{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,1,25]],"date-time":"2026-01-25T21:56:44Z","timestamp":1769378204198,"version":"3.49.0"},"reference-count":50,"publisher":"FapUNIFESP (SciELO)","issue":"4","license":[{"start":{"date-parts":[[2019,1,1]],"date-time":"2019-01-01T00:00:00Z","timestamp":1546300800000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"},{"start":{"date-parts":[[2019,1,1]],"date-time":"2019-01-01T00:00:00Z","timestamp":1546300800000},"content-version":"am","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"},{"start":{"date-parts":[[2019,1,1]],"date-time":"2019-01-01T00:00:00Z","timestamp":1546300800000},"content-version":"tdm","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Biota Neotrop."],"abstract":"<jats:p>Abstract: According to the enemy release hypothesis (ERH) the spread of invasive species will be facilitated by release from their enemies as they occupy new areas. However, the ERH has rarely been tested by comparing populations of native (non-invasive, long established) species with expanding or shifting ranges, to the same species as invasive in another area. We tested the ERH with respect to blood parasite levels (prevalence and intensity of Plasmodium spp. and Haemoproteus spp.) of (a) two closely related, widely distributed species of thrush (Turdus leucomelas and T. merula), and (b) an invasive sparrow (Passer domesticus) whose range has expanded from the Old World to the New World since the 18th century. A total of 158 birds were sampled in Portugal and 99 in Brazil. All bird species were parasitized, and 55% of the individuals collected were parasitized, and the mean intensity of infection was of 28 parasites per 10,000 erythrocytes. We assessed whether differences in levels of infection (prevalence and intensity) were due to site (tropical\/New World and temperate\/Old World) or host species. The ERH was supported: Passer domesticus and Turdus merula had higher levels of parasitism in the Old World than in the New World. Thus, P. domesticus seems to be benefitting from its \"recent\" range expansion, compared to T. leucomelas, through ecological release from its native parasites and because the parasites of the recently invaded area seem to be infesting native species instead.<\/jats:p>","DOI":"10.1590\/1676-0611-bn-2018-0716","type":"journal-article","created":{"date-parts":[[2019,9,7]],"date-time":"2019-09-07T15:25:14Z","timestamp":1567869914000},"source":"Crossref","is-referenced-by-count":11,"title":["Patterns of avian malaria in tropical and temperate environments: testing the \"The enemy release hypothesis\""],"prefix":"10.1590","volume":"19","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-5582-8193","authenticated-orcid":false,"given":"Yasmine","family":"Antonini","sequence":"first","affiliation":[{"name":"Universidade Federal de Ouro Preto,  Brasil"}]},{"given":"Debora Nogueira Campos","family":"Lobato","sequence":"additional","affiliation":[{"name":"Universidade Federal de Ouro Preto,  Brasil"}]},{"given":"Ana Cl\u00e1udia","family":"Norte","sequence":"additional","affiliation":[{"name":"Universidade de Coimbra,  Portugal"}]},{"given":"Jaime A.","family":"Ramos","sequence":"additional","affiliation":[{"name":"Universidade de Coimbra,  Portugal; Universidade de Coimbra,  Portugal"}]},{"given":"Patr\u00edcia de Abreu","family":"Moreira","sequence":"additional","affiliation":[{"name":"Universidade Federal de Ouro Preto,  Brasil"}]},{"given":"Erika Martins","family":"Braga","sequence":"additional","affiliation":[{"name":"Universidade Federal de Minas Gerais,  Brasil"}]}],"member":"530","published-online":{"date-parts":[[2019]]},"reference":[{"issue":"2","key":"ref1","doi-asserted-by":"crossref","first-page":"558","DOI":"10.1093\/auk\/122.2.558","article-title":"Male reproductive success is correlated with blood parasite levels and body condition in the promiscuous aquatic warbler (Acrocephalus paludicola)","volume":"122","author":"ANDREZJ D.","year":"2005","journal-title":"Auk"},{"issue":"3","key":"ref2","article-title":"Prevalence and lineage diversity of avian haemosporidians from three distinct cerrado habitats in Brazil","volume":"6","author":"BELO N.O.","year":"2011","journal-title":"PLOS ONE"},{"issue":"2","key":"ref3","doi-asserted-by":"crossref","first-page":"339","DOI":"10.7589\/0090-3558-24.2.339","article-title":"Influence of blood parasites on the body mass of Passeriform birds","volume":"24","author":"BENNETT G.F.","year":"1988","journal-title":"J. Wildlife Dis"},{"key":"ref4","series-title":"Current Ornithology","first-page":"67","volume-title":"Assessing body condition in birds","author":"BROWN M.E.","year":"1996"},{"issue":"1-2","key":"ref5","doi-asserted-by":"crossref","first-page":"74","DOI":"10.1016\/j.vetpar.2013.04.025","article-title":"The pathology and pathogenicity of a novel Haemoproteus spp. infection in wild Little Penguins (Eudyptula minor)","volume":"197","author":"CANNELL B.L.","year":"2013","journal-title":"Vet. Parasitol."},{"issue":"14","key":"ref6","doi-asserted-by":"crossref","first-page":"891","DOI":"10.1016\/j.ijpara.2015.08.008","article-title":"Specialist enemies, generalist weapons and the potential spread of exotic pathogens: malaria parasites in a highly invasive bird","volume":"45","author":"CLARK N.J.","year":"2015","journal-title":"Intl. J. Parasitol."},{"key":"ref7","series-title":"Thrushes","author":"CLEMENT P.","year":"2000"},{"key":"ref8","series-title":"Handbook of birds of the world","first-page":"514","volume-title":"Family Turdidae (thrushes)","author":"COLLAR N.","year":"2005"},{"key":"ref9","series-title":"Dynamics of Populations: Proceedings of the Advanced Study Institute on Dynamics of Numbers in Populations","first-page":"298","volume-title":"On the role of natural enemies in preventing competitive exclusion in some marine animals and in rain forest trees","author":"CONNELL J.H.","year":"1971"},{"issue":"6","key":"ref10","doi-asserted-by":"crossref","first-page":"1737","DOI":"10.1002\/ece3.1889","article-title":"Costs of resistance and infection by a generalist pathogen","volume":"6","author":"DALLAS T.","year":"2016","journal-title":"Ecol. Evol."},{"issue":"1","key":"ref11","doi-asserted-by":"crossref","first-page":"83","DOI":"10.2307\/3676964","article-title":"Blood parasites, health, reproductive success, and egg volume in female Great Tit Parus major","volume":"27","author":"DULFA R.","year":"1996","journal-title":"J. Avian Biol"},{"key":"ref12","series-title":"Guia ilustrado das aves de Porto Alegre","author":"EFE M. A.","year":"2001"},{"issue":"5","key":"ref13","doi-asserted-by":"crossref","first-page":"1044","DOI":"10.1645\/GE-3157","article-title":"Detecting Avian Malaria: an improved polymerase chain reaction diagnostic","volume":"89","author":"FALLON S.M.","year":"2003","journal-title":"J. Parasitol."},{"issue":"12","key":"ref14","doi-asserted-by":"crossref","first-page":"1419","DOI":"10.1139\/Z08-129","article-title":"Reduced parasite infestation in urban Eurasian blackbirds (Turdus merula): a factor favoring urbanization?","volume":"86","author":"GEUE D.","year":"2008","journal-title":"Can. J. Zoolog."},{"issue":"4","key":"ref15","doi-asserted-by":"crossref","first-page":"558","DOI":"10.7589\/0090-3558-23.4.558","article-title":"Quantification of hematozoa in blood smears","volume":"23","author":"GODFREY Jr. R.D.","year":"1987","journal-title":"J. Wildlife Dis"},{"issue":"4","key":"ref16","doi-asserted-by":"crossref","first-page":"574","DOI":"10.1007\/s004420050482","article-title":"Blood parasites and nest defense behavior of Tengmalm's owls","volume":"114","author":"HAKKARAINEN H.","year":"1998","journal-title":"Oecologia"},{"issue":"4","key":"ref17","doi-asserted-by":"crossref","first-page":"849","DOI":"10.7589\/0090-3558-47.4.849","article-title":"Low Haemosporidian diversity and one key-host species in a bird malaria community on a mid-atlantic island (S\u00e3o Miguel, Azores)","volume":"47","author":"HELLGREN O.","year":"2011","journal-title":"J. Wildlife Dis"},{"issue":"2-3","key":"ref18","doi-asserted-by":"crossref","first-page":"441","DOI":"10.1023\/A:1010717502442","article-title":"Global-scale relationships between climate and the dengue fever vector, Aedes aegypti","volume":"48","author":"HOPP M.","year":"2001","journal-title":"Climatic Change"},{"issue":"1586","key":"ref19","doi-asserted-by":"crossref","first-page":"587","DOI":"10.1098\/rspb.2005.3313","article-title":"Prevalence and evolutionary relationships of haematozoan parasites in native versus introduced populations of common myna Acridotheres tristis","volume":"273","author":"ISHTIAQ F.","year":"2006","journal-title":"P. R. Soc. B."},{"issue":"940","key":"ref20","doi-asserted-by":"crossref","first-page":"501","DOI":"10.1086\/282687","article-title":"Herbivores and the number of tree species in tropical forests","volume":"104","author":"JANZEN D.","year":"1970","journal-title":"Am. Nat."},{"issue":"5","key":"ref21","doi-asserted-by":"crossref","first-page":"214","DOI":"10.1016\/j.pt.2006.02.011","article-title":"Parasite prevalence and sample size: misconceptions and solutions","volume":"22","author":"JOVANI R.","year":"2006","journal-title":"Trends Parasitol"},{"issue":"4","key":"ref22","doi-asserted-by":"crossref","first-page":"164","DOI":"10.1016\/S0169-5347(02)02499-0","article-title":"Exotic plant invasions and the enemy release hypothesis","volume":"17","author":"KEANE R.M.","year":"2002","journal-title":"Trends Ecol. Evol."},{"issue":"4","key":"ref23","doi-asserted-by":"crossref","first-page":"420","DOI":"10.2307\/2390029","article-title":"Blood parasites and reproductive success of Tengmalm's owls: detrimental effects on females but not on males?","volume":"7","author":"KORPIMAKI E.","year":"1993","journal-title":"Funct. Ecol."},{"issue":"7","key":"ref24","doi-asserted-by":"crossref","first-page":"654","DOI":"10.1046\/j.1461-0248.2003.00480.x","article-title":"How should environmental stress affect the population dynamics of disease?","volume":"6","author":"LAFFERTY K.D.","year":"2003","journal-title":"Ecol. Lett."},{"key":"ref25","series-title":"Species invasions: insights into ecology, evolution, and biogeography","first-page":"111","volume-title":"The role of infectious diseases in natural communities: what introduced species tell us","author":"LAFFERTY K.D.","year":"2005"},{"issue":"4","key":"ref26","first-page":"297","article-title":"Low prevalence of haemosporidian parasites in the introduced house sparrow (Passer domesticus) in Brazil","volume":"55","author":"LIMA M.R.","year":"2010","journal-title":"Acta Parasit"},{"issue":"6","key":"ref27","doi-asserted-by":"crossref","first-page":"771","DOI":"10.1590\/S1984-46702011000600010","article-title":"Hematological and parasitological health conditions of the Pale-breasted Thrush (Turdus leucomelas) (Passeriformes: Turdidae) in southeastern Brazil","volume":"28","author":"LOBATO D.N.C.","year":"2011","journal-title":"Zoolog"},{"issue":"1709","key":"ref28","doi-asserted-by":"crossref","first-page":"1264","DOI":"10.1098\/rspb.2010.1968","article-title":"Plasmodium relictum infection and MHC diversity in the house sparrow (Passer domesticus)","volume":"278","author":"LOISEAU C.","year":"2011","journal-title":"P. R. Soc. B."},{"issue":"2","key":"ref29","doi-asserted-by":"crossref","first-page":"419","DOI":"10.1111\/j.1474-919X.2007.00668.x","article-title":"Greater seasonal variation in blood and ectoparasite infections in a temperate than a tropical population of House Sparrows Passer domesticus in North America","volume":"149","author":"MARTIN L.B.","year":"2007","journal-title":"Ibis"},{"issue":"4","key":"ref30","doi-asserted-by":"crossref","first-page":"541","DOI":"10.1007\/s00442-004-1757-2","article-title":"Malarial parasites decrease reproductive success: an experimental study in a passerine bird","volume":"142","author":"MARZAL A.","year":"2005","journal-title":"Oecologia"},{"issue":"7","key":"ref31","doi-asserted-by":"crossref","DOI":"10.1371\/journal.pone.0021905","article-title":"Diversity, loss, and gain of malaria parasites in a globally invasive bird","volume":"6","author":"MARZAL A.","year":"2011","journal-title":"PLOS ONE"},{"issue":"10","key":"ref32","doi-asserted-by":"crossref","first-page":"1798","DOI":"10.1139\/z95-212","article-title":"Geographic and individual variation in haematozoan infections in the greenfinch, Carduelis chloris","volume":"73","author":"MERIL\u00c4 J.","year":"1995","journal-title":"Can. J. Zool"},{"issue":"4","key":"ref33","doi-asserted-by":"crossref","first-page":"629","DOI":"10.1093\/beheco\/arh054","article-title":"Predation risk, host imune response, and parasitism","volume":"15","author":"NAVARRO C.","year":"2004","journal-title":"Behav. Ecol."},{"issue":"4","key":"ref34","doi-asserted-by":"crossref","first-page":"677","DOI":"10.1111\/j.1474-919X.2009.00960.x","article-title":"Haematozoa infections in a great tit Parus major population in Central Portugal: relationship with breeding effort and health","volume":"151","author":"NORTE A.C.","year":"2009","journal-title":"Ibis"},{"issue":"2","key":"ref35","doi-asserted-by":"crossref","first-page":"257","DOI":"10.1080\/10635150802044003","article-title":"Accounting for phylogenetic uncertainty in biogeography: a bayesian approach to dispersal-vicariance analysis of the Thrushes (Aves: Turdus)","volume":"57","author":"NYLANDER J.A.A.","year":"2008","journal-title":"Syst. Biol."},{"issue":"8","key":"ref36","doi-asserted-by":"crossref","first-page":"370","DOI":"10.1016\/S1471-4922(03)00149-1","article-title":"Mixed models: getting the best use of parasitological data","volume":"19","author":"PATERSON S.","year":"2003","journal-title":"Trends Parasitol"},{"key":"ref37","series-title":"R: A language and environment for statistical computing"},{"issue":"10","key":"ref38","doi-asserted-by":"crossref","first-page":"4722","DOI":"10.1073\/pnas.89.10.4722","article-title":"Embryonic development period and prevalence of avian blood parasites","volume":"89","author":"RICKLEFS R.E.","year":"1992","journal-title":"Proc. Nat. Acad. Sci."},{"issue":"4","key":"ref39","doi-asserted-by":"crossref","first-page":"1254","DOI":"10.1093\/auk\/124.4.1254","article-title":"Malaria prevalence and white-blood-cell response to infection in a tropical and in a temperate thrush","volume":"124","author":"RICKLEFS R.E.","year":"2007","journal-title":"Auk"},{"key":"ref40","doi-asserted-by":"crossref","first-page":"928","DOI":"10.1111\/j.1469-185X.2012.00234.x","article-title":"Diptera vectors of avian haemosporidian parasites: untangling parasite life cycles and their taxonomy","volume":"87","author":"SANTIAGO-ALARCON D.","year":"2012","journal-title":"Biol. Rev."},{"issue":"3","key":"ref41","doi-asserted-by":"crossref","first-page":"441","DOI":"10.1111\/j.0021-8790.2004.00815.x","article-title":"A trade-off between two resource- demanding functions: post-nuptial molt and immunity during reproduction in male Pied Flycatchers","volume":"73","author":"SANZ J.J.","year":"2004","journal-title":"J. Anim. Ecol."},{"issue":"1","key":"ref42","doi-asserted-by":"crossref","first-page":"130","DOI":"10.1642\/0004-8038(2003)120[0130:SPOAHP]2.0.CO;2","article-title":"Seasonal prevalence of a haematozoan parasite of red-bellied woodpeckers (Melanerpes carolinus) and its association with host condition and overwinter survival","volume":"120","author":"SCHRADER M.S.","year":"2003","journal-title":"Auk"},{"issue":"1","key":"ref43","doi-asserted-by":"crossref","first-page":"69","DOI":"10.2989\/00306521003690630","article-title":"Infection prevalence and absence of positive correlation between avian haemosporidian parasites, mass and body condition in the cape weaver Ploceus capensis","volume":"81","author":"SCHULTZ A.","year":"2010","journal-title":"Ostrich"},{"issue":"1","key":"ref44","doi-asserted-by":"crossref","first-page":"7","DOI":"10.1590\/S1984-29612012000100003","article-title":"Blood parasites in passerine birds from the Brazilian Atlantic Forest","volume":"21","author":"SEBAIO F.","year":"2012","journal-title":"Rev. Bras. Parasitol."},{"key":"ref45","series-title":"The Sparrows: a study of the genus Passer","author":"SUMMERS-SMITH J.D.","year":"1988","edition":"1 ed"},{"issue":"6923","key":"ref46","doi-asserted-by":"crossref","first-page":"628","DOI":"10.1038\/nature01346","article-title":"Introduced species and their missing parasites","volume":"421","author":"TORCHIN M.E.","year":"2003","journal-title":"Nature"},{"issue":"2","key":"ref47","doi-asserted-by":"crossref","first-page":"418","DOI":"10.1645\/GE-3547RN.1","article-title":"Nested cytochrome b polymerase chain reaction diagnostics underestimate mixed infections of avian blood haemosporidian parasites: microscopy is still essential","volume":"92","author":"VALKI\u016aNAS G.","year":"2006","journal-title":"J. Parasitol."},{"key":"ref48","series-title":"Avian malaria parasites and other haemosporidia","author":"VALKI\u016aNAS G.","year":"2005","edition":"1 ed"},{"issue":"4","key":"ref49","article-title":"Outbreak of avian malaria associated to multiple species of Plasmodium in Magellanic Penguins undergoing rehabilitation in Southern Brazil","volume":"9","author":"VANSTREELS R.E.T.","year":"2014","journal-title":"PLOS ONE"},{"issue":"2","key":"ref50","doi-asserted-by":"crossref","first-page":"101","DOI":"10.2307\/1365954","article-title":"The role of introduced diseases in the extinction of the endemic Hawaiian avifauna","volume":"70","author":"WARNER R.E.","year":"1968","journal-title":"Condor"}],"container-title":["Biota Neotropica"],"original-title":[],"link":[{"URL":"http:\/\/www.scielo.br\/pdf\/bn\/v19n4\/1676-0611-bn-19-04-e20180716.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2020,2,7]],"date-time":"2020-02-07T16:51:31Z","timestamp":1581094291000},"score":1,"resource":{"primary":{"URL":"http:\/\/www.scielo.br\/scielo.php?script=sci_arttext&pid=S1676-06032019000400204&tlng=en"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2019]]},"references-count":50,"journal-issue":{"issue":"4","published-online":{"date-parts":[[2019]]}},"alternative-id":["S1676-06032019000400204"],"URL":"https:\/\/doi.org\/10.1590\/1676-0611-bn-2018-0716","relation":{},"ISSN":["1676-0611"],"issn-type":[{"value":"1676-0611","type":"electronic"}],"subject":[],"published":{"date-parts":[[2019]]},"article-number":"e20180716"}}