Apparent Lack of Circovirus Transmission from Invasive Parakeets to Native Birds
Abstract
:1. Introduction
2. Materials and Methods
2.1. Fieldwork
2.2. DNA Extraction and Screening of Avian Circovirus
3. Results and Discussion
4. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Vitousek, P.M.; D’Antonio, C.M.; Loope, L.L.; Westbrooks, R. Biological invasions as global environmental change. Am. Sci. 1996, 84, 468–478. [Google Scholar]
- Mack, R.N.; Simberloff, D.; Mark Lonsdale, W.; Evans, H.; Clout, M.; Bazzaz, F.A. Biotic invasions: Causes, epidemiology, global consequences, and control. Ecol. Appl. 2000, 10, 689–710. [Google Scholar] [CrossRef]
- Crowl, T.A.; Crist, T.O.; Parmenter, R.R.; Belovsky, G.; Lugo, A.E. The spread of invasive species and infectious disease as drivers of ecosystem change. Front. Ecol. Environ. 2008, 6, 238–246. [Google Scholar] [CrossRef]
- Martin, L.B.; Hopkins, W.A.; Mydlarz, L.D.; Rohr, J.R. The effects of anthropogenic global changes on immune functions and disease resistance. Ann. N. Y. Acad. Sci. 2010, 1195, 129–148. [Google Scholar] [CrossRef]
- Ortega, N.; Roznik, E.A.; Surbaugh, K.L.; Cano, N.; Price, W.; Campbell, T.; Rohr, J.R. Parasite spillover to native hosts from more tolerant, supershedding invasive hosts: Implications for management. J. Appl. Ecol. 2021, 59, 39–51. [Google Scholar] [CrossRef]
- Mori, E.; Meini, S.; Strubbe, D.; Ancillotto, L.; Sposimo, P.; Menchetti, M. Do alien free-ranging birds affect human health? A global summary of known zoonoses. In Invasive Species and Human Health, 1st ed.; Mazza, G., Tricarcio, E., Eds.; CABI Editions: Wallingford, UK, 2018; pp. 120–129. [Google Scholar]
- Baker, J.; Harvey, K.J.; French, K. Threats from introduced birds to native birds. Emu Austral Ornithol. 2014, 114, 1–12. [Google Scholar] [CrossRef] [Green Version]
- Martin-Albarracin, V.L.; Amico, G.C.; Simberloff, D.; Nuñez, M.A. Impact of Non-Native Birds on Native Ecosystems: A Global Analysis. PLoS ONE 2015, 10, e0143070. [Google Scholar] [CrossRef]
- Kundu, S.; Faulkes, C.G.; Greenwood, A.G.; Jones, C.G.; Kaiser, P.; Lyne, O.D.; Black, S.A.; Chowrimootoo, A.; Groombridge, J.J. Tracking Viral Evolution during a Disease Outbreak: The Rapid and Complete Selective Sweep of a Circovirus in the Endangered Echo Parakeet. J. Virol. 2012, 86, 5221–5229. [Google Scholar] [CrossRef] [Green Version]
- Raidal, S.R.; Peters, A. Psittacine beak and feather disease: Ecology and implications for conservation. Emu Austral Ornithol. 2018, 118, 80–93. [Google Scholar] [CrossRef]
- Fogell, D.J.; Tollington, S.; Tatayah, V.; Henshaw, S.; Naujeer, H.; Jones, C.; Raisin, C.; Greenwood, A.; Groombridge, J.J. Evolution of Beak and Feather Disease Virus across Three Decades of Conservation Intervention for Population Recovery of the Mauritius Parakeet. Diversity 2021, 13, 584. [Google Scholar] [CrossRef]
- Fogell, D.J.; Martin, R.O.; Bunbury, N.; Lawson, B.; Sells, J.; McKeand, A.M.; Tatayah, V.; Trung, C.T.; Groombridge, J.J. Trade and conservation implications of new beak and feather disease virus detection in native and introduced parrots. Conserv. Biol. 2018, 32, 1325–1335. [Google Scholar] [CrossRef] [Green Version]
- Amery-Gale, J.; Marenda, M.; Owens, J.; Eden, P.A.; Browning, G.; Devlin, J. A high prevalence of beak and feather disease virus in non-psittacine Australian birds. J. Med Microbiol. 2017, 66, 1005–1013. [Google Scholar] [CrossRef]
- Blanco, G.; Morinha, F. Genetic signatures of population bottlenecks, relatedness, and inbreeding highlight recent and novel conservation concerns in the Egyptian vulture. PeerJ 2021, 9, e11139. [Google Scholar] [CrossRef]
- Todd, D. Circoviruses: Immunosuppressive threats to avian species: A review. Avian Pathol. 2000, 29, 373–394. [Google Scholar] [CrossRef]
- Preston, C.E.C.; Pruett-Jones, S. The Number and Distribution of Introduced and Naturalized Parrots. Diversity 2021, 13, 412. [Google Scholar] [CrossRef]
- Morinha, F.; Carrete, M.; Tella, J.L.; Blanco, G. High Prevalence of Novel Beak and Feather Disease Virus in Sympatric Invasive Parakeets Introduced to Spain from Asia and South America. Diversity 2020, 12, 192. [Google Scholar] [CrossRef]
- Hernández-Brito, D.; Carrete, M.; Tella, J.L. Annual Censuses and Citizen Science Data Show Rapid Population Increases and Range Expansion of Invasive Rose-Ringed and Monk Parakeets in Seville, Spain. Animals 2022, 12, 677. [Google Scholar] [CrossRef]
- Hernández-Brito, D.; Carrete, M.; Popa-Lisseanu, A.G.; Ibanez, C.; Tella, J.L. Crowding in the City: Losing and Winning Competitors of an Invasive Bird. PLoS ONE 2014, 9, e100593. [Google Scholar] [CrossRef]
- Hernández-Brito, D.; Carrete, M.; Blanco, G.; Romero-Vidal, P.; Senar, J.; Mori, E.; White, T.; Álvaro, L.; Tella, J. The Role of Monk Parakeets as Nest-Site Facilitators in Their Native and Invaded Areas. Biology 2021, 10, 683. [Google Scholar] [CrossRef]
- Pass, D.A.; Perry, R.A. The pathology of psittacine beak and feather disease. Aust. Vet. J. 1984, 61, 69–74. [Google Scholar] [CrossRef]
- Svensson, L. Identification Guide to European Passerines, 4th ed.; Naturhistoriska Riksmuseet: Stockholm, Sweden, 1992; p. 368. [Google Scholar]
- Eastwood, J.R.; Berg, M.L.; Spolding, B.; Buchanan, K.L.; Bennett, A.T.D.; Walder, K. Prevalence of beak and feather disease virus in wild Platycercus elegans: Comparison of three tissue types using a probe-based real-time qPCR test. Aust. J. Zool. 2015, 63, 1–8. [Google Scholar] [CrossRef] [Green Version]
- Griffiths, R.; Double, M.C.; Orr, K.; Dawson, R.J.G. A DNA test to sex most birds. Mol. Ecol. 1998, 7, 1071–1075. [Google Scholar] [CrossRef]
- Ypelaar, I.; Bassami, M.; Wilcox, G.; Raidal, S. A universal polymerase chain reaction for the detection of psittacine beak and feather disease virus. Vet. Microbiol. 1999, 68, 141–148. [Google Scholar] [CrossRef]
- Sarker, S.; Lloyd, C.; Forwood, J.; Raidal, S.R. Forensic genetic evidence of beak and feather disease virus infection in a Powerful Owl, Ninox strenua. Emu Austral Ornithol. 2016, 116, 71–74. [Google Scholar] [CrossRef]
- Sarker, S.; Moylan, K.G.; Ghorashi, S.; Forwood, J.; Peters, A.; Raidal, S.R. Evidence of a deep viral host switch event with beak and feather disease virus infection in rainbow bee-eaters (Merops ornatus). Sci. Rep. 2015, 5, 14511. [Google Scholar] [CrossRef] [Green Version]
- Ritchie, P.A.; Anderson, I.L.; Lambert, D.M. Evidence for specificity of psittacine beak and feather disease viruses among avian hosts. Virology 2003, 306, 109–115. [Google Scholar] [CrossRef]
- Todd, D.; Weston, J.; Ball, N.W.; Borghmans, B.J.; Smyth, J.A.; Gelmini, L.; Lavazza, A. Nucleotide sequence-based identification of a novel circovirus of canaries. Avian Pathol. 2001, 30, 321–325. [Google Scholar] [CrossRef]
- Todd, D.; Weston, J.; Soike, D.; Smyth, J. Genome Sequence Determinations and Analyses of Novel Circoviruses from Goose and Pigeon. Virology 2001, 286, 354–362. [Google Scholar] [CrossRef]
- Todd, D.; Scott, A.N.J.; Fringuelli, E.; Shivraprasad, H.L.; Gavier-Widen, D.; Smyth, J.A. Molecular characterization of novel circoviruses from finch and gull. Avian Pathol. 2007, 36, 75–81. [Google Scholar] [CrossRef] [PubMed]
- Jovani, R.; Tella, J.L. Parasite prevalence and sample size: Misconceptions and solutions. Trends Parasitol. 2006, 22, 214–218. [Google Scholar] [CrossRef]
- Rúa, M.A.; Pollina, E.C.; Power, A.G.; Mitchell, C.E. The role of viruses in biological invasions: Friend or foe? Curr. Opin. Virol. 2011, 1, 68–72. [Google Scholar] [CrossRef] [PubMed]
- Fogell, D.J.; Groombridge, J.J.; Tollington, S.; Canessa, S.; Henshaw, S.; Zuel, N.; Jones, C.G.; Greenwood, A.; Ewen, J.G. Hygiene and biosecurity protocols reduce infection prevalence but do not improve fledging success in an endangered parrot. Sci. Rep. 2019, 9, 4779. [Google Scholar] [CrossRef] [PubMed]
- Hernández-Brito, D.; Tella, J.L.; Blanco, G.; Carrete, M. Nesting innovations allow population growth in an invasive population of rose-ringed parakeets. Curr. Zool. 2021. [Google Scholar] [CrossRef]
- Ritchie, B.W. Circoviridae. Avian Viruses, Function and Control; Wingers Publishing Inc.: Lake Worth, FL, USA, 1995; pp. 223–252. [Google Scholar]
- Sa, R.C.C.; Cunningham, A.A.; Dagleish, M.P.; Wheelhouse, N.; Pocknell, A.; Borel, N.; Peck, H.L.; Lawson, B. Psittacine beak and feather disease in a free-living ring-necked parakeet (Psittacula krameri) in Great Britain. Eur. J. Wildl. Res. 2014, 60, 395–398. [Google Scholar] [CrossRef] [Green Version]
- Hernández-Brito, D.; Blanco, G.; Tella, J.L.; Carrete, M. A protective nesting association with native species counteracts biotic resistance for the spread of an invasive parakeet from urban into rural habitats. Front. Zool. 2020, 17, 1–13. [Google Scholar] [CrossRef]
- Kessler, S.; Heenemann, K.; Krause, T.; Twietmeyer, S.; Fuchs, J.; Lierz, M.; Corman, V.M.; Vahlenkamp, T.M.; Rubbenstroth, D. Monitoring of free-ranging and captive Psittacula populations in Western Europe for avian bornaviruses, circoviruses and polyomaviruses. Avian Pathol. 2019, 49, 119–130. [Google Scholar] [CrossRef]
Order, Family Species | Number of Individuals (% Juveniles) * | Shared with Parakeets | |||||
---|---|---|---|---|---|---|---|
Examined for Disease Symptoms | Tested for Circovirus | Diet | Nesting Habits | Migratory Status | Nesting Sites | Foraging Sites | |
Bucerotiformes, Upupidae | |||||||
Upupa epops | 7 (42.9) | 5 (60.0) | I | hole | migratory | RR, M | M |
Columbiformes, Columbidae | |||||||
Streptopelia decaocto | 17 (47.1) | 5 (60.0) | G | open | sedentary | M | RR, M |
Passeriformes, Laniidae | |||||||
Lanius senator | 3 (33.3) | 1 (0.0) | I | open | migratory | - | RR |
Passeriformes, Corvidae | |||||||
Cyanopica cooki | 1 (0.0) | - | O | open | sedentary | - | RR, M |
Passeriformes, Certhiidae | |||||||
Certhia brachydactyla | 1 (100) | 1 (100) | I | hole | sedentary | - | - |
Passeriformes, Alaudidae | |||||||
Galerida cristata | 1 (0.0) | 1 (0.0) | G, I | open | sedentary | - | M |
Passeriformes, Sturnidae | |||||||
Sturnus unicolor | 13 (26.1) | 8 (37.5) | O | hole | sedentary | RR, M | RR, M |
Passeriformes, Sylviidae | |||||||
Curruca melanocephala | 15 (55.1) | 5 (60.0) | I, F | open | sedentary | - | RR, M |
Sylvia atricapilla | 1 (0.0) | - | I, F | open | sedentary | - | RR, M |
Passeriformes, Muscicapidae | |||||||
Luscinia megarhynchos | 1 (0.0) | - | I | open | migratory | - | - |
Passeriformes, Turdidae | |||||||
Turdus merula | 46 (46.2) | 5 (40.0) | I, F | open | sedentary | - | RR, M |
Passeriformes, Paridae | |||||||
Parus major | 13 (57.1) | 10 (60.0) | I | hole | sedentary | RR | RR, M |
Cyanistes caeruleus | 6 (66.7) | 5 (60.0) | I | hole | sedentary | - | RR, M |
Passeriformes, Passeridae | |||||||
Passer domesticus | 51 (14.6) | 10 (10.0) | G, I | hole | sedentary | RR, M | RR, M |
Passer hispaniolensis | 8 (0.0) | 6 (0.0) | G, I | open | sedentary | M | RR, M |
Passer sp. | 13 (0.0) | - | G, I | open | sedentary | M | RR, M |
Passeriformes, Fringillidae | |||||||
Serinus serinus | 18 (50.0) | 5 (80.0) | G, I | open | sedentary | - | RR, M |
Carduelis carduelis | 22 (63.4) | 7 (85.7) | G, I | open | sedentary | - | RR, M |
Chloris chloris | 53 (47.2) | 5 (60.0) | G, I | open | sedentary | M | RR, M |
Total | 290 (37.1) | 79 (48.1) |
Primer Sequences (5′–3′) | Ta (°C) | Avian Orders with Circovirus Strains Detected | References |
---|---|---|---|
Forward 5′-AACCCTACAGACGGCGAG-3′ Reverse 5′-GTCACAGTCCTCCTTGTACC-3′ | 58 | Psittaciformes, Coraciiformes Strigiformes | [25,26,27] |
Forward 5′-TTAACAACCCTACAGACGGCGA-3′ Reverse 5′-GGCGGAGCATCTCGCAATAAG-3′ | 58 | Psittaciformes | [28] |
Forward 5′-GGGTCCTCCTTGTAGTGGGATC-3′ Reverse 5′-CAGACGCCGTTTCACAACCAATAG-3′ | 58 | Psittaciformes, Passeriformes, Anseriformes, Caprimulgiformes, Coraciiformes, Strigiformes, Pelecaniformes Accipitriformes | [13] |
Forward 5′-TTCACCCTTAAYAAYCCT-3′ Reverse 5′-CCRTSATATCCATCCCACCA-3′ | 52 | Passeriformes, Columbiformes Anseriformes | [29,30] |
Forward 5′-GGAGCTGTTGCCGCCGTGA-3′ Reverse 5′-TACCCATCCCACCAGTCACC-3′ | 55 | Passeriformes Charadriiformes | [31] |
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Blanco, G.; Morinha, F.; Carrete, M.; Tella, J.L. Apparent Lack of Circovirus Transmission from Invasive Parakeets to Native Birds. Int. J. Environ. Res. Public Health 2022, 19, 3196. https://doi.org/10.3390/ijerph19063196
Blanco G, Morinha F, Carrete M, Tella JL. Apparent Lack of Circovirus Transmission from Invasive Parakeets to Native Birds. International Journal of Environmental Research and Public Health. 2022; 19(6):3196. https://doi.org/10.3390/ijerph19063196
Chicago/Turabian StyleBlanco, Guillermo, Francisco Morinha, Martina Carrete, and José L. Tella. 2022. "Apparent Lack of Circovirus Transmission from Invasive Parakeets to Native Birds" International Journal of Environmental Research and Public Health 19, no. 6: 3196. https://doi.org/10.3390/ijerph19063196