Vector incrimination and transmission of avian malaria at an aquarium in Japan: mismatch in parasite composition between mosquitoes and penguins

Abstract Background Captive populations of penguins outside of their natural distributions are often maintained in outdoor facilities, such as zoos and aquariums. Consequently, such penguins in captivity are constantly exposed to mosquito vectors and risk of avian malarial infection during their act...

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Main Authors: Mizue Inumaru, Atsushi Yamada, Misa Shimizu, Ayana Ono, Makiko Horinouchi, Tatsuki Shimamoto, Yoshio Tsuda, Koichi Murata, Yukita Sato
Format: Article
Language:English
Published: BMC 2021-03-01
Series:Malaria Journal
Subjects:
Online Access:https://doi.org/10.1186/s12936-021-03669-3
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spelling doaj-553852ee37d44869a44707a0078cc4082021-03-11T12:48:28ZengBMCMalaria Journal1475-28752021-03-0120111210.1186/s12936-021-03669-3Vector incrimination and transmission of avian malaria at an aquarium in Japan: mismatch in parasite composition between mosquitoes and penguinsMizue Inumaru0Atsushi Yamada1Misa Shimizu2Ayana Ono3Makiko Horinouchi4Tatsuki Shimamoto5Yoshio Tsuda6Koichi Murata7Yukita Sato8Laboratory of Biomedical Science, Department of Veterinary Medicine, College of Bioresource Sciences, Nihon UniversityNiigata City Aquarium Marinepia NihonkaiLaboratory 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 UniversityDepartment of Medical Entomology, National Institute of Infectious DiseasesLaboratory of Wildlife Science, Department of Animal Resource Sciences, College of Bioresource Sciences, Nihon UniversityLaboratory of Biomedical Science, Department of Veterinary Medicine, College of Bioresource Sciences, Nihon UniversityAbstract Background Captive populations of penguins outside of their natural distributions are often maintained in outdoor facilities, such as zoos and aquariums. Consequently, such penguins in captivity are constantly exposed to mosquito vectors and risk of avian malarial infection during their active period from spring to autumn, which can be lethal to these naïve birds. Previous studies have investigated parasite prevalence in mosquitoes or penguins, but simultaneous investigations, which would be crucial to monitor the transmission dynamics and cycle within a facility, have not been done. To identify dominant lineages and trends, multiple-year surveys are recommended. Methods Avian malaria parasites (Plasmodium spp.) and related haemosporidia were tested in penguins and mosquitoes at an aquarium in Japan through multiple years from 2011 to 2018. Prevalence and dynamics were confirmed, and molecular analyses targeting the protozoal cytb gene were used to reveal the transmission cycle. Blood meals of mosquitoes were also identified using molecular methods. Results Parasite detection in penguins tended to fluctuate within an individual. Two Plasmodium lineages were consistently detected in mosquitoes that had fed on penguins and wild birds observed around the aquarium. Plasmodium lineage CXPIP09 was detected from both mosquitoes and penguins, suggesting active transmission at this facility. However, Plasmodium cathemerium PADOM02 was only detected in mosquitoes, which may be due to host, vector or parasite-related factors, or detection methods and their limits. Additionally, Haemoproteus larae SPMAG12 was detected from penguins, suggesting active transmission via biting midges. Conclusions The mismatch in parasite composition between penguins and mosquitoes shows that multiple aspects such as captive birds, wild birds and vector insects should be monitored in order to better understand and control avian malarial infection within ex-situ conservation facilities. Furthermore, morphological analyses would be needed to confirm competency and infection dynamics of avian malaria parasites.https://doi.org/10.1186/s12936-021-03669-3Avian malariaBlood mealJapanMosquitoPenguinPlasmodium
collection DOAJ
language English
format Article
sources DOAJ
author Mizue Inumaru
Atsushi Yamada
Misa Shimizu
Ayana Ono
Makiko Horinouchi
Tatsuki Shimamoto
Yoshio Tsuda
Koichi Murata
Yukita Sato
spellingShingle Mizue Inumaru
Atsushi Yamada
Misa Shimizu
Ayana Ono
Makiko Horinouchi
Tatsuki Shimamoto
Yoshio Tsuda
Koichi Murata
Yukita Sato
Vector incrimination and transmission of avian malaria at an aquarium in Japan: mismatch in parasite composition between mosquitoes and penguins
Malaria Journal
Avian malaria
Blood meal
Japan
Mosquito
Penguin
Plasmodium
author_facet Mizue Inumaru
Atsushi Yamada
Misa Shimizu
Ayana Ono
Makiko Horinouchi
Tatsuki Shimamoto
Yoshio Tsuda
Koichi Murata
Yukita Sato
author_sort Mizue Inumaru
title Vector incrimination and transmission of avian malaria at an aquarium in Japan: mismatch in parasite composition between mosquitoes and penguins
title_short Vector incrimination and transmission of avian malaria at an aquarium in Japan: mismatch in parasite composition between mosquitoes and penguins
title_full Vector incrimination and transmission of avian malaria at an aquarium in Japan: mismatch in parasite composition between mosquitoes and penguins
title_fullStr Vector incrimination and transmission of avian malaria at an aquarium in Japan: mismatch in parasite composition between mosquitoes and penguins
title_full_unstemmed Vector incrimination and transmission of avian malaria at an aquarium in Japan: mismatch in parasite composition between mosquitoes and penguins
title_sort vector incrimination and transmission of avian malaria at an aquarium in japan: mismatch in parasite composition between mosquitoes and penguins
publisher BMC
series Malaria Journal
issn 1475-2875
publishDate 2021-03-01
description Abstract Background Captive populations of penguins outside of their natural distributions are often maintained in outdoor facilities, such as zoos and aquariums. Consequently, such penguins in captivity are constantly exposed to mosquito vectors and risk of avian malarial infection during their active period from spring to autumn, which can be lethal to these naïve birds. Previous studies have investigated parasite prevalence in mosquitoes or penguins, but simultaneous investigations, which would be crucial to monitor the transmission dynamics and cycle within a facility, have not been done. To identify dominant lineages and trends, multiple-year surveys are recommended. Methods Avian malaria parasites (Plasmodium spp.) and related haemosporidia were tested in penguins and mosquitoes at an aquarium in Japan through multiple years from 2011 to 2018. Prevalence and dynamics were confirmed, and molecular analyses targeting the protozoal cytb gene were used to reveal the transmission cycle. Blood meals of mosquitoes were also identified using molecular methods. Results Parasite detection in penguins tended to fluctuate within an individual. Two Plasmodium lineages were consistently detected in mosquitoes that had fed on penguins and wild birds observed around the aquarium. Plasmodium lineage CXPIP09 was detected from both mosquitoes and penguins, suggesting active transmission at this facility. However, Plasmodium cathemerium PADOM02 was only detected in mosquitoes, which may be due to host, vector or parasite-related factors, or detection methods and their limits. Additionally, Haemoproteus larae SPMAG12 was detected from penguins, suggesting active transmission via biting midges. Conclusions The mismatch in parasite composition between penguins and mosquitoes shows that multiple aspects such as captive birds, wild birds and vector insects should be monitored in order to better understand and control avian malarial infection within ex-situ conservation facilities. Furthermore, morphological analyses would be needed to confirm competency and infection dynamics of avian malaria parasites.
topic Avian malaria
Blood meal
Japan
Mosquito
Penguin
Plasmodium
url https://doi.org/10.1186/s12936-021-03669-3
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