly, this holds for a group of the world’s most iconic large-bodied animals: sharks. Our analysis shows rapid and steep contemporary population declines in sharks coinciding with an increasing rate in species discovery. Larger sharks occupying lower trophic positions with wide geographic distributions (latitudinal ranges) found in shallow waters tend to be discovered first. In light of this increasing trend in species discovery and a cumulative description record far from reaching an asymptote, models cannot predict the global number of sharks. Our results highlight that while our knowledge of shark diversity improves at an accelerating rate, this diversity is under threat and declining rapidly; most shark species are vulnerable to declines, especially smaller-bodied sharks. This surprising finding may relate to mesopredator declines following periods of rapid expansion due to the demise of large sharks (apex predators). Furthermore, shark population declines are structured by phylogeny and, to a lesser extent, geography. Decline in sharks are likely to influence other species as well, e.g. via trophic cascades. The net result may be a greater loss of biodiversity in the oceans and could potentially explain why fewer extinction events are observed than predicted by models. Likewise, it is not inconceivable that species may be lost prior to their discovery.
    Ecography 04/2014; · 4.21 Impact Factor
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    Melanie M Lloyd, Robert Poulin
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    ABSTRACT: Similarly to the division of labour in social insects, castes of morphologically distinct individuals exist within colonies of some species of parasitic trematodes. These colonies occur in the first intermediate host of the trematode's complex life cycle and are composed of clonal individuals. Individuals of the reproductive caste have significantly larger bodies while non-reproductive individuals are small and appear to be specialised for defence against co-infecting trematode colonies. In parallel with colony organisation of social insects, demographic traits such as the proportion of the small, non-reproducing individuals relative to the large, reproducing individuals and colony size are expected to vary and adjust to local conditions. In the case of colonies from geographically and potentially genetically distinct populations, this variation is hypothesised to become fixed by evolutionary divergence, as reported in social insect studies. In this study, the adaptive demography theory was further tested by looking at caste ratio and colony organisation of Philophthalmus sp. (a parasitic trematode with a recently discovered division of labour) colonies from geographically distinct populations. Results indicate that the caste ratio from geographically distinct Philophthalmus sp. colonies differs; the proportion of small, defensive individuals is higher in colonies from the location where the risk of competition is highest. This is suggestive of local adaptation, as caste ratios do not change over time under standardised laboratory conditions. This is the first evidence to support the adaptive demography theory in a species with a division of labour other than social insects.
    Parasitology Research 04/2014; · 2.33 Impact Factor
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    PLoS Pathogens 04/2014; in press. · 8.14 Impact Factor
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    A Studer, R Poulin
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    ABSTRACT: The potential of species for evolutionary adaptation in the context of global climate change has recently come under scrutiny. Estimates of phenotypic variation in biological traits may prove valuable for identifying species, or groups of species, with greater or lower potential for evolutionary adaptation, as this variation, when heritable, represents the basis for natural selection. Assuming that measures of trait variability reflect the evolutionary potential of these traits, we conducted an analysis across trematode species to determine the potential of these parasites as a group to adapt to increasing temperatures. Firstly, we assessed how the mean number of infective stages (cercariae) emerging from infected snail hosts as well as the survival and infectivity of cercariae are related to temperature. Secondly and importantly in the context of evolutionary potential, we assessed how coefficients of variation for these traits are related to temperature, in both cases controlling for other factors such as habitat, acclimatisation, latitude and type of target host. With increasing temperature, an optimum curve was found for mean output and mean infectivity, and a linear decrease for survival of cercariae. For coefficients of variation, temperature was only an important predictor in the case of cercarial output, where results indicated that there is, however, no evidence for limited trait variation at the higher temperature range. No directional trend was found for either variation of survival or infectivity. These results, characterising general patterns among trematodes, suggest that all three traits considered may have potential to change through adaptive evolution.
    International journal for parasitology 03/2014; · 3.39 Impact Factor
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    ABSTRACT: Impacts of environmental changes on zoonotic disease risk are the subject of speculation, but lack a coherent framework for understanding environmental drivers of pathogen transmission from animal hosts to humans. We review how environmental factors affect the distributions of zoonotic agents and their transmission to humans, exploring the roles they play in zoonotic systems. We demonstrate the importance of capturing the distributional ecology of any species involved in pathogen transmission, defining the environmental conditions required, and the projection of that niche onto geography. We further review how environmental changes may alter the dispersal behaviour of populations of any component of zoonotic disease systems. Such changes can modify relative importance of different host species for pathogens, modifying contact rates with humans.
    Trends in Parasitology 03/2014; · 6.22 Impact Factor
  • Robert Poulin
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    ABSTRACT: Although parasites are widely touted as representing a large fraction of the Earth's total biodiversity, several questions remain about the magnitude of parasite diversity, our ability to discover it all and how it varies among host taxa or areas of the world. This review addresses four topical issues about parasite diversity. First, we cannot currently estimate how many parasite species there are on Earth with any accuracy, either in relative or absolute terms. Species discovery rates show no sign of slowing down and cryptic parasite species complicate matters further, rendering extrapolation methods useless. Further, expert opinion, which is also used as a means to estimate parasite diversity, is shown here to be prone to serious biases. Second, it seems likely that we may soon not have enough parasite taxonomists to keep up with the description of new species, as taxonomic expertise appears to be limited to a few individuals in the latter stages of their career. Third, we have made great strides toward explaining variation in parasite species richness among host species, by identifying basic host properties that are universal predictors of parasite richness, whatever the type of hosts or parasites. Fourth, in a geographical context, the main driver of variation in parasite species richness across different areas is simply local host species richness; as a consequence, patterns in the spatial variation of parasite species richness tend to match those already well-documented for free-living species. The real value of obtaining good estimates of global parasite diversity is questionable. Instead, our efforts should be focused on ensuring that we maintain sufficient taxonomic resources to keep up with species discovery, and apply what we know of the variation in parasite species richness among host species or across geographical areas to contribute to areas of concern in the ecology of health and in conservation biology.
    International journal for parasitology 03/2014; · 3.39 Impact Factor
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    ABSTRACT: Parasitic nematodes of the family Mermithidae were found to be infecting the introduced European earwig Forficula auricularia (Dermaptera: Forficulidae) in Dunedin, South Island, New Zealand. Adult females were later collected from various garden plants while depositing eggs. These mermithid specimens were identified morphologically as Mermis nigrescens Dujardin, 1842. A genetic distance of 0.7% between these specimens and a M. nigrescens isolate from Canada (18S rRNA gene), suggests that they have diverged genetically, but there are currently no available comparable sequences for the European M. nigrescens. Two additional nuclear fragments were also amplified, the 28S rRNA and the ribosomal DNA first internal transcribed spacer (ITS1), providing a basis for future studies. Bearing in mind the morphological similarity with other reported M. nigrescens and the lack of sequence data from other parts of the world, we retain the name M. nigrescens, and suggest that the species may be found to represent a complex of cryptic species when more worldwide data are available. Herein, we present a brief description of the post-parasitic worms and adult females, along with an inferred phylogeny using 18S rRNA gene sequences.
    Journal of Helminthology 02/2014; · 1.30 Impact Factor

Publication Stats

10k Citations
1,358.37 Total Impact Points

Institutions

  • 1993–2015
    • University of Otago
      • Department of Zoology
      Taieri, Otago, New Zealand
  • 2013
    • University of Canberra
      Canberra, Australian Capital Territory, Australia
    • Koninklijk Nederlands Instituut voor Onderzoek der Zee - NIOZ
      • Department of Marine Ecology (MEE)
      Burg, North Holland, Netherlands
  • 2004–2013
    • Ben-Gurion University of the Negev
      • • The Swiss Institute for Dryland Environmental and Energy Research(SIDEER)
      • • Department of Life Sciences
      Be'er Sheva`, Southern District, Israel
    • University of Jyväskylä
      • Department of Biological and Environmental Science
      Jyväskylä, Western Finland, Finland
    • Centro de Estudios Parasitologicos y de Vectores CEPAVE
      Eva Perón, Buenos Aires, Argentina
  • 2012
    • University of the Azores
      • Grupo da Biodiversidade dos Açores
      PDL, Azores, Portugal
    • Minnesota State University, Mankato
      • Department of Biological Sciences
      Mankato, MN, United States
  • 2011–2012
    • University of Vermont
      • Department of Biology
      Burlington, VT, United States
    • University of Burgundy
      • Laboratoire Biogéosciences
      Dijon, Bourgogne, France
    • National University of Comahue
      Nequen, Neuquén, Argentina
  • 2010–2011
    • University of New England (Australia)
      • School of Environmental and Rural Science
      Armidale, New South Wales, Australia
    • University of Colorado at Boulder
      • Department of Ecology and Evolutionary Biology (EBIO)
      Boulder, CO, United States
    • Hochschule Koblenz
      Coblenz, Rheinland-Pfalz, Germany
  • 2003–2010
    • Universidad Nacional de Mar del Plata
      • • Departamento de Biología
      • • Facultad de Ciencias Exactas y Naturales
      Mar del Plata, Provincia de Buenos Aires, Argentina
    • Academy of Sciences of the Czech Republic
      Praha, Praha, Czech Republic
  • 2009
    • University of the Pacific (California - USA)
      • Department of Biological Sciences
      Stockton, California, United States
    • Landcare Research
      Christchurch, Canterbury Region, New Zealand
    • Le Moyne College
      Syracuse, New York, United States
  • 2003–2009
    • Center for Research and Advanced Studies of the National Polytechnic Institute
      Ciudad de México, The Federal District, Mexico
  • 2008
    • French National Centre for Scientific Research
      • Institut des Sciences de l’Évolution Montpellier (ISEM)
      Montpellier, Languedoc-Roussillon, France
    • University of Valencia
      • Plant Biology
      Valenza, Valencia, Spain
    • University of Leicester
      • Department of Biology
      Leicester, ENG, United Kingdom
    • University of Chicago
      Chicago, Illinois, United States
  • 2001–2008
    • Institute of Research for Development
      Marsiglia, Provence-Alpes-Côte d'Azur, France
  • 2004–2007
    • Federal Rural University of Rio de Janeiro
      • Departamento de Parasitologia Animal (DPA)
      Rio de Janeiro, Rio de Janeiro, Brazil
  • 2006
    • University of Queensland
      Brisbane, Queensland, Australia
    • Aarhus University
      • Section for Marine Ecology
      Aars, Region North Jutland, Denmark
  • 1997–2006
    • Université de Montpellier 1
      Montpelhièr, Languedoc-Roussillon, France
  • 2005
    • National Scientific and Technical Research Council
      • Departamento de Biología
      Mendoza, Provincia de Mendoza, Argentina
    • Catholic University of the Most Holy Conception
      • Facultad de Ciencias
      Ciudad de Concepcion, Biobío, Chile
    • Universidade Estadual de Maringá
      • Departamento de Biologia
      Maringá, Paraná, Brazil
    • Universidad Austral de Chile
      Ciudad de Valdivía, Los Ríos, Chile
  • 1993–2005
    • Université du Québec à Montréal
      • Department of Biological Sciences
      Montréal, Quebec, Canada
  • 2000–2002
    • Universita degli studi di Ferrara
      • Department of Audiology
      Ferrara, Emilia-Romagna, Italy
  • 1999
    • Lincoln University New Zealand
      Lincoln, Canterbury Region, New Zealand
  • 1998
    • Université de Perpignan
      Perpinyà, Languedoc-Roussillon, France