Abstract
BackgroundThe majority of penguins (Sphenisciformes) have evolved in areas with weak or absent transmission of haemosporidian parasites and are usually naïve to avian haemosporidian infections. Plasmodium parasites are transmitted by mosquitoes, and lethal avian malaria has been often reported in captive penguins in many countries. The related haemosporidian parasites belonging to Haemoproteus and Leucocytozoon have also been detected in penguins but less often than Plasmodium infections. The majority of Haemoproteus infection reports in penguins are based solely on PCR-based diagnostics. It remains unclear if haemoproteids can complete their life-cycle and produce infective stages (gametocytes) in penguins or whether these infections are abortive in penguins, and thus dead ends for transmission. In other words, it remains unknown if penguins are competent hosts for Haemoproteus parasites, which cause disease in non-adapted birds.MethodsTwo captive African penguins (Spheniscus demersus) and two Magellanic penguins (S. magellanicus) were found to be positive for Haemoproteus infection in two open-air aquariums in Japan, and the parasites were investigated using both PCR-based testing and microscopical examination of blood films. Samples from a black-tailed gull (Larus crassirostris) and previously tested gulls were used for comparison.ResultsThe lineage hSPMAG12 was detected, and gametocytes of Haemoproteus sp. were seen in the examined penguins and gull. Observed gametocytes were indistinguishable from those of Haemoproteus larae, which naturally parasitize birds of the genus Larus (Laridae). The detected sequence information and Bayesian phylogenetic analysis supported this conclusion. Additionally, morphologically similar gametocytes and closely related DNA sequences were also found in other gull species in Japan. Phylogenetic analysis based on partial cytb sequences placed the lineage hSPMAG12 of H. larae within the clade of avian haemoproteids which belong to the subgenus Parahaemoproteus, indicating that Culicoides biting midges likely transmit the parasites between penguins and gulls.ConclusionsThis study shows that some species of Haemoproteus parasites complete their development and produce gametocytes in penguins, which may be source of infection for biting midges transmitting haemoproteosis. To prevent haemosporidiosis in zoos, we call for control not only of mosquitoes, but also biting midges.
Highlights
The majority of penguins (Sphenisciformes) have evolved in areas with weak or absent transmission of haemosporidian parasites and are usually naïve to avian haemosporidian infections
All detected sequences were identified as Haemoproteus sp. hSPMAG12, which is the lineage previously found in a captive Magellanic penguin in Japan
Key: dark grey area, species of subgenus Haemoproteus; light grey area, species of subgenus Parahaemoproteus; diamond, Haemoproteus spp. lineages derived from penguins in previous studies; circle, Haemoproteus spp. lineages derived from Larus sp. gulls in previous studies; red letters, lineage derived in this study (GenBank: AB604310)
Summary
The majority of penguins (Sphenisciformes) have evolved in areas with weak or absent transmission of haemosporidian parasites and are usually naïve to avian haemosporidian infections. Plasmodium parasites are transmitted by mosquitoes, and lethal avian malaria has been often reported in captive penguins in many countries. The majority of Haemoproteus infection reports in penguins are based solely on PCR-based diagnostics It remains unclear if haemoproteids can complete their life-cycle and produce infective stages (gametocytes) in penguins or whether these infections are abortive in penguins, and dead ends for transmission. In other words, it remains unknown if penguins are competent hosts for Haemoproteus parasites, which cause disease in non-adapted birds. The first case of avian haemosporidian infection was the Plasmodium parasite reported in a captive king penguin (Aptenodytes patagonicus) at London Zoo in 1926 [4]. Blood of S. demersus has been detected in Culex pipiens pallens, which is one of the major vectors of avian malaria in Japan [12]
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