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Epidemiology, hematology, and unusual morphological characteristics of Plasmodium during an avian malaria outbreak in penguins in Brazil

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Abstract

Avian malaria is a mosquito-borne disease caused by Plasmodium spp. protozoa, and penguins are considered particularly susceptible to this disease, developing rapid outbreaks with potentially high mortality. We report on an outbreak of avian malaria in Magellanic penguins (Spheniscus magellanicus) at a rehabilitation center in Espírito Santo, southeast Brazil. In August and September 2015, a total of 89 Magellanic penguins (87 juveniles and 2 adults) received care at Institute of Research and Rehabilitation of Marine Animals. Over a period of 2 weeks, Plasmodium infections were identified in eight individuals (9.0%), four of which died (mortality = 4.5%, lethality = 50%). Blood smears and sequencing of the mitochondrial cytochrome b gene revealed the presence of Plasmodium lutzi SPMAG06, Plasmodium elongatum GRW06, Plasmodium sp. PHPAT01, Plasmodium sp. SPMAG10, and Plasmodium cathemerium (sequencing not successful). Two unusual morphological features were observed in individuals infected with lineage SPMAG06: (a) lack of clumping of pigment granules and (b) presence of circulating exoerythrocytic meronts. Hematological results (packed cell volume, plasma total solids, complete blood cell counts) of positive individuals showed differences from those of negative individuals depending on the lineages, but there was no overarching pattern consistently observed for all Plasmodium spp. The epidemiology of the outbreak and the phylogeography of the parasite lineages detected in this study support the notion that malarial infections in penguins undergoing rehabilitation in Brazil are the result of the spillover inoculation by plasmodia that circulate in the local avifauna, especially Passeriformes.

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Acknowledgments

We thank Instituto Estadual do Meio Ambiente e Recursos Hídricos (IEMA) for the valuable partnership that was essential to this study, and to the contributions by Instituto Brasileiro do Meio Ambiente e dos Recursos Naturais Renováveis (IBAMA) and Instituto de Mamíferos Aquáticos (IMA). We are grateful for the indirect contributions by Jorge Oyakawa, Trudi Webster, Staffan Bensch and Gediminas Valkiūnas. We also would like to express our appreciation for the efforts by Staffan Bensch and colleagues in maintaining the MalAvi database. This study was supported by Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP), Minas Gerais Research Foundation (FAPEMIG), Brazilian Federal Agency for the Support and Evaluation of Graduate Education (CAPES), National Counsel of Technological and Scientific Development (CNPq), and the Program for Technological Development in Tools for Health-PDTIS-FIOCRUZ.

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Authors and Affiliations

  1. Laboratory of Wildlife Comparative Pathology (LAPCOM), School of Veterinary Medicine, University of São Paulo, São Paulo, Brazil

    Ralph Eric Thijl Vanstreels & José Luiz Catão-Dias

  2. Institute of Research and Rehabilitation of Marine Animals (IPRAM), Cariacica, Brazil

    Ralph Eric Thijl Vanstreels, Renata Hurtado, Leandro Egert, Luis Felipe S. P. Mayorga & Renata C. C. Bhering

  3. Department of Parasitology, Institute of Biological Sciences, Federal University of Minas Gerais (UFMG), Belo Horizonte, Brazil

    Daniela de Angeli Dutra, Francisco C. Ferreira-Junior & Érika M. Braga

  4. Center for Conservation Genomics, Smithsonian Conservation Biology Institute, Washington, USA

    Francisco C. Ferreira-Junior

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  1. Ralph Eric Thijl Vanstreels
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  2. Daniela de Angeli Dutra
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  3. Francisco C. Ferreira-Junior
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  9. José Luiz Catão-Dias
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Correspondence to Ralph Eric Thijl Vanstreels.

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All procedures in this study were approved by the Ethics Committee on Animal Use of the School of Veterinary Medicine and Animal Science of the University of São Paulo (CEUA 601415) and were authorized by the Brazilian authorities (SISBIO 20825-6).

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Vanstreels, R.E.T., Dutra, D.d., Ferreira-Junior, F.C. et al. Epidemiology, hematology, and unusual morphological characteristics of Plasmodium during an avian malaria outbreak in penguins in Brazil. Parasitol Res 118, 3497–3508 (2019). https://doi.org/10.1007/s00436-019-06459-8

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