Penguins are competent hosts of Haemoproteus parasites: the first detection of gametocytes, with molecular characterization of Haemoproteus larae
Abstract Background 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 repo...
| Main Authors: | , , , , , , |
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| Format: | Article |
| Language: | English |
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BMC
2020-06-01
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| Series: | Parasites & Vectors |
| Subjects: | |
| Online Access: | http://link.springer.com/article/10.1186/s13071-020-04176-1 |
| _version_ | 1818262118207586304 |
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| author | Mizue Inumaru Shiori Aratani Misa Shimizu Mineka Yamamoto Yukita Sato Koichi Murata Gediminas Valkiūnas |
| author_facet | Mizue Inumaru Shiori Aratani Misa Shimizu Mineka Yamamoto Yukita Sato Koichi Murata Gediminas Valkiūnas |
| author_sort | Mizue Inumaru |
| collection | DOAJ |
| description | Abstract Background 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 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. Methods Two 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. Results The 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. Conclusions This 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. |
| first_indexed | 2024-12-12T18:58:02Z |
| format | Article |
| id | doaj.art-c4e668cf2d2747dcb286fdd306a60a4d |
| institution | Directory Open Access Journal |
| issn | 1756-3305 |
| language | English |
| last_indexed | 2024-12-12T18:58:02Z |
| publishDate | 2020-06-01 |
| publisher | BMC |
| record_format | Article |
| series | Parasites & Vectors |
| spelling | doaj.art-c4e668cf2d2747dcb286fdd306a60a4d2022-12-22T00:15:12ZengBMCParasites & Vectors1756-33052020-06-0113111510.1186/s13071-020-04176-1Penguins are competent hosts of Haemoproteus parasites: the first detection of gametocytes, with molecular characterization of Haemoproteus laraeMizue Inumaru0Shiori Aratani1Misa Shimizu2Mineka Yamamoto3Yukita Sato4Koichi Murata5Gediminas Valkiūnas6Laboratory of Biomedical Science, Department of Veterinary Medicine, College of Bioresource Sciences, Nihon UniversityLaboratory of Biomedical Science, Department of Veterinary Medicine, College of Bioresource Sciences, Nihon UniversityLaboratory of Biomedical Science, Department of Veterinary Medicine, College of Bioresource Sciences, Nihon UniversityLaboratory of Biomedical Science, Department of Veterinary Medicine, College of Bioresource Sciences, Nihon UniversityLaboratory of Biomedical Science, Department of Veterinary Medicine, College of Bioresource Sciences, Nihon UniversityLaboratory of Wildlife Science, Department of Animal Science and Resources, College of Bioresource Sciences, Nihon UniversityNature Research CentreAbstract Background 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 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. Methods Two 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. Results The 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. Conclusions This 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.http://link.springer.com/article/10.1186/s13071-020-04176-1HaemoproteusCytochrome b lineageMolecular characterizationPenguingametocyteJapan |
| spellingShingle | Mizue Inumaru Shiori Aratani Misa Shimizu Mineka Yamamoto Yukita Sato Koichi Murata Gediminas Valkiūnas Penguins are competent hosts of Haemoproteus parasites: the first detection of gametocytes, with molecular characterization of Haemoproteus larae Parasites & Vectors Haemoproteus Cytochrome b lineage Molecular characterization Penguin gametocyte Japan |
| title | Penguins are competent hosts of Haemoproteus parasites: the first detection of gametocytes, with molecular characterization of Haemoproteus larae |
| title_full | Penguins are competent hosts of Haemoproteus parasites: the first detection of gametocytes, with molecular characterization of Haemoproteus larae |
| title_fullStr | Penguins are competent hosts of Haemoproteus parasites: the first detection of gametocytes, with molecular characterization of Haemoproteus larae |
| title_full_unstemmed | Penguins are competent hosts of Haemoproteus parasites: the first detection of gametocytes, with molecular characterization of Haemoproteus larae |
| title_short | Penguins are competent hosts of Haemoproteus parasites: the first detection of gametocytes, with molecular characterization of Haemoproteus larae |
| title_sort | penguins are competent hosts of haemoproteus parasites the first detection of gametocytes with molecular characterization of haemoproteus larae |
| topic | Haemoproteus Cytochrome b lineage Molecular characterization Penguin gametocyte Japan |
| url | http://link.springer.com/article/10.1186/s13071-020-04176-1 |
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