Next Article in Journal
Plant Invasion Has Limited Impact on Soil Microbial α-Diversity: A Meta-Analysis
Previous Article in Journal
Simultaneous Metabarcoding of Eukaryotes and Prokaryotes to Elucidate the Community Structures within Tardigrade Microhabitats
 
 
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Article

Do Invasive Mosquito and Bird Species Alter Avian Malaria Parasite Transmission?

1
Estación Biológica de Doñana (EBD-CSIC). Av. Américo Vespucio 26, E-41092 Sevilla, Spain
2
CIBER Epidemiología y Salud Pública (CIBERESP), 28029 Madrid, Spain
3
Agencia de Salud Pública de Barcelona. Consorci Sanitari de Barcelona. Pl. Lesseps, 1, E-08023 Barcelona, Spain
4
Departamento de Investigación y Desarrollo (I+D), Laboratorios Lokímica, 46470 Catarroja-València, Spain
5
Evolutionary and Behavioural Ecology Research Unit, Museu de Ciències Naturals de Barcelona, Psg. Picasso s/n., E-08003 Barcelona, Spain
*
Authors to whom correspondence should be addressed.
Diversity 2020, 12(3), 111; https://doi.org/10.3390/d12030111
Received: 4 March 2020 / Revised: 18 March 2020 / Accepted: 19 March 2020 / Published: 20 March 2020
(This article belongs to the Section Animal Diversity)

Abstract

:
Alien mosquito and vertebrate host species may create novel epidemiological scenarios for the transmission of pathogens naturally circulating in the invaded area. The exotic Monk parakeet (Myiopsitta monachus) has established populations in Europe and is currently considered an invasive pest. Due to their high abundance in urban areas, Monk parakeets could be involved in the transmission of pathogens, potentially affecting wildlife and livestock. To test this hypothesis, we determined the prevalence and diversity of three vector-borne parasites, namely Plasmodium, Haemoproteus and Leucocytozoon, in Monk parakeets from Barcelona. Many areas of southern Europe shelter high densities of the invasive Asian tiger mosquito Aedes albopictus, which in addition to native mosquito species could affect the transmission of mosquito-borne parasites, such as avian Plasmodium. Thus, we also sampled mosquitoes in the area to trace their blood-feeding hosts and determine the presence of Plasmodium parasites. Monk parakeets were neither infected by Plasmodium nor by Haemoproteus parasites, and only five individuals (3.13%; n = 160) were infected by Leucocytozoon. Monk parakeets were bitten by Culiseta longiareolata and represented 9.5% of Culex pipiens blood meals. The invasive Ae. albopictus showed a clear anthropophilic feeding pattern, with humans dominating its diet. Three Plasmodium lineages were detected in pools of Cx pipiens. These results suggest that Plasmodium circulating in the area cannot develop in the invasive Monk parakeet, in spite of the relatively high fraction of native mosquito vectors feeding on this species in its invaded distribution range.

1. Introduction

Pathogens are an important factor explaining the invasion success of alien species [1]. The Enemy Release Hypothesis proposes that invasive species proliferate in invaded areas because they lose their original parasites present in their native distribution range [2]. In addition to this possibility, the Novel Weapons Hypothesis proposes that invasive species may harbor new pathogens to the immunological naive native populations [3]. However, locally circulating pathogens may also be able to infect alien hosts [4], although the transmission of pathogens with complex life cycles may be limited by the occurrence of competent hosts allowing its successful transmission [1]. This may be the case for vector-borne pathogens that require the coexistence of competent vertebrate hosts and insect vectors to be effectively transmitted from an infected individual to a susceptible host. Thus, different factors may explain the absence of infections by vector-borne pathogens in alien species in the invaded areas including those affecting the transmission routes of pathogens, such as 1) the absence of competent vectors for the transmission of pathogens and 2) limited contact rates between vectors and susceptible vertebrate hosts.
Avian malaria parasites of the genus Plasmodium are commonly found to infect birds and are transmitted by mosquitoes [5,6]. The life cycle of these parasites includes asexual reproduction stages in the vertebrate hosts and a sexual phase in the mosquito vector. To be transmitted, the parasite requires the bite of a competent mosquito on an infected bird. In addition to Plasmodium, birds usually suffer infection by the related Haemoproteus and Leucocytozoon parasites. These two parasite genera have a similar life cycle to Plasmodium but are transmitted by different vectors [5]. Culicoides and louse flies are the main vectors of Haemoproteus of the subgenera Parahaemoproteus and Haemoproteus, respectively, while Leucocytozoon are transmitted by blackflies [6]. Avian haemosporidians have been used as study models to assess the role of parasites on the invasive success of different alien species including house sparrows (Passer domesticus) [7,8] and mynas (Acridotheres tristis) [9]. However, the role of insect vectors to explain the epidemiology of these pathogens affecting invasive avian species has traditionally been neglected.
Mosquitoes represent an important public health concern as sources of nuisance due to their bites to humans and as vectors of pathogens [10]. As in the case of other hematophagous insects, mosquitoes show a certain degree of feeding preference, with some species feeding mainly on a particular group of vertebrates, such as birds or mammals, while other species show opportunistic behaviors [11,12]. The common house mosquito Culex pipiens frequently occurs in European urban areas where it may play a central role in the transmission of avian malaria parasites [13,14,15,16]. During the last decades, the invasive Asian tiger mosquito Aedes albopictus has dramatically increased its distribution range from the native area in Asia to other continents [16]. This species is currently present in most countries of the Mediterranean basin, reaching high abundances in densely populated areas and producing important nuisances to humans and a risk to public health [17]. As well as humans, other mammals and occasionally birds are bitten by Ae. albopictus which could potentially affect the transmission of mosquito-borne pathogens in the invaded area [12,18].
Urban ecosystems are considered hotspots of biological invasions where alien species could represent an important public health concern and animal health concern for pets and other animals. In particular, Monk parakeets Myiopsitta monachus are considered one of the most effective parrot species colonizing new territories [19]. In addition to their native range in South America, this species is currently present in areas from North America and Europe, including islands in the Atlantic Ocean (e.g., Canary Islands) [20,21]. The Monk parakeet is listed as an invasive species according to both Spanish and European regulations [22] and its abundance is quickly increasing [21,23]. In the invaded areas, Monk parakeets produce economic costs due to the damage to human infrastructures and agriculture [24,25]. Moreover, as is the case for other parrot species, Monk parakeets may be involved in the transmission of pathogens and parasites, causing diseases in humans and other animals [19,26,27].
Here, we assessed the prevalence of the avian malaria parasite Plasmodium and the related Haemoproteus and Leucocytozoon in Monk parakeets from the city of Barcelona, where the presence of the species was first described in the 1970s [28], and its abundance has dramatically increased during the last decades [21,29]. In addition, we screened the blood meal sources of mosquitoes and identified the Plasmodium parasites potentially transmitted by both native and invasive mosquitoes in the area [30,31].

2. Materials and Methods

Monk parakeets were sampled in ten sampling sites covering six of the ten districts of Barcelona, focusing on the districts with a higher density of birds (see [27]). Adult plumaged Monk parakeets were captured from 2014 to 2015 using a special Yunick Platform Trap placed at the Natural History Museum of Barcelona (Ciutadella Park) and using pre-baited clap nets at the other localities (see [32] for details of the trapping procedures). Birds were individually marked with metal rings. We obtained blood samples from a total of 160 birds to determine infection status by hemosporidian parasites. Birds were handled and blood samples taken with special permission EPI 7/2015 (01529/1498/2015) from Direcció General del Medi Natural i Biodiversitat, Generalitat de Catalunya, following Catalan regional ethical guidelines for the handling of birds. J.C.S. received special authorization (001501-0402.2009) for the handling of animals in research from Servei de Protecció de la Fauna, Flora i Animal de Companyia, according to Decree 214/1997/30.07, Generalitat de Catalunya.
Mosquitoes were collected in Barcelona city (Ciutat Vella), which included the Zoological garden. Mosquitoes were captured weekly from April to November during 2014 and 2015. Adults were captured using BG Sentinel traps (Biogents GmbH, Regensburg, Germany) supplemented with BG-Lure (BioGents GmbH, Regensburg, Germany) and CO2 as attractants. In addition, to increase the number of blood fed mosquitoes captured, we used entomological aspirators (Improved Prokopack Aspirator, Mod. 1419, John W. Hock Company, Gainesville, FL, USA and CDC Backpack Aspirator Mod. 2846, BioQuip, Los Angeles, CA, USA), sampling mosquitoes in sinks or other resting areas. Mosquitoes were identified to species level following the procedure in [33]. The whole bodies of unfed female mosquitoes were grouped in pools containing 1–30 individuals according to the species, date of capture and sampling site. Engorged female mosquitoes were stored individually at −80 °C until further molecular analyses.
DNA was isolated from bird blood samples, the abdomen of engorged mosquitoes and from mosquito pools using a semi-automatic kit (Maxwell®16 LEV system Research; Promega, Madison, WI USA), following manufacturer specifications. Bird samples were tested for the presence of Plasmodium, Haemoproteus and Leucocytozoon parasites by the amplification of a fragment of the parasite mitochondrial cytochrome b (cyt b) gene [34]. For the case of mosquitoes, we only tested samples for the presence of Plasmodium/Haemoproteus DNA, as mosquitoes transmit only Plasmodium parasites. We amplified a fragment of the mitochondrial cytochrome oxidase 1 (COI) gene of the vertebrate hosts from the abdomen of engorged mosquitoes [35].
Positive amplifications were sequenced using the Big Dye 1.1 technology (PE Applied Biosystems, Foster City, CA, USA) in the facilities of the Estación Biológica de Doñana (Seville, Spain) or in the Macrogen Inc. sequencing service (The Netherlands). Labelled DNA fragments of positive PCR products were resolved using the same forward and reverse primers used in the nested-PCR amplification for the case of blood parasite identifications. For blood meal identifications, amplicons were sequenced in one direction using the primer BCRV2, (Isogen Life Science, De Meern, the Netherlands) except for the case of Ae. albopictus blood meals that were sequenced using the primer BCVINT-RV (Isogen Life Science, De Meern, the Netherlands) (see [30]). Sequences were edited using the software Sequencher™ v 4.9 (Gene Codes Corp., © 2020–2009, Ann Arbor, MI, USA) and assigned to particular vertebrate species by blast comparison with sequences deposited in GenBank DNA sequence database (National Center for Biotechnology Information Blast) or the Barcode of Life Data Systems (BOLD). Parasite lineages were identified by comparison with those sequences deposited in GenBank database. Plasmodium prevalence was assessed from pool data using EpiTools [36], which estimates parasite prevalence derived from pooled samples considering the number of mosquitoes in each pool.

3. Results

3.1. Blood Parasite Prevalence in Birds

Five out of the 160 (3.13%) Monk parakeets tested were infected by Leucocytozoon parasites corresponding to the lineage CIAE2 (100% overlap). None of the birds captured were infected by Plasmodium or Haemoproteus parasites.

3.2. Blood Feeding Patterns of Mosquitoes

The origin of blood meals was successfully identified from 295 out of 511 mosquitoes tested. Positive results were obtained for 263 Cx. pipiens, 20 Ae. albopictus, three Culiseta longiareolata and nine mosquitoes which were identified to the genus level (including eight Culex sp. and one Aedes sp.) (Table 1). Culex pipiens fed blood on both mammals (19.4%) and birds (80.6%), with 25 out of the 263 (9.5%) blood meals identified corresponding to Monk parakeets (Table 1). In addition to Cx. pipiens, a single Cs. longiareolata fed on this invasive species. In total, 18 out of 20 Ae. albopictus blood meals derived from humans.

3.3. Blood Parasite Prevalence in Mosquitoes

The presence of blood parasites was screened in 1808 mosquitoes grouped in 308 pools (Table 2). Plasmodium parasites were only detected in four pools of Cx. pipiens. Three infected pools were trapped in 2014 (2014 prevalence for Cx. pipiens: 0.004; 95% interval: 0.001–0.010) corresponding to the lineages Delurb04 (two pools) and Delurb05 (one pool). During 2015, the Plasmodium relictum lineage SGS1 was identified from a single Cx. pipiens pool (2015 prevalence for Cx. pipiens: 0.003; 95% interval: 0.0001–0.011).

4. Discussion

We tested the role of the invasive Monk parakeet in the transmission of avian hemosporidians in an area with the presence of both native and invasive potential vectors. Monk parakeets showed an apparent absence of blood parasites of the genera Plasmodium and Haemoproteus and a very low (3.13%) prevalence of infection by Leucocytozoon. Parasites may be an important factor affecting the success of establishment of alien species in new areas, with those species escaping from the attack of their parasites from their native distribution range being favored [37]. Avian hemosporidians produce deleterious effects on birds, compromising the life expectance and reproductive success of infected individuals [38,39,40], including parrots maintained in captivity [41]. In addition, immunological responses to parasites are costly for birds [42]; thus, invasive species may benefit from avoiding the interactions with parasites in the invaded area [4].
Among the different hypotheses proposed to explain the infection pattern of alien species in the invaded distribution range, the Enemy Release Hypothesis has received strong support [7,43]. Our results agree with this hypothesis, since the invasive population of Monk parakeets showed a very low prevalence of infection by a single parasite lineage. Similarly, invasive house sparrow populations had a lower prevalence and parasite diversity than native populations [7]. The host range may differ between parasite genera [44,45], but also clear differences between parasite lineages within each parasite genera may occur, with some lineages only developing in a restricted host range while others are able to develop in a huge number of species [46]. The phylogenetic relatedness of the avian community in the invaded area with the introduced species may determine parasite pressure on the alien species [47]. This fact may benefit parrots introduced in Europe, due to the absence of related species in the native bird community. The only parasite lineage identified from Monk parakeets was the generalist Leucocytozoon lineage CIAE2, which circulates between bird species of different orders in Europe, Africa and Asia (see records in Malavi database [48]). Three Larus species are hosts of this parasite lineage. Gulls could play a role in the transmission of this parasite in the metropolitan area of Barcelona due to their relative high density (2 ind/km2; see [49,50]). In addition, different species of the order Falconiformes are hosts of CIAE2, including records in Spain, potentially playing a role in the transmission of the parasites to Monk parakeets. Further studies are necessary to identify the main reservoirs of this parasite lineage in the area and to assess the ability of hemosporidians circulating in the area to develop in Monk parakeets.
Alternatively, it is also possible that Monk parakeets are refractory to infections by Plasmodium and Haemoproteus parasites in both native and introduced areas. Although the ability of Leucocytozoon parasites to infect Monk parakeets was previously reported [51] (see also [52] for records in other parakeet species from South America), to our knowledge, there are no previous records of infections by Plasmodium and Haemoproteus parasites in this species. Some bird groups show a very low prevalence or total absence of hemosporidian infections [53], with parrots representing one of these groups [52,54]. In fact, a very low prevalence of blood parasites was found in species of American Psittacidae with only 36 individuals infected out of the 1199 tested [55]. Furthermore, a single Haemoproteus species has been described in South American parrots [56]. However, parrots maintained in captivity are susceptible to infection by European parasite lineages, which produce high mortality rates in the infected individuals [41]. This suggests the possibility that the absence of Haemoproteus and Plasmodium infections in Monk parakeets could also be due to an extremely high mortality rate of infected individuals (see [56]). Nevertheless, this possibility remains unlikely due to the absence of reports of massive mortalities of Monk parakeets in the study area.
A priori, the absence of competent insect vectors in the area or their inability to bite Monk parakeets could also explain the absence of Plasmodium infections. However, invasive populations of Monk parakeets are affected by different arthropod ectoparasites in the invaded areas [27,57,58], including blood-sucking mosquitoes [30]. Monk parakeets are hosts of mosquitoes including Cs. longierolata and Cx. pipiens, representing 9.5% of the Cx. pipiens blood meals in this study. Both mosquito species are potential vectors of avian malaria parasites, with the last species considered a well-known competent mosquito for the transmission of avian Plasmodium [6,14].

5. Conclusions

Monk parakeets from Barcelona show a low prevalence of infection by blood parasites. The inability of locally circulating Plasmodium parasites to develop in Monk parakeets represents the most plausible reason for the absence of infections in this invasive species. This was not the case of Leucocytozoon parasites, which infected 3.13% of the Monk parakeets tested. Therefore, differences in the specificity/generalist characteristics of each host–parasite assemblage may determine the success of parasite development in alien species in the area. The invasion success of a species is likely affected by different factors including the suitability of urban habitats and the lack of predators in urban areas. Our results suggest that the low prevalence of infection by blood parasites found in Monk parakeets may add to all these factors, facilitating the spread of this species worldwide.

Author Contributions

J.M.-d.l.P., T.M., J.C.S., J.F. designed the study with considerable assistance from R.C.S. and R.B.-M.; T.M., R.B.-M. and J.C.S. collected the samples. J.M.-d.l.P., A.D.-F., Q.P. performed all molecular analyses. J.M.-d.l.P., A.D.-F., J.F. analysed the data. J.M.-d.l.P. wrote the manuscript with substantial contribution from all authors. All authors have read and agreed to the published version of the manuscript.

Funding

This study was funded by projects CGL2012-30759, CGL2012-38262, CGL2015-65055-P and CGL-2016-79568-C3-3-P from the Spanish Ministry of Science and Innovation. A.D.-F. was supported by Severo-Ochoa grant from the Spanish Ministry of Economy and Competitiveness (SVP-2014-068571). With the support of the Fundación Barcelona Zoo and Barcelona City Council.

Acknowledgments

We thank Isabel Martín and Laura Gómez for their help in the laboratory, and Lluïsa Arroyo, Alba Ortega-Segalerva and Helena Navalpotro for their help in the field-trapping of parakeets and mosquitoes. Lokimica contributed assistant workers and logistic support; in particular, Juan López and Cristina Sesé. We also wish to acknowledge the support provided by COST European Cooperation in Science and Technology Actions “ParrotNet” and “AedesCOST” 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 which might be made of the information contained herein. Three anonymous reviewers provided constructive comments on a previous version of this manuscript.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Prenter, J.; MacNeil, C.; Dick, J.T.A.; Dunn, A.M. Roles of parasites in animal invasions. Trends Ecol. Evol. 2004, 19, 385–390. [Google Scholar] [CrossRef] [PubMed]
  2. Torchin, M.E.; Lafferty, K.D.; Dobson, A.P.; McKenzie, V.J.; Kuris, A.M. Introduced species and their missing parasites. Nature 2003, 421, 628–630. [Google Scholar] [CrossRef] [PubMed]
  3. Callaway, R.M.; Ridenour, W.M. Novel weapons: A biochemically based hypothesis for invasive success and the evolution of increased competitive ability. Front. Ecol. Environ. 2004, 2, 436–443. [Google Scholar] [CrossRef]
  4. Young, H.S.; Parker, I.M.; Gilbert, G.S.; Guerra, A.S.; Nunn, C.L. Introduced species, disease ecology, and biodiversity–disease relationships. Trends Ecol. Evol. 2017, 32, 41–54. [Google Scholar] [CrossRef]
  5. Valkiūnas, G. Avian Malaria Parasites and other Haemosporidia; CRC Press: Boca Raton, FL, USA, 2005; p. 932. [Google Scholar]
  6. Santiago-Alarcon, D.; Palinauskas, V.; Schaefer, H.M. Diptera vectors of avian Haemosporidian parasites: untangling parasite life cycles and their taxonomy. Biol. Rev. Camb. Philos. Soc. 2012, 87, 928–964. [Google Scholar] [CrossRef]
  7. Marzal, A.; Ricklefs, R.E.; Valkiūnas, G.; Albayrak, T.; Arriero, E.; Bonneaud, C.; Czirják, G.A.; Ewen, J.; Hellgren, O.; Hořáková, D.; et al. Diversity, loss, and gain of malaria parasites in a globally invasive bird. PLoS ONE 2011, 6, e21905. [Google Scholar] [CrossRef][Green Version]
  8. Santiago-Alarcon, D.; Carbó-Ramírez, P.; Macgregor-Fors, I.; Chávez-Zichinelli, C.A.; Yeh, P.J. The prevalence of avian haemosporidian parasites in an invasive bird is lower in urban than in non-urban environments. Ibis 2020, 162, 201–214. [Google Scholar] [CrossRef]
  9. Clark, N.J.; Olsson-Pons, S.; Ishtiaq, F.; Clegg, S.M. Specialist enemies, generalist weapons and the potential spread of exotic pathogens: malaria parasites in a highly invasive bird. Int J Parasitol 2015, 45, 891–899. [Google Scholar] [CrossRef][Green Version]
  10. Lehane, M.J. The Biology of Blood-Sucking in Insects, 2nd ed.; Cambridge University Press: Cambridge, UK, 2005; p. 321. [Google Scholar]
  11. Tempelis, C.H. Host-feeding patterns of mosquitoes, with a review of advances in analysis of blood meals by serology. J. Med. Entomol. 1975, 11, 635–653. [Google Scholar] [CrossRef]
  12. Martínez-de la Puente, J.; Muñoz, J.; Capelli, G.; Montarsi, F.; Soriguer, R.; Arnoldi, D.; Rizzoli, A.; Figuerola, J. Avian malaria parasites in the last supper: identifying encounters between parasites and the invasive Asian mosquito tiger and native mosquito species in Italy. Malar. J. 2015, 14, 32. [Google Scholar] [CrossRef][Green Version]
  13. Farajollahi, A.; Fonseca, D.M.; Kramer, L.D.; Kilpatrick, A.M. “Bird biting” mosquitoes and human disease: A review of the role of Culex pipiens complex mosquitoes in epidemiology. Infect. Genet. Evol. 2011, 11, 1577–1585. [Google Scholar] [CrossRef] [PubMed][Green Version]
  14. Gutiérrez-López, R.; Martínez-de la Puente, J.; Gangoso, L.; Yan, J.; Soriguer, R.C.; Figuerola, J. Do mosquitoes transmit the avian malaria-like parasite Haemoproteus? An experimental test of vector competence using mosquito saliva. Parasit. Vectors 2016, 9, 609. [Google Scholar] [CrossRef] [PubMed][Green Version]
  15. Martínez-de la Puente, J.; Ferraguti, M.; Ruiz, S.; Roiz, D.; Soriguer, R.; Figuerola, J. Culex pipiens forms and urbanization: Effects on blood feeding sources and transmission of avian Plasmodium. Malar. J. 2016, 15, 589. [Google Scholar] [CrossRef] [PubMed][Green Version]
  16. Kraemer, M.U.; Sinka, M.E.; Duda, K.A.; Mylne, A.Q.; Shearer, F.M.; Barker, C.M.; Moore, C.G.; Carvalho, R.G.; Coelho, G.E.; van Bortel, W.; et al. The global distribution of the arbovirus vectors Aedes aegypti and Ae. albopictus. Elife 2015, 4, e08347. [Google Scholar] [CrossRef] [PubMed]
  17. Medlock, J.M.; Hansford, K.M.; Schaffner, F.; Versteirt, V.; Hendrickx, G.; Zeller, H.; Van Bortel, W. Review of the invasive mosquitoes in Europe: Ecology, public health risks, and control options. Vector Borne Zoonotic Dis. 2012, 12, 435–447. [Google Scholar] [CrossRef][Green Version]
  18. Valerio, L.; Marini, F.; Bongiorno, G.; Facchinelli, L.; Pombi, M.; Caputo, B.; Maroli, M.; Della Torre, A. Host-feeding patterns of Aedes albopictus (Diptera: Culicidae) in urban and rural contexts within Rome province, Italy. Vector Borne Zoonotic Dis. 2010, 10, 291–294. [Google Scholar] [CrossRef]
  19. Menchetti, M.; Mori, E. Worldwide impact of alien parrots (Aves Psittaciformes) on native biodiversity and environment: a review. Ethol. Ecol. Evol. 2014, 26, 172–194. [Google Scholar] [CrossRef]
  20. Lever, C. Naturalised Birds of the World; T & AD Poyser: London, UK, 2005; p. 352. [Google Scholar]
  21. Postigo, J.L.; Strubbe, D.; Mori, E.; Ancillotto, L.; Carneiro, I.; Latsoudis, P.; Menchetti, M.; Pârâu, L.G.; Parrott, D.; Reino, L.; et al. Mediterranean versus Atlantic monk parakeets Myiopsitta monachus: Towards differentiated management at the European scale. Pest Manag. Sci. 2019, 75, 915–922. [Google Scholar] [CrossRef]
  22. del Estado, B.O. Real Decreto 630/2013, de 2 de agosto, por el que se regula el Catálogo español de especies exóticas invasoras. BOE 2013, 185, 56764–56786. [Google Scholar]
  23. Molina, B.; Postigo, J.L.; Román-Muñoz, A.; del Moral, J.C. La cotorra argentina en España: Población reproductora en 2015 y método de censo; SEO/BirdLife: Madrid, Spain, 2016; p. 95. [Google Scholar]
  24. Averis, M.L.; Greiner, E.C.; Lindsay, J.R.; Newman, J.R.; Pruett-Jones, S. Monk parakeet management at electric utility facilities in South Florida. In Proceedings of the Vertebrate Pest Conference; Timm, R.M., Schmidt, R.H., Eds.; University of California: Davis, CA, USA, 2002; pp. 140–145. [Google Scholar]
  25. Senar, J.C.; Domènech, J.; Arroyo, L.; Torre, I.; Gordo, O. An evaluation of monk parakeet damage to crops in the metropolitan area of Barcelona. Anim. Biodivers. Conserv. 2016, 39, 141–145. [Google Scholar] [CrossRef]
  26. Raso, T.F.; Ferreira, V.L.; Timm, L.N.; Abreu, M.D.F.T. Psittacosis domiciliary outbreak associated with monk parakeets (Myiopsitta monachus) in Brazil: need for surveillance and control. J.M.M. Case. Rep. 2014, 1, 1–4. [Google Scholar] [CrossRef][Green Version]
  27. Mori, E.; Pascual, J.; Fattorini, N.; Menchetti, M.; Montalvo, T.; Senar, J.C. Ectoparasite sharing among native and invasive birds in a metropolitan area. Parasitol. Res. 2019, 118, 399–409. [Google Scholar] [CrossRef] [PubMed]
  28. Batllori, X.; Nos, R. Presencia de la Cotorrita Gris (Myiopsitta monachus) y de la Cotorrita de Collar (Psittacula krameri) en el area metropolitana de Barcelona. Misc. Zool. 1985, 9, 407–411. [Google Scholar]
  29. Rodríguez–Pastor, R.; Senar, J.C.; Ortega, A.; Faus, J.; Uribe, F.; Montalvo, T. Distribution patterns of invasive Monk parakeets (Myiopsitta monachus) in an urban habitat. Anim. Biodivers. Conserv. 2012, 35, 107–117. [Google Scholar]
  30. Muñoz, J.; Eritja, R.; Alcaide, M.; Montalvo, T.; Soriguer, R.C.; Figuerola, J. Host-feeding patterns of native Culex pipiens and invasive Aedes albopictus mosquitoes (Diptera: Culicidae) in urban zones from Barcelona, Spain. J Med Entomol 2011, 48, 956–960. [Google Scholar] [CrossRef] [PubMed]
  31. Laynez-Roldán, P.; Martínez-de la Puente, J.; Montalvo, T. Mas, J.; Muñoz, J.; Figuerola, J.; Rodríguez-Valero, N. Two cases of subcutaneous dirofilariasis in Barcelona, Spain. Parasitol. Res. 2018, 117, 3679–3681. [Google Scholar] [CrossRef] [PubMed][Green Version]
  32. Senar, J.C.; Conroy, M.J.; Montalvo, T. Population dynamics and decision-making models of the Monk parakeet inform alternative management scenarios. In Naturalized Parrots of the World; Pruett-Jones, S., Ed.; Princeton University Press: Princeton, NJ, USA, 2020. [Google Scholar]
  33. Schaffner, E.; Angel, G.; Geoffroy, B.; Hervy, J.P.; Rhaiem, A.; Brunhes, J. The Mosquitoes of Europe: An Identification and Training Programme (CD-ROM); IRD Editions: Montpellier, France, 2001. [Google Scholar]
  34. Hellgren, O.; Waldenstrom, J.; Bensch, S. A new PCR assay for simultaneous studies of Leucocytozoon, Plasmodium and Haemoproteus from avian blood. J. Parasitol. 2004, 90, 797–802. [Google Scholar] [CrossRef] [PubMed]
  35. Alcaide, M.; Rico, C.; Ruiz, S.; Soriguer, R.; Muñoz, J.; Figuerola, J. Disentangling vector-borne transmission networks: a universal DNA barcoding method to identify vertebrate hosts from arthropod bloodmeals. PLoS ONE 2009, 4, e7092. [Google Scholar] [CrossRef][Green Version]
  36. Epitools. Available online: http://epitools.ausvet.com.au/content.php?page=home (accessed on 10 January 2020).
  37. Lockwood, J.L.; Hoopes, M.F.; Marchetti, M.P. Invasion Ecology; Blackwell publishing: Oxford, UK, 2007; p. 304. [Google Scholar]
  38. Asghar, M.; Hasselquist, D.; Hansson, B.; Zehtindjiev, P.; Westerdahl, H.; Bensch, S. Hidden costs of infection: Chronic malaria accelerates telomere degradation and senescence in wild birds. Science 2015, 347, 436–438. [Google Scholar] [CrossRef]
  39. Martínez-de la Puente, J.; Merino, S.; Tomás, G.; Moreno, J.; Morales, J.; Lobato, E.; García-Fraile, S.; Belda, E.J. The blood parasite Haemoproteus reduces survival in a wild bird: a medication experiment. Biol. Lett. 2010, 6, 663–665. [Google Scholar] [CrossRef][Green Version]
  40. Merino, S.; Moreno, J.; Sanz, J.J.; Arriero, E. Are avian blood parasites pathogenic in the wild? A medication experiment in blue tits (Parus caeruleus). Proc. Biol. Sci. 2000, 267, 2507–2510. [Google Scholar] [CrossRef][Green Version]
  41. Olias, P.; Wegelin, M.; Zenker, W.; Freter, S.; Gruber, A.D.; Klopfleisch, R. Avian malaria deaths in parrots, Europe. Emerg. Infect. Dis. 2011, 17, 950–952. [Google Scholar] [CrossRef]
  42. Tomás, G.; Merino, S.; Moreno, J.; Morales, J.; Martínez-de la Puente, J. Impact of blood parasites on immunoglobulin level and parental effort: A medication field experiment on a wild passerine. Funct. Ecol. 2007, 21, 125–133. [Google Scholar] [CrossRef]
  43. Blakeslee, M.H.; Fowler, A.E.; Keogh, C.L. Marine invasions and parasite escape: Updates and new perspectives Adv. Mar. Biol. 2013, 66, 87–169. [Google Scholar]
  44. Beadell, J.S.; Gering, E.; Austin, J.; Dumbacher, J.P.; Peirce, M.A.; Pratt, T.K.; Atkinson, C.T.; Fleischer, R.C. Prevalence and differential host-specificity of two avian blood parasite genera in the Australo-Papuan region. Mol. Ecol. 2004, 13, 3829–3844. [Google Scholar] [CrossRef]
  45. Reeves, A.B.; Smith, M.M.; Meixell, B.W.; Fleskes, J.P.; Ramey, A.M. Genetic diversity and host specificity varies across three genera of blood parasites in ducks of the Pacific Americas flyway. PLoS ONE 2015, 10, e0116661. [Google Scholar] [CrossRef]
  46. Dimitrov, D.; Palinauskas, V.; Iezhova, T.A.; Bernotienė, R.; Ilgūnas, M.; Bukauskaitė, D.; Zehtindjiev, P.; Ilieva, M.; Shapoval, A.P.; Bolshakov, C.V.; et al. Plasmodium spp.: an experimental study on vertebrate host susceptibility to avian malaria. Exp. Parasitol. 2015, 148, 1–16. [Google Scholar] [CrossRef]
  47. Parker, I.M.; Saunders, M.; Bontrager, M.; Weitz, A.P.; Hendricks, R.; Magarey, R.; Suiter, K.; Gilbert, G.S. Phylogenetic structure and host abundance drive disease pressure in communities. Nature 2015, 520, 542. [Google Scholar] [CrossRef][Green Version]
  48. Malavi Database. Available online: http://130.235.244.92/Malavi/ (accessed on 10 January 2020).
  49. Montalvo, T.; Pascual, J.; Senar, J.C.; Peracho, V. Gavià argentat -Larus michahellis. In Atles dels ocells nidificants de Barcelona; Anton, M., Herrando, S., García, D., Ferrer, X., Parés, M., Cebrian, R., Eds.; Ajuntament de Barcelona: Barcelona, Spain, 2017; pp. 88–89. [Google Scholar]
  50. Sol, D.; Arcos, J.M.; Senar, J.C. The influence of refuse tips on the winter distribution of Yellow-legged Gulls Larus cachinnans. Bird Study 1995, 42, 216–221. [Google Scholar] [CrossRef][Green Version]
  51. Borst, G.H.; Zwart, P. An aberrant form of Leucocytozoon infection in two quaker parakeets (Myiopsitta monachus Boddaert, 1783). Z. Parasitenkd. 1972, 40, 131–138. [Google Scholar] [CrossRef]
  52. Masello, J.F.; Martínez, J.; Calderón, L.; Calderón, L.; Wink, M.; Quillfeldt, P.; Sanz, V.; Theuerkauf, J.; Ortiz-Catedral, L.; Berkunsky, I.; et al. Can the intake of antiparasitic secondary metabolites explain the low prevalence of hemoparasites among wild Psittaciformes? Parasit. Vectors 2018, 11, 357. [Google Scholar] [CrossRef][Green Version]
  53. Martínez-Abraín, A.; Esparza, B.; Oro, D. Lack of blood parasites in bird species: Does absence of blood parasite vectors explain it all? Ardeola 2004, 51, 225–232. [Google Scholar]
  54. Masello, J.F.; Choconi, R.G.; Sehgal, R.N.M.; Tell, L.; Quillfeldt, P. Blood and intestinal parasites in wild Psittaciformes: A case study of Burrowing Parrots (Cyanoliseus patagonus). Ornitol. Neotrop. 2006, 17, 515–530. [Google Scholar]
  55. White, E.M.; Greiner, E.C.; Bennett, G.F.; Herman, C.M. Distribution of the hematozoa of Neotropical birds. Rev. Biol. Trop. 1978, 26, 43–102. [Google Scholar]
  56. Valkiūnas, G.; Pendl, H.; Olias, P. New Haemoproteus parasite of parrots, with remarks on the virulence of haemoproteids in naive avian hosts. Acta Tropica. 2017, 176, 256–262. [Google Scholar] [CrossRef]
  57. Mori, E.; Ancillotto, L.; Groombridge, J.; Howard, T.; Smith, V.S.; Menchetti, M. Macroparasites of introduced parakeets in Italy: a possible role for parasite-mediated competition. Parasitol. Res. 2015, 114, 3277–3281. [Google Scholar] [CrossRef]
  58. Briceño, C.; Surot, D.; González-Acuña, D.; Martínez, F.J.; Fredes, F. Parasitic survey on introduced monk parakeets (Myiopsitta monachus) in Santiago, Chile. Braz. J. Vet Parasitol. 2017, 26, 129–135. [Google Scholar] [CrossRef][Green Version]
Table 1. Vertebrate hosts of mosquitoes from Barcelona.
Table 1. Vertebrate hosts of mosquitoes from Barcelona.
Vertebrate HostsFamilyHost SpeciesAe. albopictusAedes sp.Cx. pipiensCulex sp.Cs. longireolataTotal
MammalCercopithecoidaeErythrocebus patas 6 6
EquidaeEquus caballus 4 4
FelidaeFelis silvestris2 1 3
HominidaeHomo sapiens181371 57
RhinocerotidaeCeratotherium simum 1 1
UrsidaeUrsus arctos 2 2
BirdArdeidaeArdea cinerea 7 7
Bubulcus ibis 191 20
Egretta garzetta 7 7
ColumbidaeColumba livia 352 37
Columba palumbus 2 2
Streptopelia decaocto 151 16
CorvidaeColoeus monedula 13 13
Pica pica 152219
ParidaeCyanistes caeruleus 2 2
Parus major 5 5
PasseridaePasser domesticus 6 6
PhasianidaePavo sp. 4 4
PhoenicopteridaePhoenicopterus sp. 6 6
PsittacidaeMyiopsitta monachus 25 126
SpheniscidaeSpheniscus humboldti 471 48
SturnidaeSturnus vulgaris 2 2
TurdidaeTurdus merula 2 2
Table 2. Blood parasite prevalence found in pools of mosquitoes from Barcelona.
Table 2. Blood parasite prevalence found in pools of mosquitoes from Barcelona.
Mosquito SpeciesMosquitoesPoolsPositive pools
Aedes albopictus473840
Aedes sp.1470
Anopheles claviger110
Culiseta longiareolata109360
Culex sp.1690
Cx. modestus320
Cx. pipiens11901674
Ochlerotatus. berlandi110
Oc. geniculatus110

Share and Cite

MDPI and ACS Style

Martínez-de la Puente, J.; Díez-Fernández, A.; Montalvo, T.; Bueno-Marí, R.; Pangrani, Q.; Soriguer, R.C.; Senar, J.C.; Figuerola, J. Do Invasive Mosquito and Bird Species Alter Avian Malaria Parasite Transmission? Diversity 2020, 12, 111. https://doi.org/10.3390/d12030111

AMA Style

Martínez-de la Puente J, Díez-Fernández A, Montalvo T, Bueno-Marí R, Pangrani Q, Soriguer RC, Senar JC, Figuerola J. Do Invasive Mosquito and Bird Species Alter Avian Malaria Parasite Transmission? Diversity. 2020; 12(3):111. https://doi.org/10.3390/d12030111

Chicago/Turabian Style

Martínez-de la Puente, Josué, Alazne Díez-Fernández, Tomás Montalvo, Rubén Bueno-Marí, Quentin Pangrani, Ramón C. Soriguer, Juan Carlos Senar, and Jordi Figuerola. 2020. "Do Invasive Mosquito and Bird Species Alter Avian Malaria Parasite Transmission?" Diversity 12, no. 3: 111. https://doi.org/10.3390/d12030111

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop