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      Effects of habitat suitability for vectors, environmental factors and host characteristics on the spatial distribution of the diversity and prevalence of haemosporidians in waterbirds from three Brazilian wetlands

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          Abstract

          Background

          Wetlands are ecosystems in which vectors of avian haemosporidians live and reproduce and where waterbirds join to breed in colonies. Brazil has wetlands at different latitudes, which enables testing the influence of the ecological factors on the prevalence and diversity of haemosporidians. We identified avian haemosporidians in waterbird species in three wetlands and investigated the effects of vector habitat suitability, landscape and host characteristics on the diversity and prevalence of these parasites.

          Methods

          We created a map with the probability of occurrence of avian haemosporidian vectors using maximum-entropy modelling based on references addressing species known to be vectors of haemosporidians in birds in Brazil. We determined the prevalence and diversity index of haemosporidians in the great egret ( Ardea alba) ( n = 129) and roseate spoonbill ( Platalea ajaja) ( n = 180) and compared the findings to data for the wood stork ( Mycteria americana) ( n = 199).

          Results

          We report the first record of Plasmodium in the family Threskiornithidae: four lineages in the roseate spoonbill, which also presented one lineage of Haemoproteus. In the family Ardeidae, we found three Plasmodium lineages in the great egret. The similar habitat suitability for vectors found in three wetlands explains the pattern of haemosporidian diversity determined for great egret and wood stork populations. Comparisons of haemosporidian diversity within each waterbird species and between regions showed a higher level in the central-western roseate spoonbill population than in the northern population ( P = 0.021). Removing the host effect, we discussed the results obtained in terms of characteristics of the Pantanal region. Comparisons of Plasmodium spp. prevalence among waterbird species within the same wetland showed higher level in roseate spoonbill (74%) than those found in the great egret (21%) and wood stork (11%). Excluding the environmental effect, we interpreted result focusing host characteristics that favour infection: time required for nestlings to be covered by feathers and migratory behaviour.

          Conclusions

          The map of habitat suitability showed that wetlands located in a 30° latitudinal range offer similar conditions for avian vectors species and diversity of haemosporidians. The lineages described in waterbirds were previously identified in birds of prey as Plasmodium paranucleophilum.

          Electronic supplementary material

          The online version of this article (10.1186/s13071-018-2847-z) contains supplementary material, which is available to authorized users.

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          Most cited references57

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          Insights into the area under the receiver operating characteristic curve (AUC) as a discrimination measure in species distribution modelling

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            Odor-mediated behavior of Afrotropical malaria mosquitoes.

            The African mosquito species Anopheles gambiae sensu lato s.l. and Anopheles funestus rank among the world's most efficient vectors of human malaria. Their unique bionomics, particularly their anthropophilic, endophagic and endophilic characters, guarantee a strong mosquito-host interaction, favorable to malaria transmission. Olfactory cues govern the various behaviors of female mosquitoes and here we review the role of semiochemicals in the life history of African malaria vectors. Recent evidence points towards the existence of human-specific kairomones affecting host-seeking A. gambiae s.l., and efforts are under way to identify the volatiles mediating this behavior. Based on examples from other Culicidae spp., it is argued that there is good reason to assume that mating, sugar feeding, and oviposition behavior in Afrotropical malaria vectors may also be mediated by semiochemicals. It is foreseen that increased knowledge of odor-mediated behaviors will be applied in the development of novel sampling techniques and possibly alternative methods of intervention to control malaria.
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              A three-genome phylogeny of malaria parasites (Plasmodium and closely related genera): evolution of life-history traits and host switches.

              Phylogenetic analysis of genomic data allows insights into the evolutionary history of pathogens, especially the events leading to host switching and diversification, as well as alterations of the life cycle (life-history traits). Hundreds, perhaps thousands, of malaria parasite species exploit squamate reptiles, birds, and mammals as vertebrate hosts as well as many genera of dipteran vectors, but the evolutionary and ecological events that led to this diversification and success remain unresolved. For a century, systematic parasitologists classified malaria parasites into genera based on morphology, life cycle, and vertebrate and insect host taxa. Molecular systematic studies based on single genes challenged the phylogenetic significance of these characters, but several significant nodes were not well supported. We recovered the first well resolved large phylogeny of Plasmodium and related haemosporidian parasites using sequence data for four genes from the parasites' three genomes by combining all data, correcting for variable rates of substitution by gene and site, and using both Bayesian and maximum parsimony analyses. Major clades are associated with vector shifts into different dipteran families, with other characters used in traditional parasitological studies, such as morphology and life-history traits, having variable phylogenetic significance. The common parasites of birds now placed into the genus Haemoproteus are found in two divergent clades, and the genus Plasmodium is paraphyletic with respect to Hepatocystis, a group of species with very different life history and morphology. The Plasmodium of mammal hosts form a well supported clade (including Plasmodium falciparum, the most important human malaria parasite), and this clade is associated with specialization to Anopheles mosquito vectors. The Plasmodium of birds and squamate reptiles all fall within a single clade, with evidence for repeated switching between birds and squamate hosts.
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                Author and article information

                Contributors
                schahad@gmail.com
                angela.fushita@ufabc.edu.br
                gustavo.lacorte@ifmg.edu.br
                pan_assis@hotmail.com
                dsdl@ufscar.br
                Journal
                Parasit Vectors
                Parasit Vectors
                Parasites & Vectors
                BioMed Central (London )
                1756-3305
                2 May 2018
                2 May 2018
                2018
                : 11
                : 276
                Affiliations
                [1 ]ISNI 0000 0001 2163 588X, GRID grid.411247.5, Departamento de Genética e Evolução, , Universidade Federal de São Carlos, ; Rodovia Washington Luís, km 235 SP-310, São Carlos, SP 13565-905 Brazil
                [2 ]ISNI 0000 0004 0643 8839, GRID grid.412368.a, Centro de Engenharia, , Modelagem e Ciências Aplicadas Universidade Federal do ABC, ; Avenida dos Estados 5001, Santo André, São Paulo, 09210-580 Brazil
                [3 ]ISNI 0000 0004 0370 1822, GRID grid.462191.9, Laboratório Biologia Molecular, , Instituto Federal de Minas Gerais, ; Bambuí, Fazenda Varginha, Rodovia Bambuí - Medeiros, km 5, Bambuí, Minas Gerais 38900-000 Brazil
                Article
                2847
                10.1186/s13071-018-2847-z
                5930942
                29716645
                327b2b24-8e30-456f-bea1-d19c62eff38e
                © The Author(s). 2018

                Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

                History
                : 10 January 2018
                : 13 April 2018
                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/501100001807, Fundação de Amparo à Pesquisa do Estado de São Paulo;
                Award ID: 2004/15205-8, 2010/ 50406-5, 2016/01673-7
                Categories
                Research
                Custom metadata
                © The Author(s) 2018

                Parasitology
                blood parasites,plasmodium,haemoproteus,prevalence,herons,spoonbills,parasitism
                Parasitology
                blood parasites, plasmodium, haemoproteus, prevalence, herons, spoonbills, parasitism

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