Robert Poulin

University of Otago , Taieri, Otago Region, New Zealand

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Publications (436)1316 Total impact

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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). · 1.26 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; · 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;
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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;
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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
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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; · 5.12 Impact Factor
  • 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; · 2.85 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; · 5.51 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; · 1.16 Impact Factor
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    ABSTRACT: Abstract The evolution of traits involved in ecological interactions such as predator-prey, host-parasite, and plant-pollinator interactions, are likely to be shaped by the phylogenetic history of both parties. We develop generalized linear mixed-effects models (GLMM) that estimate the effect of both parties' phylogenetic history on trait evolution, both in isolation but also in terms of how the two histories interact. Using data on the incidence and abundance of 206 flea species on 121 mammal species, we illustrate our method and compare it to previously used methods for detecting host-parasite coevolution. At large spatial scales we find that the phylogenetic interaction effect was substantial, indicating that related parasite species were more likely to be found on related host species. At smaller spatial scales, and when sampling effort was not controlled for, phylogenetic effects on the number and types of parasite species harbored by hosts were found to dominate. We go on to show that in situations where these additional phylogenetic effects exist, then previous methods have very high Type I error rates when testing for the phylogenetic interaction. Our GLMM method represents a robust and reliable approach to quantify the phylogenetic effects of traits determined by, or defined by, ecological interactions and has the advantage that it can easily be extended and interpreted in a broader context than existing permutation tests.
    The American Naturalist 02/2014; 183(2):174-87. · 4.55 Impact Factor
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    K. O’Dwyer, T. Kamiya, R. Poulin
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    ABSTRACT: The distribution of organisms at small spatial scales and their use of microhabitats are important determinants of species-level interactions. In many ubiquitous rocky shore invertebrates, use of intertidal microhabitats has previously been studied with relation to thermal and desiccation stress, ontogenetic changes and predation. Here, the effects of parasitism on the microhabitat use and movement of two New Zealand littorinid hosts, Austrolittorina antipodum and A. cincta, were investigated by examining the effect of infection by a philophthalmid trematode parasite. Alterations in microhabitat use and movement of infected versus uninfected individuals were found during both field mark-recapture and laboratory experiments, carried out from August 2012 to March 2013 in Otago Harbour, New Zealand (45.83°S, 170.64°E). Specifically, a trend towards increased use of rock surface habitats and a reduction in the distance moved by infected snails was observed. In addition, decreased downward movement was observed for some infected individuals. This alteration in individual distribution is likely to increase the availability of infected individuals to predators, hence aiding the successful transmission of the trematode parasite. These results highlight the importance of including parasitism as a biotic factor in studies of gastropod movement and spatial distribution.
    Marine Biology 02/2014; 161(2). · 2.47 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 01/2014; · 5.12 Impact Factor
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    Katie O’Dwyer, Aaron Lynch, Robert Poulin
    Journal of Experimental Marine Biology and Ecology 01/2014; 458:1–5. · 2.26 Impact Factor
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    Robert Poulin, Haseeb S Randhawa
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    ABSTRACT: From hundreds of independent transitions from a free-living existence to a parasitic mode of life, separate parasite lineages have converged over evolutionary time to share traits and exploit their hosts in similar ways. Here, we first summarize the evidence that, at a phenotypic level, eukaryotic parasite lineages have all converged toward only six general parasitic strategies: parasitoid, parasitic castrator, directly transmitted parasite, trophically transmitted parasite, vector-transmitted parasite or micropredator. We argue that these strategies represent adaptive peaks, with the similarities among unrelated taxa within any strategy extending to all basic aspects of host exploitation and transmission among hosts and transcending phylogenetic boundaries. Then, we extend our examination of convergent patterns by looking at the evolution of parasite genomes. Despite the limited taxonomic coverage of sequenced parasite genomes currently available, we find some evidence of parallel evolution among unrelated parasite taxa with respect to genome reduction or compaction, and gene losses or gains. Matching such changes in parasite genomes with the broad phenotypic traits that define the convergence of parasites toward only six strategies of host exploitation is not possible at present. Nevertheless, as more parasite genomes become available, we may be able to detect clear trends in the evolution of parasitic genome architectures representing true convergent adaptive peaks, the genomic equivalents of the phenotypic strategies used by all parasites.
    Parasitology 11/2013; In press - First View. · 2.36 Impact Factor
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    ABSTRACT: Phenotypic diversification among colony members often leads to formation of physical castes which are morphologically specialised for particular tasks within the colony. The relative abundance of these castes and their body sizes represent two key aspects of the demography of a colony that may reflect the colony’s needs and conditions, and ultimately influence its survival and reproductive success. In a recently discovered social trematode, Philophthalmus sp., which exhibits a reproductive division of labour, the role of competition and colony composition in shaping reproductive success and behaviour of colony members has been documented. As body size variation within physical castes often influences colony efficiency, we investigated how the growth of reproductive and non-reproductive morphs of Philophthalmus sp. responds to competitive pressure, and to other attributes of colony demography such as colony size and composition. Our survey of a natural population and in vitro experiments demonstrate that the growth of reproductive colony members reflects the interaction between colony composition and the presence of a competitor, while the non-reproductive members simply grow larger in the presence of the intra-host competitor, Maritrema novaezealandensis. Furthermore, the close association between the volume and reproductive capacity of the reproductive members corroborates an adaptive value of colony member size in determining the fitness of the trematode colony as a whole. The present study is the first to demonstrate a fitness consequence, and identify the determinants, of the growth of colony members in social trematodes.
    Evolutionary Ecology 11/2013; 27:1235-1247. · 2.41 Impact Factor

Publication Stats

8k Citations
1,316.00 Total Impact Points

Institutions

  • 1993–2014
    • University of Otago
      • Department of Zoology
      Taieri, Otago Region, 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 Hospital Essen
      • Institut für Medizinische Informatik, Biometrie und Epidemiologie
      Duisburg, North Rhine-Westphalia, Germany
    • Centro de Estudios Parasitologicos y de Vectores CEPAVE
      Eva Perón, Buenos Aires, Argentina
    • University of Jyväskylä
      • Department of Biological and Environmental Science
      Jyväskylä, Western Finland, Finland
  • 2012
    • Minnesota State University, Mankato
      • Department of Biological Sciences
      Mankato, MN, United States
    • University of the Azores
      PDL, Azores, Portugal
  • 2011
    • National University of Comahue
      Nequen, Neuquén, Argentina
    • University of Burgundy
      • Laboratoire Biogéosciences
      Dijon, Bourgogne, France
  • 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
    • University of Alberta
      • Department of Biological Sciences
      Edmonton, Alberta, Canada
  • 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
    • Université Montpellier 2 Sciences et Techniques
      • Institut des Sciences de l’Évolution Montpellier (ISEM)
      Montpellier, Languedoc-Roussillon, France
    • University of California, Santa Barbara
      Santa Barbara, California, United States
    • University of Valencia
      • Plant Biology
      Valenza, Valencia, Spain
    • University of Leicester
      • Department of Biology
      Leicester, ENG, United Kingdom
  • 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
    • Universidade Estadual de Maringá
      • Departamento de Biologia
      Maringá, Paraná, Brazil
    • Austral University of Chile
      Ciudad de Valdivía, Los Ríos, Chile
  • 1993–2005
    • Université du Québec à Montréal
      • Department of Biological Sciences
      Montréal, Quebec, Canada
  • 2002
    • Oregon State University
      • Department of Entomology
      Corvallis, OR, United States
  • 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