Prevalence and genetic diversity of avian haemosporidian parasites in islands within a mega hydroelectric dam in the Brazilian Amazon.


Journal

Parasitology research
ISSN: 1432-1955
Titre abrégé: Parasitol Res
Pays: Germany
ID NLM: 8703571

Informations de publication

Date de publication:
Sep 2023
Historique:
received: 20 01 2023
accepted: 19 06 2023
medline: 17 8 2023
pubmed: 1 7 2023
entrez: 30 6 2023
Statut: ppublish

Résumé

The Brazilian Amazon supports an extremely diverse avifauna and serves as the diversification center for avian malaria parasites in South America. Construction of hydroelectric dams can drive biodiversity loss by creating islands incapable of sustaining the bird communities found in intact forest sites. Besides anthropogenic actions, the presence of parasites can also influence the dynamics and structure of bird communities. Avian malaria (Plasmodium) and related haemosporidian parasites (Haemoproteus and Leucocytozoon) are a globally distributed group of protozoan parasites recovered from all major bird groups. However, no study to date has analyzed the presence of avian haemosporidian parasites in fragmented areas such as land bridge islands formed during artificial flooding following the construction of hydroelectric dams. The aim of this study is to assess the prevalence and molecular diversity of haemosporidians in bird communities inhabiting artificial islands in the area of the Balbina Hydroelectric Dam. The reservoir area covers 443,700 ha with 3546 islands on the left bank of the Uatumã River known to contain more than 400 bird species. We surveyed haemosporidian infections in blood samples collected from 445 understory birds, belonging to 53 species, 24 families, and 8 orders. Passeriformes represented 95.5% of all analyzed samples. We found a low overall Plasmodium prevalence (2.9%), with 13 positive samples (two Plasmodium elongatum and 11 Plasmodium sp.) belonging to eight lineages. Six of these lineages were previously recorded in the Amazon, whereas two of them are new. Hypocnemis cantator, the Guianan Warbling Antbird, represented 38.5% of all infected individuals, even though it represents only 5.6% of the sampled individuals. Since comparison with Plasmodium prevalence data prior to construction of Balbina is not possible, other studies in artificially flooded areas are imperative to test if anthropogenic flooding may disrupt vector-parasite relationships leading to low Plasmodium prevalence.

Identifiants

pubmed: 37391644
doi: 10.1007/s00436-023-07906-3
pii: 10.1007/s00436-023-07906-3
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

2065-2077

Informations de copyright

© 2023. The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature.

Références

Anjos CC, Chagas CRF, Fecchio A et al (2021) Avian malaria and related parasites from resident and migratory birds in the Brazilian Atlantic Forest, with description of a new Haemoproteus species. Pathogens 10:103. https://doi.org/10.3390/pathogens10020103
doi: 10.3390/pathogens10020103 pubmed: 33494428 pmcid: 7912314
Bandelt HJ, Forster P, Rohl A (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16:37–48. https://doi.org/10.1093/oxfordjournals.molbev.a026036
doi: 10.1093/oxfordjournals.molbev.a026036 pubmed: 10331250
Barbieri AF, Sawyeriana O, Soares-Filho BS (2005) Population and land use effects on malaria prevalence in the southern Brazilian Amazon. Hum Ecol 33:847–874. https://doi.org/10.1007/s10745-005-8213-8
doi: 10.1007/s10745-005-8213-8
Becker PH (2003) Chapter 19: biomonitoring with birds. In: Trace Metals and other Contaminants in the Environment. Elsevier, pp 677–736
Benchimol M, Peres CA (2015) Widespread forest vertebrate extinctions induced by a mega hydroelectric dam in lowland Amazonia. PLoS ONE 10:e0129818. https://doi.org/10.1371/journal.pone.0129818
doi: 10.1371/journal.pone.0129818 pubmed: 26132139 pmcid: 4488572
Bensch S, Hellgren O, Pérez-Tris J (2009) MalAvi: a public database of malaria parasites and related haemosporidians in avian hosts based on mitochondrial cytochrome b lineages. Mol Ecol Resour 9:1353–1358. https://doi.org/10.1111/j.1755-0998.2009.02692.x
doi: 10.1111/j.1755-0998.2009.02692.x pubmed: 21564906
Bicudo T, Anciães M, Arregui L, Gil D (2020) Effects of forest fragmentation on feather corticosterone levels in an Amazonian avian community. Ardeola 67:229. https://doi.org/10.13157/arla.67.2.2020.ra1
doi: 10.13157/arla.67.2.2020.ra1
Blas J (2015) Stress in birds. In: Sturkie’s Avian Physiology. Elsevier, In, pp 769–810
doi: 10.1016/B978-0-12-407160-5.00033-6
Buckley LB, Jetz W (2007) Insularity and the determinants of lizard population density. Ecol Letters 10:481–489. https://doi.org/10.1111/j.1461-0248.2007.01042.x
doi: 10.1111/j.1461-0248.2007.01042.x
Cabral MMM, De Mattos GE, Rosas FCW (2008) Mammals, birds and reptiles in Balbina reservoir, state of Amazonas, Brazil. Check List 4:152–157. https://doi.org/10.15560/4.2.152
doi: 10.15560/4.2.152
Chagas CRF, Valkiūnas G, de Oliveira GL et al (2017) Diversity and distribution of avian malaria and related haemosporidian parasites in captive birds from a Brazilian megalopolis. Malar J 16:83. https://doi.org/10.1186/s12936-017-1729-8
doi: 10.1186/s12936-017-1729-8 pubmed: 28212654 pmcid: 5316177
Chagas CRF, Valkiūnas G, Nery CVC et al (2013) Plasmodium (Novyella) nucleophilum from an Egyptian Goose in São Paulo Zoo, Brazil: microscopic confirmation and molecular characterization. Int J Parasitol Parasites Wildl 2:286–291. https://doi.org/10.1016/j.ijppaw.2013.09.008
doi: 10.1016/j.ijppaw.2013.09.008 pubmed: 24533348 pmcid: 3862519
Clark NJ, Clegg SM, Klaassen M (2016) Migration strategy and pathogen risk: non-breeding distribution drives malaria prevalence in migratory waders. Oikos 125:1358–1368. https://doi.org/10.1111/oik.03220
doi: 10.1111/oik.03220
Clark NJ, Clegg SM, Lima MR (2014) A review of global diversity in avian haemosporidians (Plasmodium and Haemoproteus: Haemosporida): new insights from molecular data. Int J Parasitol 44:329–338. https://doi.org/10.1016/j.ijpara.2014.01.004
doi: 10.1016/j.ijpara.2014.01.004 pubmed: 24556563
De La Torre GM, Freitas FF, Fratoni RDO et al (2020) Hemoparasites and their relation to body condition and plumage coloration of the White-necked thrush (Turdus albicollis). Ethol Ecol Evol 32:509–526. https://doi.org/10.1080/03949370.2020.1769739
doi: 10.1080/03949370.2020.1769739
Dias VS, Pereira da Luz M, Medero G, Tarley Ferreira Nascimento D (2018) An overview of hydropower reservoirs in Brazil: current situation, future perspectives and impacts of climate change. Water 10:592. https://doi.org/10.3390/w10050592
doi: 10.3390/w10050592
Doussang D, González-Acuña D, Torres-Fuentes LG et al (2019) Spatial distribution, prevalence and diversity of haemosporidians in the rufous-collared sparrow, Zonotrichia capensis. Parasit Vectors 12:2. https://doi.org/10.1186/s13071-018-3243-4
doi: 10.1186/s13071-018-3243-4 pubmed: 30606248 pmcid: 6318949
Fallon SM, Bermingham E, Ricklefs RE (2005) Host specialization and geographic localization of avian malaria parasites: a regional analysis in the Lesser Antilles. Am Nat 165:466–480. https://doi.org/10.1086/428430
doi: 10.1086/428430 pubmed: 15791538
Fecchio A, Bell JA, Bosholn M et al (2020b) An inverse latitudinal gradient in infection probability and phylogenetic diversity for Leucocytozoon blood parasites in New World birds. J Anim Ecol 89:423–435. https://doi.org/10.1111/1365-2656.13117
doi: 10.1111/1365-2656.13117 pubmed: 31571223
Fecchio A, Bell JA, Collins MD et al (2018b) Diversification by host switching and dispersal shaped the diversity and distribution of avian malaria parasites in Amazonia. Oikos 127:1233–1242. https://doi.org/10.1111/oik.05115
doi: 10.1111/oik.05115
Fecchio A, Bell JA, Pinheiro RBP et al (2019) Avian host composition, local speciation and dispersal drive the regional assembly of avian malaria parasites in South American birds. Mol Ecol 28:2681–2693. https://doi.org/10.1111/mec.15094
doi: 10.1111/mec.15094 pubmed: 30959568
Fecchio A, Chagas CRF, Bell JA, Kirchgatter K (2020a) Evolutionary ecology, taxonomy, and systematics of avian malaria and related parasites. Acta Trop 204:105364. https://doi.org/10.1016/j.actatropica.2020.105364
doi: 10.1016/j.actatropica.2020.105364 pubmed: 32007445
Fecchio A, Clark NJ, Bell JA et al (2021a) Global drivers of avian haemosporidian infections vary across zoogeographical regions. Global Ecol Biogeogr 30:2393–2406. https://doi.org/10.1111/geb.13390
doi: 10.1111/geb.13390
Fecchio A, de Faria IP, Bell JA et al (2021b) Mining increases the prevalence of avian haemosporidian parasites in Northeast Amazonia. Parasitol Res 120:605–613. https://doi.org/10.1007/s00436-020-06986-9
doi: 10.1007/s00436-020-06986-9 pubmed: 33415388
Fecchio A, Lima MR, Bell JA et al (2021c) Loss of forest cover and host functional diversity increases prevalence of avian malaria parasites in the Atlantic Forest. Int J Parasitol 51:719–728. https://doi.org/10.1016/j.ijpara.2021.01.001
doi: 10.1016/j.ijpara.2021.01.001 pubmed: 33722680
Fecchio A, Pinheiro R, Felix G et al (2018a) Host community similarity and geography shape the diversity and distribution of haemosporidian parasites in Amazonian birds. Ecography 41:505–515. https://doi.org/10.1111/ecog.03058
doi: 10.1111/ecog.03058
Fecchio A, Silveira P, Weckstein JD et al (2018c) First record of Leucocytozoon (Haemosporida: Leucocytozoidae) in Amazonia: evidence for rarity in neotropical lowlands or lack of sampling for this parasite genus? J Parasitol 104:168–172. https://doi.org/10.1645/17-182
doi: 10.1645/17-182 pubmed: 29346738
Feldman RA, Freed LA, Cann RL (1995) A PCR test for avian malaria in Hawaiian birds. Mol Ecol 4:663–674. https://doi.org/10.1111/j.1365-294X.1995.tb00267.x
doi: 10.1111/j.1365-294X.1995.tb00267.x pubmed: 8564006
Ferreira Junior FC, Rodrigues RA, Ellis VA et al (2017) Habitat modification and seasonality influence avian haemosporidian parasite distributions in southeastern Brazil. PLoS One 12:e0178791. https://doi.org/10.1371/journal.pone.0178791
doi: 10.1371/journal.pone.0178791 pubmed: 28575046 pmcid: 5456369
Forrester DJ, Greiner EC (2008) Leucocytozoonosis. In: Atkinson CT, Thomas NJ, Hunter DB (eds) Parasitic diseases of wild birds. Wiley-Blackwell, Ames, Iowa
Fränzle O (2003) Chapter 2 Bioindicators and environmental stress assessment. In: Trace Metals and other Contaminants in the Environment. Elsevier, pp 41–84
González M, López S, Mullens BA et al (2013) A survey of Culicoides developmental sites on a farm in northern Spain, with a brief review of immature habitats of European species. Vet Parasitol 191:81–93. https://doi.org/10.1016/j.vetpar.2012.08.025
doi: 10.1016/j.vetpar.2012.08.025 pubmed: 22999100
Hellgren WJ, Bensch S (2004) A new PCR assay for simultaneous studies of Leucocytozoon, Plasmodium, and Haemoproteus from avian blood. J Parasitol 90:797–802. https://doi.org/10.1645/GE-184R1
doi: 10.1645/GE-184R1 pubmed: 15357072
Hudson P (1998) Competition mediated by parasites: biological and theoretical progress. Trends Ecol Evol 13:387–390. https://doi.org/10.1016/S0169-5347(98)01475-X
doi: 10.1016/S0169-5347(98)01475-X pubmed: 21238357
Huelsenbeck JP, Ronquist F (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17:754–755. https://doi.org/10.1093/bioinformatics/17.8.754
doi: 10.1093/bioinformatics/17.8.754 pubmed: 11524383
ICMBio (1997) Plano de Manejo da Reserva Biológica de Uatumã. ICMBio, Brasília, p 4162
ICMBio (2018) Livro Vermelho da Fauna Brasileira Ameaçada de Extinção: Volume III - Aves. ICMBio, Brasília, p 4162
Illera JC, Fernández-Álvarez Á, Hernández-Flores CN, Foronda P (2015) Unforeseen biogeographical patterns in a multiple parasite system in Macaronesia. J Biogeogr 42:1858–1870. https://doi.org/10.1111/jbi.12548
doi: 10.1111/jbi.12548
Ishtiaq F, Renner SC (2020) Bird migration and vector-borne parasite transmission. In: Santiago-Alarcon D, Marzal A (eds) Avian Malaria and Related Parasites in the Tropics. Springer International Publishing, Cham, pp 513–526
doi: 10.1007/978-3-030-51633-8_16
IUCN 2023. The IUCN red list of threatened species. Version 2022-2. https://www.iucnredlist.org . Accessed 10 Jan 2022
Jetz W, Thomas GH, Joy JB, Hartmann K, Mooers AO (2012) The global diversity of birds in space and time. Nature. 491(7424):444–448. https://doi.org/10.1038/nature11631
doi: 10.1038/nature11631 pubmed: 23123857
Lacorte GA, Félix GMF, Pinheiro RRB et al (2013) Exploring the diversity and distribution of neotropical avian malaria parasites — a molecular survey from Southeast Brazil. PLoS One 8:e57770. https://doi.org/10.1371/journal.pone.0057770
doi: 10.1371/journal.pone.0057770 pubmed: 23469235 pmcid: 3585926
Lauron EJ, Loiseau C, Bowie RCK et al (2014) Coevolutionary patterns and diversification of avian malaria parasites in African sunbirds (family Nectariniidae). Parasitology 142:635–647. https://doi.org/10.1017/S0031182014001681
doi: 10.1017/S0031182014001681 pubmed: 25352083
Loiseau C, Melo M, Lobato E et al (2017) Insularity effects on the assemblage of the blood parasite community of the birds from the Gulf of Guinea. J Biogeogr 44:2607–2617. https://doi.org/10.1111/jbi.13060
doi: 10.1111/jbi.13060 pubmed: 29104347 pmcid: 5663302
Lotta IA, Gonzalez AD, Pacheco MA et al (2015) Leucocytozoon pterotenuis sp. nov. (Haemosporida, Leucocytozoidae): description of the morphologically unique species from the Grallariidae birds, with remarks on the distribution of Leucocytozoon parasites in the Neotropics. Parasitol Res 114:1031–1044. https://doi.org/10.1007/s00436-014-4269-y
doi: 10.1007/s00436-014-4269-y pubmed: 25544705
MacArthur RH, Wilson EO (1967) The theory of island biogeography. Princeton University Press, Princeton
Marzal A, de Lope F, Navarro C, Møller AP (2005) Malarial parasites decrease reproductive success: an experimental study in a passerine bird. Oecologia 142:541–545. https://doi.org/10.1007/s00442-004-1757-2
doi: 10.1007/s00442-004-1757-2 pubmed: 15688214
Munck A, Guyre PM, Holbrook NJ (1984) Physiological functions of glucocorticoids in stress and their relation to pharmacological actions. Endocr Rev 5:25–44. https://doi.org/10.1210/edrv-5-1-25
doi: 10.1210/edrv-5-1-25 pubmed: 6368214
Olson SH, Gangnon R, Silveira GA, Patz JA (2010) Deforestation and malaria in Mâncio Lima County, Brazil. Emerg Infect Dis 16:1108–1115. https://doi.org/10.3201/eid1607.091785
doi: 10.3201/eid1607.091785 pubmed: 20587182 pmcid: 3321904
Pérez-Rodríguez A, Ramírez Á, Richardson DS, Pérez-Tris J (2013) Evolution of parasite island syndromes without long-term host population isolation: parasite dynamics in Macaronesian blackcaps S ylvia atricapilla: Blackcap haemosporidians in Macaronesia. Glob Ecol Biogeogr 22:1272–1281. https://doi.org/10.1111/geb.12084
doi: 10.1111/geb.12084
Philips JR (1990) What’s bugging your birds? Avian parasitic arthropods. Wildl Rehab 8:155–203
Primack RB, Rodrigues E (2001) Biologia da Conservação, 1st edn. Planta, Londrina
Rambaut (2010) FigTree: Tree Figure Drawing Tool Version 1.4.0. Institute of Evolutionary Biology, University of Edinburgh
Ricklefs RE, Fallon SM, Bermingham E (2004) Evolutionary relationships, cospeciation, and host switching in avian malaria parasites. Syst Biol 53:111–119. https://doi.org/10.1080/10635150490264987
doi: 10.1080/10635150490264987 pubmed: 14965906
Santiago-Alarcon D, Palinauskas V, Schaefer HM (2012) Diptera vectors of avian Haemosporidian parasites: untangling parasite life cycles and their taxonomy. Biol Rev 87:928–964. https://doi.org/10.1111/j.1469-185X.2012.00234.x
doi: 10.1111/j.1469-185X.2012.00234.x pubmed: 22616880
Schöngart J, Wittmann F, Faria de Resende A et al (2021) The shadow of the Balbina dam: a synthesis of over 35 years of downstream impacts on floodplain forests in Central Amazonia. Aquatic Conserv: Mar Freshw Ecosyst 31:1117–1135. https://doi.org/10.1002/aqc.3526
doi: 10.1002/aqc.3526
Sehgal RNM (2015) Manifold habitat effects on the prevalence and diversity of avian blood parasites. Int. J Parasitol Parasites Wildl 4:421–430. https://doi.org/10.1016/j.ijppaw.2015.09.001
doi: 10.1016/j.ijppaw.2015.09.001 pubmed: 26835250 pmcid: 4699977
Silva JMC, Rylands AB, Fonseca GAB (2005) The fate of the Amazonian areas of endemism. Conserv Biol 19:689–694.  http://www.jstor.org/stable/3591055
doi: 10.1111/j.1523-1739.2005.00705.x
Valkiūnas G (2005) Avian malaria parasites and other haemosporidia, 1st edn. CRC Press
Valkiūnas G, Zehtindjiev P, Dimitrov D et al (2008) Polymerase chain reaction-based identification of Plasmodium (Huffia) elongatum, with remarks on species identity of haemosporidian lineages deposited in GenBank. Parasitol Res 102:1185–1193. https://doi.org/10.1007/s00436-008-0892-9
doi: 10.1007/s00436-008-0892-9 pubmed: 18270739
Vanstreels R, da Silva-Filho R, Kolesnikovas C et al (2015) Epidemiology and pathology of avian malaria in penguins undergoing rehabilitation in Brazil. Vet Res 46:30. https://doi.org/10.1186/s13567-015-0160-9
doi: 10.1186/s13567-015-0160-9 pubmed: 25888987 pmcid: 4357068
Vittor AY, Pan W, Gilman RH et al (2009) Linking deforestation to malaria in the Amazon: characterization of the breeding habitat of the principal malaria vector, Anopheles darlingi. Am J Trop Med Hyg 81:5–12
pubmed: 19556558
White EM, Greiner EC, Bennett GF, Herman CM (1978) Distribution of the hematozoa of Neotropical birds. Rev Biol Trop 26(Suppl 1):43–102
pubmed: 108771
Whitney BM, Cohn-Haft M (2013) Fifteen new species of Amazonian birds. In: del Hoyo J, Elliotte A, Christie D (eds) Handbook of the Birds of the World, Volume Special Volume: New Species and Global Index. Lynx Edicions
Whittaker RJ, Fernández-Palacios JM (2007) Island biogeography: ecology, evolution, and conservation, 2nd edn. Oxford University Press, Oxford, New York
Willis EO, Oniki Y (1988) Aves observadas em Balbina, Amazonas e os prováveis efeitos da barragem. Ciênc Cult 40:280–284
Wingfield JC (2013) The comparative biology of environmental stress: behavioural endocrinology and variation in ability to cope with novel, changing environments. Anim Behav 85:1127–1133. https://doi.org/10.1016/j.anbehav.2013.02.018
doi: 10.1016/j.anbehav.2013.02.018
Ya’cob Z, Takaoka H, Pramual P et al (2016) Breeding habitat preference of preimaginal black flies (Diptera: Simuliidae) in Peninsular Malaysia. Acta Trop 153:57–63. https://doi.org/10.1016/j.actatropica.2015.10.007
doi: 10.1016/j.actatropica.2015.10.007 pubmed: 26476394

Auteurs

Carolina C Anjos (CC)

Programa de Pós-Graduação em Medicina Tropical, Instituto de Medicina Tropical, Faculdade de Medicina, Universidade de São Paulo, São Paulo, SP, 05403-000, Brazil.

Thiago Bicudo (T)

Instituto de Desenvolvimento Sustentável Mamirauá, Tefé, AM, 69553-225, Brazil.

Alan Fecchio (A)

Centro de Investigación Esquel de Montaña y Estepa Patagónica (CIEMEP), CONICET - Universidad Nacional de la Patagonia San Juan Bosco, Esquel, Chubut, Argentina.

Marina Anciães (M)

Instituto Nacional de Pesquisas da Amazônia, Coordenação de Biodiversidade, Manaus, AM, 69081-000, Brazil.

Bruno S Mathias (BS)

Programa de Pós-Graduação em Medicina Tropical, Instituto de Medicina Tropical, Faculdade de Medicina, Universidade de São Paulo, São Paulo, SP, 05403-000, Brazil.

Carolina R F Chagas (CRF)

Nature Research Centre, 08412, Vilnius, Lithuania.

Jeffrey A Bell (JA)

Department of Biology, University of North Dakota, 10 Cornell Street, Grand Forks, ND, 58202, USA.

Lilian O Guimarães (LO)

Laboratório de Bioquímica e Biologia Molecular, Instituto Pasteur, São Paulo, SP, 01027-000, Brazil.

Eliana F Monteiro (EF)

Laboratório de Bioquímica e Biologia Molecular, Instituto Pasteur, São Paulo, SP, 01027-000, Brazil.

Karin Kirchgatter (K)

Programa de Pós-Graduação em Medicina Tropical, Instituto de Medicina Tropical, Faculdade de Medicina, Universidade de São Paulo, São Paulo, SP, 05403-000, Brazil. karink@usp.br.
Laboratório de Bioquímica e Biologia Molecular, Instituto Pasteur, São Paulo, SP, 01027-000, Brazil. karink@usp.br.

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