Parasitology Research

, Volume 118, Issue 2, pp 399–409 | Cite as

Ectoparasite sharing among native and invasive birds in a metropolitan area

  • Emilano MoriEmail author
  • Jordi Pascual Sala
  • Niccolò Fattorini
  • Mattia Menchetti
  • Tomas Montalvo
  • Juan Carlos Senar
Arthropods and Medical Entomology - Original Paper


Parasite-mediated competition has been reported to be one of the most harmful, although overlooked, impacts that alien species have on native ecosystems. Monk parakeets Myiopsitta monachus are successful invaders in Europe, where they have been introduced from South America. Colonial nests of these parrots may also host other species, e.g. the rock pigeon Columba livia forma domestica. In this work, we analysed the ectoparasite composition of monk parakeets in Barcelona (Spain) and we evaluated their potential role as parasite-mediated competitors, by comparing their parasitic load with that of coexisting rock pigeons. Only two arthropod species were observed on monk parakeets, whereas four species were detected on pigeons. Parakeets were rarely infested by pigeon parasites (prevalence = 0.66%), whereas parakeet mites were recorded more often on pigeons (prevalence = 10.00%). The number of total parasites per bird increased with increasing densities of monk parakeets, both for pigeons and for parakeets. Therefore, overcrowding of birds due to the increasing population of monk parakeets in Barcelona may affect the health status of native pigeons, suggesting a potential role for parasite mediated competition by introduced parakeets. Furthermore, spill-over of alien mites (Ornithonyssus bursa) by monk parakeets to rock pigeons should be monitoring as it may affect human health.


Alien species Columba livia Myiopsitta monachus Parasite-mediated competition Spill-back Spill-over 



Birds were handled and ringed with the permission of Institut Català d’Ornitologia and the Environment Department of the Generalitat de Catalunya. We also wish to acknowledge the support provided by COST European Cooperation in Science and Technology Actions ES1304 “ParrotNet” for the development of this manuscript. The contents of this manuscript are the authors’ responsibility and neither COST nor any person acting on its behalf is responsible for the use that may be made of the information contained herein. D. Beal and V. Sfondrini kindly took the time to read our manuscript and improve English language and syntax. Two anonymous reviewers greatly improved our first draft with useful comments.

Author contributions

JCS, JP and EM conceived the idea and wrote most of the paper. TM, JP and JCS collected the parasites; EM and MM identified the parasites of monk parakeets. NF performed the statistical analyses and wrote the relevant part of the manuscript, as well as participated in writing the last draft.

Funding information

The present study was funded by CGL-2016-79568-C3-3-P research project to JCS from the Spanish Research Council (Ministry of Economics and Competiveness).

Compliance with ethical standards

All applicable international, national and/or institutional guidelines for the care and use of animals were followed.

Conflict of interest

The authors declare that they have no conflict of interest.

Data statement

All the data we used are included within the paper, in tables or figures. Further information may be asked by email to the corresponding author, by whom it may concern.

Supplementary material

436_2018_6174_MOESM1_ESM.docx (54 kb)
ESM 1 (DOCX 53 kb)


  1. Ancillotto L, Mazza G, Menchetti M, Mori E (2014) Host specificity of the badger’s flea (Paraceras melis) and first detection on a bat host. Paras Res 113:3909–3912CrossRefGoogle Scholar
  2. Ancillotto L, Studer V, Howard T, Smith VS, McAlister E, Beccaloni J, Manzia F, Renzopaoli F, Bosso L, Russo D, Mori E (2018) Environmental drivers of parasite load and species richness in introduced parakeets in an urban landscape. Paras Res 117:3591–3599CrossRefGoogle Scholar
  3. Appelt CW, Ward LC, Bender C, Fasenella J, Van Vossen BJ, Knight L (2016) Examining potential relationships between exotic monk parakeets (Myiopsitta monachus) and avian communities in an urban environment. Wilson J Ornit 128:556–566CrossRefGoogle Scholar
  4. Aramburú RM, Campos Soldini MP (2008) Presencia de Psitticimex uritui (Hemiptera: Cimicidae) en nidos de caserote Pseudoseisura lophotes (Passeriformes: Furnariidae) en la provincia de Entre Ríos. Revista Soc Entomol Argentina 67:131–133Google Scholar
  5. Aramburù RM, Calvo S, Alzugaray ME, Cicchino A (2003) Ectoparasitic load of monk parakeet (Myiopsitta monachus) nestlings. Ornitologia Neotropical 14:415–418Google Scholar
  6. Baker AS (1999) Mites and ticks of domestic animals: an identification guide and information source. The Stationary Office, LondonGoogle Scholar
  7. Baldaccini NE, Giunchi D, Mongini E, Ragionieri L (2000) Foraging flights of wild rock doves (Columba l. livia): a spatio-temporal analysis. It. J Zool 67:371–377Google Scholar
  8. Bartoń K (2012) MuMIn: multi-model inference. R package version 1.15.6. Accessed: 22 May 2018
  9. Bates D, Maechler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Soft 6:1–48Google Scholar
  10. Batllori X, Nos R (1985) Presencia de la cotorrita gris (Myiopsitta monachus) y de la cotorrita de collar (Psittacula krameri) en el Area Metropolitana de Barcelona. Miscell Zool 9:407–411Google Scholar
  11. Burger J, Gochfeld M (2005) Nesting behavior and nest site selection in monk parakeets (Myiopsitta monachus) in the Pantanal of Brazil. Acta Ethol 8:23–34CrossRefGoogle Scholar
  12. Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information-theoretic approach. Springer-Verlag, New YorkGoogle Scholar
  13. Carboneras C, Genovesi P, Vilà M, Blackburn TM, Carrete M, Clavero M, D’hondt M, Orueta JF, Gallardo B, Geraldes P, Gonzàlez-Moreno P, Gregory RD, Nentwig W, Paquet JY, Pysek P, Rabistsch W, Ramirez I, Scalera R, Tella JL, Walton P, Wynde R (2018) A prioritised list of invasive alien species to assist the effective implementation of EU legislation. J Appl Ecol 55:539–547CrossRefGoogle Scholar
  14. Carrillo-Ortiz J (2009) Dinámica de poblaciones de la cotorra de pecho gris (Myiopsitta monachus) en la ciudad de Barcelona. PhD Thesis. University of Barcelona, BarcelonaGoogle Scholar
  15. Castiglioni R, Azzola C, Capelli F, Biancardi C (2015) Aspetti ecologici e riproduttivi del parrocchetto monaco (Myiopsitta monachus Boddaert, 1783) in una colonia in provincia di Bergamo. XVIII Congresso Italiano di Ornitologia, Caramanico Terme (Pescara), 17–20 September 2015, 17Google Scholar
  16. Colautti RI, Ricciardi A, Grigorovich IA, MacIsaac HJ (2014) Is invasion success explained by the enemy release hypothesis? Ecol Lett 7:721–733CrossRefGoogle Scholar
  17. Covas L, Senar JC, Roqué L, Quesada J (2017) Records of fatal attacks by Rose-ringed parakeets Psittacula krameri on native avifauna. Revista Catalana d’Ornitologia 33:45–49Google Scholar
  18. Cox R, Stewart PD, Macdonald DW (1999) The ectoparasites of the European badger, Meles meles, and the behavior of the host-specific flea, Paraceras melis. J Insect Behav 12:245–265CrossRefGoogle Scholar
  19. Crowley SL, Hinchliffe S, McDonald RA (2017) Conflict in invasive species management. Front Ecol Environ 15:133–141CrossRefGoogle Scholar
  20. Crowley SL, Hinchliffe S, McDonald RA (2018) The parakeet protectors: understanding opposition to introduced species management. J Environ Manag 229:120–132. CrossRefGoogle Scholar
  21. Dangoisse G (2009) Étude de la population de Conures veuves (Myiopsitta monachus) de Bruxelles-Capitale. Aves 46:57–69Google Scholar
  22. Delgado CA, French K (2012) Parasite–bird interactions in urban areas: current evidence and emerging questions. Landsc Urban Plan 105:5–14CrossRefGoogle Scholar
  23. Di Santo M, Battisti C, Bologna MA (2016) Interspecific interactions in nesting and feeding urban sites among introduced monk parakeet (Myiopsitta monachus) and syntopic bird species. Ethol Ecol Evol 29:138–148CrossRefGoogle Scholar
  24. Edelaar P, Roques S, Hobson EA, Gonçalves da Silva A, Avery ML, Russello MA, Senar JC, Wright TF, Carrete M, Tella JL (2015) Shared genetic diversity across the global invasive range of the monk parakeet suggests a common restricted geographic origin and the possibility of convergent selection. Mol Ecol 24:2164–2176CrossRefGoogle Scholar
  25. Ferman LM, Peter HU, Montalti D (2010) A study of feral pigeon Columba livia var. in urban and suburban areas in the city of Jena, Germany. Arxius Misc Zool 8:1–8Google Scholar
  26. Fox J, Weisberg S (2011) An R companion to applied regression, 2nd edn. SAGE, Thousand Oaks, USAGoogle Scholar
  27. Haag-Wackernagel D (2005) Parasites from feral pigeons as a health hazard for humans. Ann Appl Biol 147:203–210CrossRefGoogle Scholar
  28. Hernández-Brito D, Carrete M, Popa-Lisseanu AG, Ibáñez C, Tella JL (2014) Crowding in the city: losing and winning competitors of an invasive bird. PLoS One 9:e100593CrossRefGoogle Scholar
  29. Hobson EA, Smith-Vidaurre G, Salinas-Melgoza A (2017) History of nonnative monk parakeets in Mexico. PloS ONE 12:e0184771Google Scholar
  30. Hutson AM (1984) Keds, flat-flies and bat-flies: Diptera, Hippoboscidae and Nycteribiidae. Royal Entomological Society of London, LondonGoogle Scholar
  31. Hyman J, Pruett-Jones S (1995) Natural history of the monk parakeet in Hyde Park, Chicago. Wilson Bull 3:510–517Google Scholar
  32. Johnson KP, Clayton DH (2003) The biology, ecology, and evolution of chewing lice. Illinois Nat Hist Surv Special Public 24:449–476Google Scholar
  33. Kelly DW, Paterson RA, Townsend CR, Poulin R, Tompkins DM (2009) Parasite spillback: a neglected concept in invasion ecology? Ecology 90:2047–2056CrossRefGoogle Scholar
  34. Lafferty KD, Holt RD (2003) How should environmental stress affect the population dynamics of disease? Ecol Lett 6:654–664CrossRefGoogle Scholar
  35. Lüdecke D (2018) sjstats: Statistical functions for regression models. R package version 0.17.1. Available online at Accessed 07 Sept 2018
  36. Lymbery AJ, Morine M, Kanani HG, Beatty SJ, Morgan DL (2014) Co-invaders: the effects of alien parasites on native hosts. Int J Parasitol 3:171–177Google Scholar
  37. MacGregor-Fors I, Calderón-Parra R, Meléndez-Herrada A, López-López S, Schondube JE (2011) Pretty, but dangerous! Records of non-native monk parakeets (Myiopsitta monachus) in Mexico. Rev Mex Biodiv 82:1053–1056Google Scholar
  38. Mack RN, Simberloff D, Lonsdale WM, Evans H, Clout M, Bazzaz FA (2000) Biotic invasions: causes, epidemiology, global consequences, and control. Ecol Appl 10:689–710CrossRefGoogle Scholar
  39. Marsot M, Chapuis JL, Gasqui P, Dozières A, Massèglia S, Pisanu B, Ferquel B, Vourc’h G (2013) Introduced Siberian chipmunk (Tamias sibiricus barberi) contribute more to Lyme borreliosis risk than native reservoir rodents. PLoS One 8:e55377CrossRefGoogle Scholar
  40. Masello JF, Martínez J, Calderón L, Wink M, Quillfeldt P, Sanz V, Theuerkauf J, Ortiz-Catedral L, Berkunsky I, Brunton D, Díaz-Luque JA, Hauber ME, Ojeda V, Barnaud A, Casalins L, Jackson B, Mijares A, Rosales R, Seixas G, Serafini P, Silva-Iturriza A, Sipinski E, Vásquez RA, Widmann P, Widmann I, Merino S (2018) Can the intake of antiparasitic secondary metabolites explain the low prevalence of hemoparasites among wild Psittaciformes? Parasit Vectors 11:357CrossRefGoogle Scholar
  41. Mazza G, Tricarico E, Genovesi P, Gherardi F (2014) Biological invaders are threats to human health: an overview. Ethol Ecol Evol 26:112–129CrossRefGoogle Scholar
  42. Mazzamuto MV, Pisanu B, Romeo C, Ferrari N, Preatoni D, Wauters LA, Chapuis JL, Martinoli A (2016) Poor parasite community of an invasive alien species: macroparasites of Pallas’s squirrel in Italy. Ann Zool Fennici 53:103–112CrossRefGoogle Scholar
  43. McInnes CJ, Coulter L, Dagleish MP, Deane D, Gilray J, Percival A, Willoughby K, Scantlebury M, Marks N, Graham D, Everest DJ, McGoldrick M, Rochford J, McKay F, Sainsbury AW (2013) The emergence of squirrel pox in Ireland. Anim Conserv 16:51–59CrossRefGoogle Scholar
  44. Menchetti M, Mori E (2014) Worldwide impact of alien parrots (Aves Psittaciformes) on native biodiversity and environment: a review. Ethol Ecol Evol 26:172–194CrossRefGoogle Scholar
  45. Menchetti M, Mori E, Angelici FM (2016) Effects of the recent world invasion by ring-necked parakeets Psittacula krameri. In: Angelici FM (ed) Problematic wildlife. A cross-disciplinary approach. Springer, New York, pp 253–266Google Scholar
  46. Moltoni E (1945) Pappagalli in libertà nei giardini pubblici di Milano e loro nidificazione in colonia in associazione con il passero. Riv It Ornitol 15:98–106Google Scholar
  47. Montalvo T, Pascual J, Senar JC, Peracho V (2017) Colom roquer Columba livia. In: Anton M, Herrando S, García D, Ferrer X, Parés M, Cebrian R (eds) Atles dels ocells nidificants de Barcelona. Barcelona. Ajuntament de Barcelona, Barcelona, pp 90–91Google Scholar
  48. Mori E, Ancillotto L, Groombridge J, Howard T, Smith VS, Menchetti M (2015a) Macroparasites of introduced parakeets in Italy: a possible role for parasite-mediated competition. Paras Res, 114:3277–3281Google Scholar
  49. Mori E, Sforzi A, Menchetti M, Mazza G, Lovari S, Pisanu B (2015b) Ectoparasite load in the crested porcupine Hystrix cristata Linnaeus, 1758 in Central Italy. Paras Res 114:2223–2229CrossRefGoogle Scholar
  50. Mori E, Pisanu B, Zozzoli R, Solano E, Olivieri E, Sassera D, Montagna M (2018a) Arthropods and associated pathogens from native and introduced rodents in Northeastern Italy. Paras Res, 117:3237–3243Google Scholar
  51. Mori E, Meini S, Strubbe D, Ancillotto L, Sposimo P, Menchetti M (2018b) Do alien free-ranging birds affect human health? A global summary of known zoonoses. In: Mazza G, Tricarico E (eds) Invasive species and human health. CABI Editions, Wallingford, pp 120–129CrossRefGoogle Scholar
  52. Muñoz AR, Real R (2006) Assessing the potential range expansion of the exotic monk parakeet in Spain. Divers Distrib 12:656–665CrossRefGoogle Scholar
  53. Navarro JL, Bucher EH (1990) Growth of monk parakeets. Wilson Bull 102:520–525Google Scholar
  54. Nentwig W, Bacher S, Kumschick S, Pyšek P, Vilà M (2018) More than “100 worst” alien species in Europe. Biol Invasions 6:1611–1621CrossRefGoogle Scholar
  55. Nores M (2009) Use of active monk parakeet nests by common pigeons and response by the host. Wilson J Ornith 121:812–815CrossRefGoogle Scholar
  56. Orton DI, Warren LJ, Wilkinson JD (2000) Avian mite dermatitis. Clin Experim Derm 25:129–131CrossRefGoogle Scholar
  57. Parau LG, Strubbe D, Mori E, Menchetti M, Ancillotto L, van Kleunen A, White RL, Hernàndez-Brito D, Le Louarn M, Clergeau P, Albayrak T, Franz D, Braun MP, Schroeder J, Wink M (2016) Rose-ringed parakeet Psittacula krameri populations and numbers in Europe: a complete overview. Open Orn J 9:1–13CrossRefGoogle Scholar
  58. Pascual J, Riba D, Senar JC (2015) Cens de la poblacio de coloms i altres aus urbanes a Barcelona 2015. Museu de Ciencies Naturals de Barcelona. Agencia de Salut Publica de Barcelona Editions, BarcelonaGoogle Scholar
  59. Postigo JL, Shwartz A, Strubbe D, Muñoz AR (2017) Unrelenting spread of the alien monk parakeet Myiopsitta monachus in Israel. Is it time to sound the alarm? Pest Manag Sci 73:349–353CrossRefGoogle Scholar
  60. Prenter J, MacNeil C, Dick JT, Dunn AM (2004) Roles of parasites in animal invasions. Trends Ecol Evol 19:385–390CrossRefGoogle Scholar
  61. Price PW, Westoby M, Rice B, Atsatt PR, Fritz RS, Thompson JN, Mobley K (1986) Parasite mediation in ecological interactions. Annu Rev Ecol Syst 17:487–505CrossRefGoogle Scholar
  62. Reed JE, McCleery RA, Silvy NJ, Smeins FE, Brightsmith DJ (2014) Monk parakeet nest site selection of electric utility structures in Texas. Landsc Urb Plann 129:65–72CrossRefGoogle Scholar
  63. Rodríguez-Pastor R, Senar JC, Ortega A, Faus J, Uribe F, Montalvo T (2012) Distribution patterns of invasive Monk parakeets (Myiopsitta monachus) in an urban habitat. Anim Biodiv Cons 35:107–117Google Scholar
  64. Romeo C, Wauters LA, Ferrari N, Lanfranchi P, Martinoli A, Pisanu B, Preatoni DG, Saino N (2014) Macroparasite fauna of alien grey squirrels (Sciurus carolinensis): composition, variability and implications for native species. PLoS One 9:e88002CrossRefGoogle Scholar
  65. Rose E, Nagel P, Haag-Wackernagel D (2006a) Spatio-temporal use of the urban habitat by feral pigeons. Behav Ecol Sociobiol 60:242–254CrossRefGoogle Scholar
  66. Rose E, Haag-Wackernagel D, Nagel P (2006b) Practical use of GPS-localization of feral pigeons Columba livia in the urban environment. Ibis 148:231–239CrossRefGoogle Scholar
  67. Santillán MA, Grande JM, Liébana MS, Martínez P, Díaz LA, Bragagnolo LA, Solaro C, Galmes MA, Sarasola JH (2015) New hosts for the mite Ornithonyssus bursa in Argentina. Medical Vet Entomol 29:439–443CrossRefGoogle Scholar
  68. Santos DM (2006) Fichas de aves introducidas en España. Grupo de Aves Exóticas (SEO/BirdLife). [Accessed on 10th July 2014]
  69. Schielzeth H (2010) Simple means to improve the interpretability of regression coefficients. Methods Ecol Evol 1:103–113CrossRefGoogle Scholar
  70. Senar JC, Domènech J, Arroyo L, Torre I, Gordo O (2016) An evaluation of monk parakeet damage to crops in the metropolitan area of Barcelona. Anim Biodivers Conserv 39:141–145Google Scholar
  71. Senar JC, Montalvo T, Pascual J, Arroyo L (2017a) Cotorra de pit gris Myiopsitta monachus. In: Manton M, Herrando S, García D, Ferrer X, Parés M, Cebrian R (eds) Atles dels ocells nidificants de Barcelona. Ajuntament de Barcelona, Barcelona, pp 136–137Google Scholar
  72. Senar JC, Montalvo T, Pascual J, Arroyo L (2017b) Cotorra de Kramer Psittacula krameri. In: Manton M, Herrando S, García D, Ferrer X, Parés M, Cebrian R (eds) Atles dels ocells nidificants de Barcelona. Ajuntament de Barcelona, Barcelona, pp 128–129Google Scholar
  73. Sol D, Santos DM, Feria E, Clavell J (1997) Habitat selection by the monk parakeet during colonization of a new area in Spain. Condor 99:39–46CrossRefGoogle Scholar
  74. Sol D, Gonzàlez-Lagos C, Lapiedra O, Dìaz M (2017) Why are exotic birds so successful in urbanized ecosystems? In: Murgui E, Hedblom M (eds) Ecology and conservation of birds in urban environments. Springer Editions, New York, pp 75–89CrossRefGoogle Scholar
  75. Soldatini C, Mainardi D, Baldaccini NE, Giunchi D (2006) A temporal analysis of the foraging flights of feral pigeons (Columba livia f. domestica). Ital J Zool 73:83–92CrossRefGoogle Scholar
  76. Tschirren B, Bischoff LL, Saladin V, Richner H (2007) Host condition and host immunity affect parasite fitness in a bird-ectoparasite system. Funct Ecol 21:372–378CrossRefGoogle Scholar
  77. Turbè A, Strubbe D, Mori E, Carrete M, Chiron F, Clergeau P, Gonzalez-Moreno P, Le Louarn M, Luna A, Menchetti M, Nentwig W, Parau LG, Postigo JL, Rabitsch W, Senar JC, Tollington S, Vanderhoeven S, Weiserbs A, Shwartz A (2017) Assessing the assessments: evaluation of four impact assessment protocols for invasive alien species. Divers Distrib 23:297–307CrossRefGoogle Scholar
  78. Viviano E, Bongiorno MR (2014) Avian mite dermatitis: an Italian case indicating the establishment and spread of Ornithonyssus bursa (Acari: Gamasida: Macronyssidae) (Berlese, 1888) in Europe. Int J Dermat 54:795–799Google Scholar
  79. Vourc’h G, Abrial D, Bord S, Jacquot M, Masseglia S, Poux V, Pisanu B, Bailly X, Chapuis JL (2016) Mapping human risk of infection with Borrelia burgdoferi sensu lato, the agent of Lyme borreliosis, in a periurban forests in France. Ticks Tick-Borne Dis 5:644–652CrossRefGoogle Scholar
  80. Weiserbs A, Jacob JP (1999) Etude de la population de perriche jeune-veuve Myiopsitta monachus à Bruxelles. Aves 36:207–223Google Scholar
  81. Zocchi A, Battisti C, Santoro R (2009) Note sul pappagallo monaco, Myiopsitta monachus, a Roma (Villa Pamphili). Riv Ital Ornitol 78:135–137Google Scholar
  82. Zuur AF, Ieno EN, Walker NJ, Saveliev AA, Smith GM (2009) Mixed effects models and extensions in ecology with R. Springer, New YorkCrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Dipartimento di Scienze della VitaUniversità degli Studi di SienaSienaItaly
  2. 2.Agència de Salut Pública de BarcelonaBarcelonaSpain
  3. 3.Institut de Biologia Evolutiva (CSIC-Universitat Pompeu Fabra)BarcelonaSpain
  4. 4.Dipartimento di BiologiaUniversità degli Studi di FirenzeFlorenceItaly
  5. 5.Servei de Vigilància i Control de Plagues Urbanes, Agència de Salut Pública de BarcelonaBarcelonaSpain
  6. 6.CIBER Epidemiology and Public Health, Public Salud Agency of BarcelonaBarcelonaSpain
  7. 7.Museu de Ciències Naturals de BarcelonaBarcelonaSpain

Personalised recommendations