Avian haemosporidians in the cattle egret (Bubulcus ibis) from central-western and southern Africa: High diversity and prevalence

PLoS One. 2019 Feb 22;14(2):e0212425. doi: 10.1371/journal.pone.0212425. eCollection 2019.

Abstract

We described the geographic distribution of 82 haemosporidian lineages (Plasmodium, Haemoproteus, and Leucocytozoon) in the cattle egret sampled in five countries in central-western and southern Africa. Seventy-three lineages have not previously been reported. We determined the prevalence of three haemosporidians in the samples. We investigated the influence of the internal environment of the host and environmental variables on the Plasmodium diversity and whether environmental variables may explain spatial variations in the prevalence of Plasmodium. We screened DNA from 509 blood samples from nestlings in 15 African colonies for infection by sequencing the cytochrome b gene of parasites. The molecular phylogenetic analysis was performed using Bayesian methods and including sequences from the MalAvi and GeneBank databases. We found 62 new Plasmodium lineages in a clade with MYCAME02, which is a lineage described in waterbirds and recently identified in birds of prey as Plasmodium paranucleophilum. Two Haemoproteus lineages identified in cattle egret formed a distinct group with Haemoproteus catharti and MYCAMH1 (Haemoproteus spp.). Seven Leucocytozoon lineages found in the cattle egret clustered with Leucocytozoon californicus. We found different Plasmodium diversities among the colonies sampled, demonstrating that the internal environment of the host is not the primary determinant of diversity. A linear mixed-effects multivariate model showed that precipitation was positively associated with Plasmodium diversity when controlling for the effects of temperature, colony composition (mixed and non-mixed species) and country. Moreover, a generalized mixed model showed that temperature was positively associated with the prevalence of Plasmodium when controlling for precipitation, elevation and country. We conclude that the cattle egret is a good model for future haemosporidian studies, as we found a significant number of new lineages in this host, which occupies regions with different climate characteristics where environmental variables exert an influence on the diversity and prevalence of Plasmodium.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Africa / epidemiology
  • Animals
  • Bird Diseases / epidemiology*
  • Bird Diseases / parasitology
  • Birds / parasitology*
  • DNA, Protozoan / genetics
  • DNA, Protozoan / isolation & purification
  • Genetic Variation
  • Haemosporida / genetics*
  • Haemosporida / isolation & purification*
  • Haemosporida / pathogenicity
  • Host-Parasite Interactions
  • Malaria / epidemiology
  • Malaria / parasitology
  • Malaria / veterinary
  • Phylogeny
  • Phylogeography
  • Plasmodium / genetics
  • Plasmodium / isolation & purification
  • Plasmodium / pathogenicity
  • Prevalence
  • Protozoan Infections, Animal / epidemiology*
  • Protozoan Infections, Animal / parasitology

Substances

  • DNA, Protozoan

Grants and funding

This work was primarily funded by governmental institutions from Brazil. This work was supported by the Brazilian fostering agency Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP [State of São Paulo Research Assistance Foundation]) through Research Grants awarded to SN Del Lama (2010/50406-5, 2016/01673-7) and awarded to R Izbicki (2017/03363-8). AfriWet Consultants provided support in the form of salaries for authors MD, but did not have any additional role in the study design, data collection and analysis, decision to publish, or preparation of the manuscript. The specific roles of these authors are articulated in the ‘author contributions’ section.