The malaria parasite Plasmodium relictum in the endemic avifauna of eastern Cuba

Abstract

Island populations are vulnerable to introduced pathogens, as evidenced by extinction or population decline of several endemic Hawaiian birds caused by the malaria parasite, Plasmodium relictum (order Haemosporida). We analyzed blood samples from 363 birds caught near Guantánamo Bay, Cuba, for the presence of haemosporidian infections. We characterized parasite lineages by determining nucleotide variation of the parasite's mitochondrial cyt b gene. Fifty-nine individuals were infected, and we identified 7 lineages of haemosporidian parasites. Fifty individuals were infected by 6 Haemoproteus sp. lineages, including a newly characterized lineage of Haem. (Parahaemoproteus) sp. CUH01. Nine individuals carried the P. relictum lineage GRW4, including 5 endemic Cuban Grassquits (Tiaris canorus) and 1 migratory Cape May Warbler (Setophaga tigrina). A sequence of the merozoite surface protein gene from one Cuban Grassquit infected with GRW4 matched that of the Hawaiian haplotype Pr9. Our results indicate that resident and migratory Cuban birds are infected with a malaria lineage that has severely affected populations of several endemic Hawaiian birds. We suggest GRW4 may be associated with the lack of several bird species on Cuba that are ubiquitous elsewhere in the West Indies. From the standpoint of avian conservation in the Caribbean Basin, it will be important to determine the distribution of haemosporidian parasites, especially P. relictum GRW4, in Cuba as well as the pathogenicity of this lineage in species that occur and are absent from Cuba.

Characterization of Plasmodium relictum, a cosmopolitan agent of avian malaria

“…Controlled experimental studies with P. relictum are relatively easy to design due to availability of laboratory-friendly experimental vertebrate hosts (canaries and some species of other common birds), laboratory-colonized susceptible mosquitoes (species of the Culex pipiens complex) and worldwide high prevalence in many wild bird species (donors of natural infections). This makes P. relictum a convenient and even unique model organism to approach numerous questions about mechanisms of host-parasite interactions, including the immunological aspects during malaria infections [ 56 – 58 ], the ecology and evolution of host-parasite associations [ 25 , 59 – 63 ], the host adaptations to tolerate malaria infections [ 10 , 31 , 47 , 64 , 65 ], patterns of mosquito transmission [ 32 , 46 , 53 , 66 – 68 ] and many other questions.…”

“…Observations of infected, naive birds in zoos and rehabilitation centres provided evidence of the severity of disease caused by these and related parasite lineages in wild birds [ 71 – 74 ]. These studies are the basis of understanding the predictions and conclusions of field observations about negative influence of P. relictum on population decline or even extinction, particularly on oceanic islands [ 63 , 75 – 78 ]. However, to evaluate the true virulence of a malaria parasite lineage in certain avian host species, experimental and field observations are needed, ideally in each targeting host-parasite system separately.…”

A highly invasive malaria parasite has expanded its range to non-migratory birds in North America

“…For example, the Pl. relictum strain GRW4 was introduced to the Hawaiian islands in the late nineteenth century, and subsequent avian malaria infections have been described as a driver of extinction for many endemic Hawaiian bird species [10,12,13]. The geographical and host specificity of avian malaria parasites is complex [14,15], but some highly invasive strains of Pl.…”

The global biogeography of avian haemosporidian parasites is characterized by local diversification and intercontinental dispersal

“…Indeed, differences in distributions among haemosporidian genera have been linked to the probability that the parasites infect migratory host species (Hellgren et al ., 2007). However, some avian haemosporidian parasites, such as the lineage GRW04 (morphological species Plasmodium relictum ) – the parasite that contributed to the decline of Hawaii's avifauna (Beadell et al ., 2006) – have nearly global distributions that cannot be attributed to natural avian migration patterns and might be related to human introductions of birds and vectors to novel areas (Soares et al ., 2017). Still other haemosporidians may have dispersed large distances without the help of humans and outside of typical bird migration routes.…”