Neglected parasite reservoirs in wetlands: Prevalence and diversity of avian haemosporidians in waterbird communities in Northeast China

Abstract

The diversity of waterbirds is threatened, and haemosporidian parasite infection is considered one of the most important causative factors. However, to date, only a few studies focusing on specific parasite species have been carried out, which cannot reflect the general patterns at the community level. To test whether the reported haemosporidian diversity in waterbirds is underestimated, we estimated the prevalence and lineage diversity of avian haemosporidian parasites in 353 waterbirds from 26 species in the Tumuji National Nature Reserve, Northeast China, as well as the host-parasite associations. According to the molecular analysis of cytochrome b (cyt b) barcode sequences, 28.3% of the birds were infected by 49 distinct parasite lineages, including 11 Plasmodium, 12 Haemoproteus, and 26 Leucocytozoon lineages, of which 39 were novel. The highest prevalence was contributed by Leucocytozoon (13.31%), followed by Plasmodium (13.03%) and Haemoproteus (4.25%), which suggested that waterbirds were infected to a lesser extent by Haemoproteus than by the other two genera. Among the most sampled birds, species belonging to Anatidae appeared to be susceptible to Leucocytozoon but resistant to Plasmodium, while Rallidae presented the opposite pattern. On the phylogenetic tree, most of the Leucocytozoon lineages detected in Anatidae clustered together and formed two well-supported clades, while lineages restricted to Gruidae were distantly related to other parasites in all three genera. SW5 was the most abundant lineage and therefore might be a major threat to waterbirds; among the hosts, the common coot harboured the highest diversity of parasite lineages and thus could act as a reservoir for potential transmission. This is the first study of avian haemosporidian infections in a wild waterbird community in Asia. Our findings have doubled the number of lineages recorded in waterbirds, broadened our understanding of host-parasite associations, and addressed the importance of studying haemosporidian infections in wild waterbird conservation.

Keywords: Haemosporidian parasites; Host specificity; Tumuji National Nature Reserve; Waterbirds; Wetland.

Graphical abstract

Fig. 1

Heatmap of the apparent prevalence of waterbird species in the Tumuji National Nature Reserve. Presenting infected waterbird species (left, sorted by order) with prevalence (indicated by colour gradient, scale from 0 to 1). The sample size is shown in parentheses.

Fig. 2

Diversity (a) and frequency (b) of haemosporidian parasite lineages obtained from waterbirds in Tumuji, China. Sankey diagrams of the correlation between waterbirds (left, sorted by order) and identified haemosporidian lineages (right). The width of the lines indicates proportion to the infection recordings in waterbirds, and the colour of the lines indicates the range of the lineage size. The numbers represent infection cases. (For interpretation of the references to colour in this figure legend, the reader is referred to the Web version of this article.)

Fig. 3

Bayesian phylogenetic reconstruction of 479 bp haemosporidian cyt b lineages from waterbirds in Tumuji, China, with Hepatocystis sp. as an outgroup, and several morpho-species were included for a higher resolution of phylogenetic patterns. Posterior probabilities higher than 0.90 are shown by the node. Lineages that were previously recorded and detected in this study are marked in bold. Major monophyletic clades with high support are labelled behind the line (Leucocytozoon: L1-L5; Haemoproteus: H1–H3).