First record of Ornithonyssus bursa (Berlese, 1888) (Mesostigmata: Macronyssidae) parasitizing invasive monk parakeets in Santiago, Chile

Primeiro registro de Ornithonyssus bursa (Berlese, 1888) (Mesostigmata: Macronyssidae) parasitando caturritas invasoras em Santiago, Chile.

Cristóbal Briceño Karina Yévenes Matilde Larraechea Alejandra Sandoval-Rodríguez María Carolina Silva-de la Fuente Fernando Fredes Héctor Hidalgo Valeria Alcayaga Pablo Oyarzún-Ruiz Cintia Munita Daniel González-Acuña About the authors

Abstract

Myiopsitta monachus is an invasive psittacine with wide distribution due to the pet trade. Its large communal nests and synanthropic nature contribute to its successful colonization of cities, from where it seems to be expanding in range and numbers. This is relevant with regard to pathogens that invasive species may harbor, especially when host populations thrive. We aimed to identify an abundant mite found in invasive monk parakeet chicks that had been collected in Santiago during 2017 and 2018. Through morphological and molecular identification of the 18S ribosomal RNA gene, we confirmed the presence of Ornithonyssus bursa. This was the first report of this mite in Chile. This mite is common in native and invasive monk parakeet populations and may affect other birds, including domestic fowl. Further, this mite bites people and can be a potential vector of pathogens such as bacteria or viruses. We conclude that this parasite was likely introduced with the parakeet and discuss possible ecological, health and economic consequences of this new potential pest.

Keywords:
Invasive species; monk parakeet; tropical fowl mite; Chile

Resumo

Myiopsitta monachus é um psitacídeo invasor amplamente distribuído devido ao tráfico de animais selvagens. Os grandes ninhos comunitários construídos e sua condição de espécies sinantrópicas contribuem para a colonização bem-sucedida das cidades, onde parece estar expandindo sua distribuição e número de indivíduos. Isso é relevante, quando se trata de patógenos que os invasores podem abrigar, especialmente quando as populações hospedeiras prosperam. O objetivo deste trabalho foi identificar um ácaro abundante, encontrado em filhotes de periquitos-monge introduzidos em Santiago, Chile, coletados durante 2017 e 2018. Por meio da identificação morfológica e molecular do gene do RNA ribossômico 18S, foi confirmada a presença de Ornithonyssus bursa, sendo o primeiro registro para o Chile. Esse ácaro é comum em populações nativas e introduzidas de periquitos-monge e pode afetar outras aves, incluindo aves domésticas. Além disso, esse ácaro pode picar pessoas e pode ser um potencial vetor de patógenos, como bactérias ou vírus. Conclui-se que esse parasita provavelmente foi introduzido com o periquito e foram discutidas as possíveis consequências ecológicas de saúde e econômicas dessa nova praga em potencial.

Palavras-chave:
Espécies invasoras; periquito-monge; ácaro de aves tropicais; Chile

Introduction

Invasive species are considered to be the second largest cause of biodiversity loss globally (Vitousek et al., 1997Vitousek PM, Mooney HA, Lubchenco J, Melillo JM. Human domination of Earth’s ecosystems. Science 1997; 277(5325): 494-499. http://dx.doi.org/10.1126/science.277.5325.494.
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) and the first in biogeographic islands (Vitousek, 1988Vitousek PM. Diversity and biological invasions of oceanic islands. In: Wilson EO, Peter FM, editors. Biodiversity. 14th ed. Washington DC, USA: The National Academies; 1988. p. 181-190.). Central Chile is recognized as a biogeographic subregion, and Santiago province is one of its two biogeographic units (Morrone, 2006Morrone JJ. Biogeographic areas and transition zones of Latin America and the Caribbean Islands based on panbiogeographic and cladistic analyses of the entomofauna. Annu Rev Entomol 2006; 51(1): 467-494. http://dx.doi.org/10.1146/annurev.ento.50.071803.130447. PMid:16332220.
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). These unique habitats are considered to be a valuable global ecoregion (Olson & Dinerstein, 1998Olson DM, Dinerstein E. The global 200: A representation approach to conserving the Earth’s most biologically valuable ecoregions. Conserv Biol 1998; 12(3): 502-515. http://dx.doi.org/10.1046/j.1523-1739.1998.012003502.x.
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). Central Chile is now identified as one of the 25 biodiversity hotspots of highest conservation priority, due its high levels of endemism and high anthropic pressure (Myers et al., 2000Myers N, Mittermeier RA, Mittermeier CG, da Fonseca GAB, Kent J. Biodiversity hotspots for conservation priorities. Nature 2000; 403(6772): 853-858. http://dx.doi.org/10.1038/35002501. PMid:10706275.
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). Nonetheless, threats to Chilean biodiversity are still underestimated (Brooks et al., 2002Brooks TM, Mittermeier RA, Mittermeier CG, da Fonseca GAB, Rylands AB, Konstant WR, et al. Habitat loss and extinction in the hotspots of biodiversity. Conserv Biol 2002; 16(4): 909-923. http://dx.doi.org/10.1046/j.1523-1739.2002.00530.x.
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).

Biological invasions relate to the emergence of diseases (Dunn & Hatcher 2015Dunn AM, Hatcher MJ. Parasites and biological invasions: parallels, interactions, and control. Trends Parasitol 2015; 31(5): 189-199. https://doi.org/10.1016/j.pt.2014.12.003.
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) that have the potential to contribute to wildlife extinctions, particularly when they interact with additional driving factors (Daszak et al., 2000Daszak P, Cunningham AA, Hyatt AD. Emerging infectious diseases of wildlife-- threats to biodiversity and human health. Science 2000; 287(5452): 443-449. http://dx.doi.org/10.1126/science.287.5452.443. PMid:10642539.
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). In this regard, invasive species have been identified as sources of spread of zoonoses. Thus, these species have the potential to affect the health of animals and people (Keesing et al., 2010Keesing F, Belden LK, Daszak P, Dobson A, Harvell CD, Holt RD, et al. Impacts of biodiversity on the emergence and transmission of infectious diseases. Nature 2010; 468(7324): 647-652. http://dx.doi.org/10.1038/nature09575. PMid:21124449.
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). Consequently, invasive parasites are also considered to constitute biological invasions, with a crucial role in species loss (Taraschewski, 2006Taraschewski H. Hosts and parasites as aliens. J Helminthol 2006; 80(2): 99-128. http://dx.doi.org/10.1079/JOH2006364. PMid:16768855.
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).

Monk parakeets are widely distributed as an invasive species as a consequence of the pet trade (Edelaar et al., 2015Edelaar P, Roques S, Hobson EA, Gonçalves da Silva A, Avery ML, Russello MA, et al. 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 2015; 24(9): 2164-2176. http://dx.doi.org/10.1111/mec.13157. PMid:25873354.
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). Currently, alien populations are found in 19 countries (ISSG, 2015Invasive Species Specialist Group – ISSG. Global Invasive Species Database. Myiopsita monachus (monk parakeet) [online]. 2015 [cited 2020 Nov 5]. Available from: http://www.iucngisd.org/gisd/speciesname/myiopsitta+monachus
http://www.iucngisd.org/gisd/speciesname...
). These parakeets are considered to be ecosystem engineers (Briceño et al., 2019Briceño C, Sandoval-Rodríguez A, Yévenes K, Larraechea M, Morgado A, Chappuzeau CV, et al. Interactions between invasive Monk Parakeets (Myiopsitta monachus) and Other Bird Species during Nesting Seasons in Santiago, Chile. Animals (Basel) 2019; 9(11): 923. http://dx.doi.org/10.3390/ani9110923. PMid:31694253.
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) because of their unique ability among psittacids for building large communal nests weighing up to several hundred kilograms (Spreyer & Bucher, 1998Spreyer MF, Bucher EH. Monk parakeet. In: Poole A, Gil F, editors. The birds of North America. Philadelphia, PA, USA: Cornell Lab of Ornithology; 1998. p. 1-23. http://dx.doi.org/10.2173/tbna.322.p.
http://dx.doi.org/10.2173/tbna.322.p...
). These nests are entwined with twigs and branches by a parakeet couple or several family members, to construct chambers that may be aggregated over several seasons, thus enlarging these nests (Spreyer & Bucher, 1998Spreyer MF, Bucher EH. Monk parakeet. In: Poole A, Gil F, editors. The birds of North America. Philadelphia, PA, USA: Cornell Lab of Ornithology; 1998. p. 1-23. http://dx.doi.org/10.2173/tbna.322.p.
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). Monk parakeets use their nests for breeding and roosting year-round (Navarro et al., 1995Navarro JL, Martella MB, Bucher EHS. Effects of laying date, clutch size, and communal nest size on the reproductive success of monk parakeets. Wilson Bull 1995; 107(4): 742-746.) and are considered to be highly philopatric (Martin & Bucher, 1993Martin LF, Bucher EH. Natal dispersal and first breeding age in monk parakeets. Auk 1993; 110(4): 930-933. http://dx.doi.org/10.2307/4088651.
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). This bird species is deemed to be synanthropic (Briceño et al., 2019Briceño C, Sandoval-Rodríguez A, Yévenes K, Larraechea M, Morgado A, Chappuzeau CV, et al. Interactions between invasive Monk Parakeets (Myiopsitta monachus) and Other Bird Species during Nesting Seasons in Santiago, Chile. Animals (Basel) 2019; 9(11): 923. http://dx.doi.org/10.3390/ani9110923. PMid:31694253.
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) and thus is mainly found in urban environments. However, they may also have an important impact in rural areas, as observed in their native distribution in Argentina, where they are considered to produce US$ 1 billion of annual costs associated with crop losses (Iriarte et al., 2005Iriarte JA, Lobos GA, Jaksic FM. Invasive vertebrate species in Chile and their control and monitoring by governmental agencies. Rev Chil Hist Nat 2005; 78(1): 143-154. http://dx.doi.org/10.4067/S0716-078X2005000100010.
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).

In Chile, the invasive population of monk parakeets grew from pets that were released in eastern Santiago during the early 1980s (Iriarte et al., 2005Iriarte JA, Lobos GA, Jaksic FM. Invasive vertebrate species in Chile and their control and monitoring by governmental agencies. Rev Chil Hist Nat 2005; 78(1): 143-154. http://dx.doi.org/10.4067/S0716-078X2005000100010.
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; Briceño et al., 2017Briceño C, Surot D, González-Acuña D, Martínez FJ, Fredes F. Parasitic survey on introduced monk parakeets (Myiopsitta monachus) in Santiago, Chile. Rev Bras Parasitol Vet 2017; 26(2): 129-135. http://dx.doi.org/10.1590/s1984-29612017023. PMid:28746442.
http://dx.doi.org/10.1590/s1984-29612017...
). Official records estimate that at least 15,000 parakeets were imported into Chile, until the species was declared harmful and importation banned. Since then, its major impact has been perceived on fruit and ornamental trees (Iriarte et al., 2005Iriarte JA, Lobos GA, Jaksic FM. Invasive vertebrate species in Chile and their control and monitoring by governmental agencies. Rev Chil Hist Nat 2005; 78(1): 143-154. http://dx.doi.org/10.4067/S0716-078X2005000100010.
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).

Although little is known about monk parakeets’ pathogen load and their role in pathogen transmission (Briceño et al., 2017Briceño C, Surot D, González-Acuña D, Martínez FJ, Fredes F. Parasitic survey on introduced monk parakeets (Myiopsitta monachus) in Santiago, Chile. Rev Bras Parasitol Vet 2017; 26(2): 129-135. http://dx.doi.org/10.1590/s1984-29612017023. PMid:28746442.
http://dx.doi.org/10.1590/s1984-29612017...
), they have been found to harbor ectoparasites in their area of native distribution, and some are specific to these birds. Hence, in Argentina the cimicid bug Psitticimex uritui (Hemiptera: Cimicidae) has been classified as one of the most abundant parasites of monk parakeet nests, even though it only parasitizes this species (Spreyer & Bucher, 1998Spreyer MF, Bucher EH. Monk parakeet. In: Poole A, Gil F, editors. The birds of North America. Philadelphia, PA, USA: Cornell Lab of Ornithology; 1998. p. 1-23. http://dx.doi.org/10.2173/tbna.322.p.
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; Aramburú et al., 2003Aramburú R, Calvo S, Alzugaray ME, Cicchino A. Ectoparasitic load of monk parakeet (Myiopsitta monachus, Psittacidae) nestlings. Ornitol Neotrop 2003; 14(3): 415-418.). The blood-sucking mite Ornithonyssus bursa (Acarina: Macronyssidae) has also been described in parakeets’ nests in Argentina (Aramburú et al., 2002Aramburú R, Cicchino A, Bucher E. Material Vegetal Fresco En Cámaras De Cría De La Cotorra Argentina Myiopsitta monachus (Psittacidae). Ornitol Neotrop 2002; 13(4): 433-436.). Two chewing lice, Heteromenopon macrurum (Phthiraptera: Menopodidae) and Paragoniocotes fulvofasciatum (Phthiraptera: Philopteridae), are permanent parasites of monk parakeets in their area of native distribution (Aramburú et al., 2003Aramburú R, Calvo S, Alzugaray ME, Cicchino A. Ectoparasitic load of monk parakeet (Myiopsitta monachus, Psittacidae) nestlings. Ornitol Neotrop 2003; 14(3): 415-418.). The latter has recently also been found in introduced monk parakeet populations in Chile and Italy (Mori et al., 2015Mori E, Ancillotto L, Groombridge J, Howard T, Smith VS, Feneru F, et al. Macroparasites of introduced parakeets in Italy: a possible role for parasite-mediated competition. Parasitol Res 2015; 114(9): 3277-3281. http://dx.doi.org/10.1007/s00436-015-4548-2. PMid:26025315.
http://dx.doi.org/10.1007/s00436-015-454...
; Briceño et al., 2017Briceño C, Surot D, González-Acuña D, Martínez FJ, Fredes F. Parasitic survey on introduced monk parakeets (Myiopsitta monachus) in Santiago, Chile. Rev Bras Parasitol Vet 2017; 26(2): 129-135. http://dx.doi.org/10.1590/s1984-29612017023. PMid:28746442.
http://dx.doi.org/10.1590/s1984-29612017...
). Finally, the soft tick Argas monachus (Ixodoidea: Argasidae) is also specific to monk parakeets and all stages of this parasite have been found dwelling in nests of these birds in Argentina and Paraguay (Keirans et al., 1973Keirans JE, Radovsky FJ, Clifford CM. Argas (Argas) monachus, new species (Ixodoidea: Argasidae), from nests of the monk parakeet, Myiopsitta monachus, in Argentina. J Med Entomol 1973; 10(5): 511-516. http://dx.doi.org/10.1093/jmedent/10.5.511. PMid:4760629.
http://dx.doi.org/10.1093/jmedent/10.5.5...
; Mastropaolo et al., 2011Mastropaolo M, Turienzo P, Di Iorio O, Nava S, Venzal JM, Guglielmone AA, et al. Distribution and 16S rDNA sequences of Argas monachus (Acari: Argasidae), a soft tick parasite of Myiopsitta monachus (Aves: Psittacidae). Exp Appl Acarol 2011; 55(3): 283-291. https://doi.org/10.1007/s10493-011-9469-x.
https://doi.org/10.1007/s10493-011-9469-...
). Furthermore, in their invasive distribution, monk parakeets are also capable of acquiring local parasites. Consequently, it was found in Rome, Italy, that monk parakeets harbored not only the invasive parasites P. fulvofasciatum and O. bursa, but also the flies Crataerina pallida and Ornithophila metallica (Diptera: Hippoboscidae) and the louse Columbicola columbae (Phthiraptera: Philopteridae) (Ancillotto et al., 2018Ancillotto L, Studer V, Howard T, Smith VS, McAlister E, Beccaloni J, et al. Environmental drivers of parasite load and species richness in introduced parakeets in an urban landscape. Parasitol Res 2018; 117(11): 3591-3599. http://dx.doi.org/10.1007/s00436-018-6058-5. PMid:30167793.
http://dx.doi.org/10.1007/s00436-018-605...
).

The aim of the present study was to report on the presence of abundant mites found on monk parakeet chicks in Santiago, characterize them morphologically and genetically and discuss the potential ecological and health implications of this blood-sucking mite for local fauna.

Material and Methods

Study site

This study was conducted in the Metropolitan Region of Santiago (33º27’ S; 70º38’ W), Chile. This region is located in the Mediterranean bioclimatic zone of Central Chile, which is characterized by dry summers and wet winters, with marked interannual variability due to the El Niño-Southern Oscillation phenomenon (Amigo & Ramírez, 1998Amigo J, Ramírez C. A bioclimatic classification of Chile: woodland communities in the temperate zone. Plant Ecol 1998; 136(1): 9-26. http://dx.doi.org/10.1023/A:1009714201917.
http://dx.doi.org/10.1023/A:100971420191...
). The mean annual temperature is 13.2 ºC and the mean annual precipitation is 531 mm (Schulz et al., 2010Schulz JJ, Cayuela L, Echeverria C, Salas J, Rey Benayas JM. Monitoring land cover change of the dryland forest landscape of Central Chile (1975-2008). Appl Geogr 2010; 30(3): 436-447. http://dx.doi.org/10.1016/j.apgeog.2009.12.003.
http://dx.doi.org/10.1016/j.apgeog.2009....
). Temperature and humidity depend upon topography, resulting in a vegetation mosaic of Acacia caven shrubland on lower hillslopes, and evergreen sclerophyllous forest, mainly on watersheds and south-facing slopes (Badano et al., 2005Badano EI, Cavieres LA, Molina-Montenegro MA, Quiroz CL. Slope aspect influences plant association patterns in the Mediterranean matorral of central Chile. J Arid Environ 2005; 62(1): 93-108. http://dx.doi.org/10.1016/j.jaridenv.2004.10.012.
http://dx.doi.org/10.1016/j.jaridenv.200...
; Schulz et al., 2010Schulz JJ, Cayuela L, Echeverria C, Salas J, Rey Benayas JM. Monitoring land cover change of the dryland forest landscape of Central Chile (1975-2008). Appl Geogr 2010; 30(3): 436-447. http://dx.doi.org/10.1016/j.apgeog.2009.12.003.
http://dx.doi.org/10.1016/j.apgeog.2009....
).

Sample collection

As part of a research project aiming to asses monk parakeets’ ecological and sanitary impact, monk parakeet nestlings (<40 days old, as suggested by Eberhard (1998)Eberhard JR. Breeding biology of the monk parakeet. Wilson Bull 1998; 110(4): 463-473. were manually collected from nests throughout the city of Santiago, during two of their reproductive seasons (austral springs of 2017 and 2018). During the collection process, abundant mites on some of the nestlings were noted. These arthropods were collected and preserved in 70% ethanol. Some of them were subsequently clarified in Nesbitt solution and mounted in Berlese medium (Krantz & Walter, 2009Krantz GW, Walter DE. A manual of acarology. 3rd ed. Lubbock, Texas: Texas Tech University Press; 2009.) for viewing and photographing using bright-field microscopy (Bf; Leica DM1000; Figures 1 and 2) and scanning electron microscopy (SEM; Hitachi SU3500; Figure 1A).

Figure 1
Female of Ornithonyssus bursa. (A) Dorsal general view (SEM); (B) Dorsal general view (Bf); (C) Posterior margin of the dorsal plate with Z3, Z4, Z5 and S5 setae.
Figure 2
Female of Ornithonyssus bursa. (A) Anal plate with paranal setae (paa) and postanal seta (poa); (B) General view of the chelicera; (C) Sternal plate with three sternal setae (st1-st3); (D) Epigynal plate with epigynal seta (st5).

Molecular analyses

To contribute to identification of mite species, five mites were individually pressed between two frozen glass slides and squashed for DNA extraction (Briceño et al., 2020Briceño C, González-Acuña D, Jiménez JE, Bornscheuer ML, Funk SM, Knapp LA. Ear mite, Otodectes cynotis, on wild foxes (Pseudalopex spp.) in Chile. J Wildl Dis 2020; 56(1): 105-112. http://dx.doi.org/10.7589/2018-10-247. PMid:31329523.
http://dx.doi.org/10.7589/2018-10-247...
). Biological material was retrieved by pipetting 180 µL of T1 buffer provided in the NucleoSpin® tissue DNA kit (Macherey-Nagel Ltd., Düren, Germany) on the rim of the slides, and collecting the material through capillary action. Extraction of DNA from each mite was completed using the NucleoSpin® tissue DNA kit, following the manufacturer’s instructions.

In order to perform PCR, a fragment of the 18S rRNA gene was amplified using the following primers: 5’-CTA TTG GAG GGC AAG TCT GG-3’ (forward) and 5´-TGG CAT AGT TTA TGG TTA G-3´ (reverse). These are modified versions of the primers Mite18S-1F and Mite18S-1R published by Otto & Wilson (2001)Otto JC, Wilson KJ. Assessment of the usefulness of ribosomal 18S and mitochondrial COI sequences in Prostigmata phylogeny. In: Halliday RB, Walter DE, Proctor HC, Norton RA, Colloff MJ, editors. Acarology: Proceedings of the 10th International Congress. Melbourne: CSIRO Publishing; 2001. p. 100-109.. PCR was performed using Taq DNA polymerase with the ThermoPol® buffer kit (New England BioLabs®), following the manufacturer’s instructions. Reactions were set up in a volume of 25 µl and contained the following: 1X of ThermoPol® reaction buffer, 200 µM of each dNTP, 0.2 µM of each primer, 2 µL of genomic DNA extracted as described above and 0.625 units of Taq polymerase. Negative controls, in which nuclease-free water was added in place of the DNA template, were used to confirm that no contamination of reagents had occurred. The PCR sequence consisted of a modified version of what was described by Otto & Wilson (2001)Otto JC, Wilson KJ. Assessment of the usefulness of ribosomal 18S and mitochondrial COI sequences in Prostigmata phylogeny. In: Halliday RB, Walter DE, Proctor HC, Norton RA, Colloff MJ, editors. Acarology: Proceedings of the 10th International Congress. Melbourne: CSIRO Publishing; 2001. p. 100-109.: 94 °C for 1 min; 35 cycles of 94 °C for 20 sec, 50 °C for 30 sec and 72 °C for 1 min and 30 secs; and a final elongation cycle of 72 °C for 5 min. The PCR products were analyzed by separately distributing 5 µL of each amplicon on 1.5% agarose gel stained using GelRed®, and visualizing the results under ultraviolet light. Successful PCR reactions (four in total) were then purified using the DNA Clean & ConcentratorTM-5 kit (Zymo Research), following the manufacturer’s instructions. Purified PCR products were then sequenced using both forward and reverse primers (Macrogen Inc., Seoul, South Korea). DNA sequences were edited manually by reviewing chromatograms and were aligned using MEGA 7 (Kumar et al., 2016Kumar S, Stecher G, Tamura K. MEGA7: molecular evolutionary genetics analysis version 7.0 for Bigger Datasets. Mol Biol Evol 2016; 33(7): 1870-1874. http://dx.doi.org/10.1093/molbev/msw054. PMid:27004904.
http://dx.doi.org/10.1093/molbev/msw054...
).

Results

Most of the manually collected monk parakeet chicks had abundant mites on them, as did the nest materials. During transportation to the laboratory for subsequent analyses, many of these mites were found creeping on research team members, who received bites that left marks lasting for days. The mites also remained on the team members’ clothing for days. Under a microscope (Figure 1A, B), these were identified as mites of the order Mesostigmata, potentially of the species Ornithonyssus bursa.

The following characteristics were described. Dorsal plate complete with short setae and with gradual distal narrowing, posterior margin of dorsal shield with four pairs of posterior setae, Z4 present and short (Figure 1AC); sternal plate with three sternal setae inside the plate (Figure 2C); chelicerae not enlarged distally (Figure 2B); epigynal plate with tapered distal end (Figure 2D); anal plate longer than wide (Figure 2A) (Strandtmann & Wharton, 1958Strandtmann RW, Wharton GW. Manual of mesostigmatid mites. College Park: The Institute of Acarology, Department of Zoology, University of Maryland; 1958.; Denmark & Cromroy, 2003Denmark HA, Cromroy HL. Tropical Fowl Mite, Ornithonyssus bursa (Berlese) (Arachnida: Acari: Macronyssidae). IFAS Extension [online] 2003 [cited 2020 Dec 11];297: 1-3. Available from: https://edis.ifas.ufl.edu/in575
https://edis.ifas.ufl.edu/in575...
; Radovsky, 2010Radovsky FJ. Revision of Genera of the parasitic mite family Macronyssidae (Mesostigmata: Dermanyssoidea) of the world. West Bloomfield, Michigan: Indra Publishing House; 2010.; Lareschi et al., 2017Lareschi M, Cicuttin GL, De Salvo MN, Ibañez L, Montalti D. The tropical fowl mite Ornithonyssus bursa (Acari: Mesostigmata: Macronyssidae) parasitizing the European starling Sturnus vulgaris (Aves: Passeriformes: Sturnidae), an invasive bird in central Argentina. An approach to the bacterial fauna of this mite. Rev Mex Biodivers 2017; 88(2): 454-458. https://doi.org/10.1016/j.rmb.2017.03.022.
https://doi.org/10.1016/j.rmb.2017.03.02...
; Bassini-Silva et al., 2019Bassini-Silva R, Jacinavicius FC, Hernandes FA, Ochoa R, Bauchan GR, Dowling APG, et al. Dermatitis in humans caused by Ornithonyssus bursa (Berlese 1888) (Mesostigmata: Macronyssidae) and new records from Brazil. Rev Bras Parasitol Vet 2019; 28(1): 134-139. http://dx.doi.org/10.1590/s1984-296120180097. PMid:30785556.
http://dx.doi.org/10.1590/s1984-29612018...
).

The preparations were deposited in the Collection of the Animal Science Department (Colección del Departamento de Ciencia Animal, CDCA; Universidad de Concepción, Chillán) under the numbers CDCA-352-353. DNA amplification by means of PCR provided four identical sequences (GenBank accession number MT176123; 457 bp), each obtained from individual mites, with 100% homology to O. bursa at the 18S ribosomal RNA gene (Reference FJ911854; 1597 bp).

Discussion

The present manuscript provides the first report of occurrence of the tropical fowl mite (Ornithonyssus bursa Berlese, 1888) in Chile. This mite belongs to the order Mesostigmata and parasitizes passerines and domestic birds (Sreenivasa Murthy & Panda, 2016Sreenivasa Murthy GS, Panda R. Prevalence of Dermanyssus and Ornithonyssus species of mites in poultry farms of Vikarabad area of Hyderabad. J Parasit Dis 2016; 40(4): 1372-1375. http://dx.doi.org/10.1007/s12639-015-0693-x. PMid:27876951.
http://dx.doi.org/10.1007/s12639-015-069...
). It is found in warmer areas of the world including North, Central and South America, in Argentina, Brazil and Colombia (Aramburú et al., 2002Aramburú R, Cicchino A, Bucher E. Material Vegetal Fresco En Cámaras De Cría De La Cotorra Argentina Myiopsitta monachus (Psittacidae). Ornitol Neotrop 2002; 13(4): 433-436.; Mascarenhas et al., 2009Mascarenhas CS, Coimbra MAA, Müller G, Brum JGW. Ocorrência de Ornithonyssus bursa (Berlese, 1888) (Acari: Macronyssidae) em filhotes de Megascops choliba (corujinha-do-mato) e Pitangus sulphuratus (bem-te-vi), no Rio Grande do Sul, Brasil. Rev Bras Parasitol Vet 2009; 18(4): 69-70. https://doi.org/10.4322/rbpv.01804013.
https://doi.org/10.4322/rbpv.01804013...
; Sreenivasa Murthy & Panda, 2016Sreenivasa Murthy GS, Panda R. Prevalence of Dermanyssus and Ornithonyssus species of mites in poultry farms of Vikarabad area of Hyderabad. J Parasit Dis 2016; 40(4): 1372-1375. http://dx.doi.org/10.1007/s12639-015-0693-x. PMid:27876951.
http://dx.doi.org/10.1007/s12639-015-069...
; Bassini-Silva et al., 2019Bassini-Silva R, Jacinavicius FC, Hernandes FA, Ochoa R, Bauchan GR, Dowling APG, et al. Dermatitis in humans caused by Ornithonyssus bursa (Berlese 1888) (Mesostigmata: Macronyssidae) and new records from Brazil. Rev Bras Parasitol Vet 2019; 28(1): 134-139. http://dx.doi.org/10.1590/s1984-296120180097. PMid:30785556.
http://dx.doi.org/10.1590/s1984-29612018...
; Mesquita-Sousa et al., 2020Mesquita-Sousa D, Viegas-Melo D, Martins TF, Monteiro SG, Faccini JLH, Labruna MB, et al. An overview of gamasoidosis caused by Ornithonyssus bursa (Mesostigmata: Macronyssidae) in Brazil and new case records. Int J Acarol 2020; 40(7): 1-6. http://dx.doi.org/10.1080/01647954.2020.1810119.
http://dx.doi.org/10.1080/01647954.2020....
). It was recently described as an invasive parasite in Italy (Castelli et al., 2015Castelli E, Viviano E, Torina A, Caputo V, Bongiorno MR. Avian mite dermatitis: an Italian case indicating the establishment and spread of Ornithonyssus bursa (Acari: Gamasida: Macronyssidae) (Berlese, 1888) in Europe. Int J Dermatol 2015; 54(7): 795-799. http://dx.doi.org/10.1111/ijd.12739. PMid:25660724.
http://dx.doi.org/10.1111/ijd.12739...
) and Spain (Mori et al., 2019Mori E, Sala JP, Fattorini N, Menchetti M, Montalvo T, Senar JC. Ectoparasite sharing among native and invasive birds in a metropolitan area. Parasitol Res 2019; 118(2): 399-409. http://dx.doi.org/10.1007/s00436-018-6174-2. PMid:30565194.
http://dx.doi.org/10.1007/s00436-018-617...
). It has also been found in domestic fowl in Indonesia, India (Sreenivasa Murthy & Panda, 2016Sreenivasa Murthy GS, Panda R. Prevalence of Dermanyssus and Ornithonyssus species of mites in poultry farms of Vikarabad area of Hyderabad. J Parasit Dis 2016; 40(4): 1372-1375. http://dx.doi.org/10.1007/s12639-015-0693-x. PMid:27876951.
http://dx.doi.org/10.1007/s12639-015-069...
; Selfiannisa et al., 2018Selfiannisa F, Susilowati S, Hastutiek P, Suwanti LT, Kusnoto K, Sunarso A. Investation of Ectoparasites In Chickens In Village of Kramat District of Bangkalan Regency of Bangkalan. J Parasit Sci 2018; 2(2): 57-60. http://dx.doi.org/10.20473/jops.v2i2.16400.
http://dx.doi.org/10.20473/jops.v2i2.164...
) and various locations in Africa and Australia (Denmark & Cromroy, 2003Denmark HA, Cromroy HL. Tropical Fowl Mite, Ornithonyssus bursa (Berlese) (Arachnida: Acari: Macronyssidae). IFAS Extension [online] 2003 [cited 2020 Dec 11];297: 1-3. Available from: https://edis.ifas.ufl.edu/in575
https://edis.ifas.ufl.edu/in575...
).

The tropical fowl mite produces feather asymmetry (Proctor & Owens, 2000Proctor H, Owens I. Mites and birds: diversity, parasitism and coevolution. Trends Ecol Evol 2000; 15(9): 358-364. http://dx.doi.org/10.1016/S0169-5347(00)01924-8. PMid:10931667.
http://dx.doi.org/10.1016/S0169-5347(00)...
), weight loss and reduced numbers of eggs and sperm counts in birds (Sreenivasa Murthy & Panda, 2016Sreenivasa Murthy GS, Panda R. Prevalence of Dermanyssus and Ornithonyssus species of mites in poultry farms of Vikarabad area of Hyderabad. J Parasit Dis 2016; 40(4): 1372-1375. http://dx.doi.org/10.1007/s12639-015-0693-x. PMid:27876951.
http://dx.doi.org/10.1007/s12639-015-069...
). This parasite may impact the poultry industry (Santillán et al., 2015Santillán MÁ, Grande JM, Liébana MS, Martínez P, Díaz LA, Bragagnolo LA, et al. New hosts for the mite Ornithonyssus bursa in Argentina. Med Vet Entomol 2015; 29(4): 439-443. http://dx.doi.org/10.1111/mve.12129. PMid:26258483.
http://dx.doi.org/10.1111/mve.12129...
; Sreenivasa Murthy & Panda, 2016Sreenivasa Murthy GS, Panda R. Prevalence of Dermanyssus and Ornithonyssus species of mites in poultry farms of Vikarabad area of Hyderabad. J Parasit Dis 2016; 40(4): 1372-1375. http://dx.doi.org/10.1007/s12639-015-0693-x. PMid:27876951.
http://dx.doi.org/10.1007/s12639-015-069...
; Selfiannisa et al., 2018Selfiannisa F, Susilowati S, Hastutiek P, Suwanti LT, Kusnoto K, Sunarso A. Investation of Ectoparasites In Chickens In Village of Kramat District of Bangkalan Regency of Bangkalan. J Parasit Sci 2018; 2(2): 57-60. http://dx.doi.org/10.20473/jops.v2i2.16400.
http://dx.doi.org/10.20473/jops.v2i2.164...
), considering that it has frequently been found parasitizing backyard chickens in Brazil (Guimarães et al., 2001Guimarães J, Barros-Battesti D, Tucci E. Ectoparasitos de importância veterinária. São Paulo: Editora Plêiade Ltda; 2001.). Moreover, it has the potential to feed on mammals such as mice and rabbits (Sikes & Chamberlain, 1954Sikes RK, Chamberlain RW. Laboratory observations on three species of bird mites. J Parasitol 1954; 40(6): 691-697. http://dx.doi.org/10.2307/3273713. PMid:13212549.
http://dx.doi.org/10.2307/3273713...
).

This parasite also bites humans (Fox, 1957Fox I. Ornithonyssus bursa (Berlese) attacking man in Puerto Rico. J Econ Entomol 1957; 50(6): 838. http://dx.doi.org/10.1093/jee/50.6.838.
http://dx.doi.org/10.1093/jee/50.6.838...
; Oliveira et al., 2012Oliveira CB, Tonin AA, Monteiro SG. Parasitismo do ácaro Ornithonyssus bursa em humanos no Sul do Brasil. Acta Sci Vet 2012; 40(4): 1091.; Castelli et al., 2015Castelli E, Viviano E, Torina A, Caputo V, Bongiorno MR. Avian mite dermatitis: an Italian case indicating the establishment and spread of Ornithonyssus bursa (Acari: Gamasida: Macronyssidae) (Berlese, 1888) in Europe. Int J Dermatol 2015; 54(7): 795-799. http://dx.doi.org/10.1111/ijd.12739. PMid:25660724.
http://dx.doi.org/10.1111/ijd.12739...
; Mentz et al., 2015Mentz MB, Silva GL, Silva CE. Dermatitis caused by the tropical fowl mite Ornithonyssus bursa (Berlese) (Acari: Macronyssidae): a case report in humans. Rev Soc Bras Med Trop 2015; 48(6): 786-788. http://dx.doi.org/10.1590/0037-8682-0170-2015. PMid:26676510.
http://dx.doi.org/10.1590/0037-8682-0170...
; Bassini-Silva et al., 2019Bassini-Silva R, Jacinavicius FC, Hernandes FA, Ochoa R, Bauchan GR, Dowling APG, et al. Dermatitis in humans caused by Ornithonyssus bursa (Berlese 1888) (Mesostigmata: Macronyssidae) and new records from Brazil. Rev Bras Parasitol Vet 2019; 28(1): 134-139. http://dx.doi.org/10.1590/s1984-296120180097. PMid:30785556.
http://dx.doi.org/10.1590/s1984-29612018...
). It can move into houses from nests when these are close to human settlements (Oliveira et al., 2012Oliveira CB, Tonin AA, Monteiro SG. Parasitismo do ácaro Ornithonyssus bursa em humanos no Sul do Brasil. Acta Sci Vet 2012; 40(4): 1091.; Castelli et al., 2015Castelli E, Viviano E, Torina A, Caputo V, Bongiorno MR. Avian mite dermatitis: an Italian case indicating the establishment and spread of Ornithonyssus bursa (Acari: Gamasida: Macronyssidae) (Berlese, 1888) in Europe. Int J Dermatol 2015; 54(7): 795-799. http://dx.doi.org/10.1111/ijd.12739. PMid:25660724.
http://dx.doi.org/10.1111/ijd.12739...
). Because it is hematophagous, it has also the potential to transmit pathogens such as bacteria and viruses (Santillán et al., 2015Santillán MÁ, Grande JM, Liébana MS, Martínez P, Díaz LA, Bragagnolo LA, et al. New hosts for the mite Ornithonyssus bursa in Argentina. Med Vet Entomol 2015; 29(4): 439-443. http://dx.doi.org/10.1111/mve.12129. PMid:26258483.
http://dx.doi.org/10.1111/mve.12129...
; Lareschi et al., 2017Lareschi M, Cicuttin GL, De Salvo MN, Ibañez L, Montalti D. The tropical fowl mite Ornithonyssus bursa (Acari: Mesostigmata: Macronyssidae) parasitizing the European starling Sturnus vulgaris (Aves: Passeriformes: Sturnidae), an invasive bird in central Argentina. An approach to the bacterial fauna of this mite. Rev Mex Biodivers 2017; 88(2): 454-458. https://doi.org/10.1016/j.rmb.2017.03.022.
https://doi.org/10.1016/j.rmb.2017.03.02...
).

Ornithonyssus bursa has been described in monk parakeets in their area of native distribution (Aramburú et al., 2002Aramburú R, Cicchino A, Bucher E. Material Vegetal Fresco En Cámaras De Cría De La Cotorra Argentina Myiopsitta monachus (Psittacidae). Ornitol Neotrop 2002; 13(4): 433-436.). It also affects several bird species with diverse host infestation rates (Santillán et al., 2015Santillán MÁ, Grande JM, Liébana MS, Martínez P, Díaz LA, Bragagnolo LA, et al. New hosts for the mite Ornithonyssus bursa in Argentina. Med Vet Entomol 2015; 29(4): 439-443. http://dx.doi.org/10.1111/mve.12129. PMid:26258483.
http://dx.doi.org/10.1111/mve.12129...
). This mite has been detected parasitizing American kestrels (Falco sparverius) (Liébana et al., 2011Liébana MS, Santillán MÁ, Cicchino AC, Sarasola JH, Martínez P, Cabezas S, et al. Ectoparasites In free-ranging american kestrels in Argentina: implications for the transmission of viral diseases. J Raptor Res 2011; 45(4): 335-341. http://dx.doi.org/10.3356/JRR-11-26.1.
http://dx.doi.org/10.3356/JRR-11-26.1...
) and has been found at high prevalence rates (90%) in native blue-crown parakeet chicks (Aratinga acuticaudata) in Argentina (Aramburú et al., 2003Aramburú R, Calvo S, Alzugaray ME, Cicchino A. Ectoparasitic load of monk parakeet (Myiopsitta monachus, Psittacidae) nestlings. Ornitol Neotrop 2003; 14(3): 415-418.). Also in Argentina, this mite has been identified as an ectoparasite of the invasive European starling (Sturnus vulgaris), and further, as vector of Wolbachia sp. bacteria (Lareschi et al., 2017Lareschi M, Cicuttin GL, De Salvo MN, Ibañez L, Montalti D. The tropical fowl mite Ornithonyssus bursa (Acari: Mesostigmata: Macronyssidae) parasitizing the European starling Sturnus vulgaris (Aves: Passeriformes: Sturnidae), an invasive bird in central Argentina. An approach to the bacterial fauna of this mite. Rev Mex Biodivers 2017; 88(2): 454-458. https://doi.org/10.1016/j.rmb.2017.03.022.
https://doi.org/10.1016/j.rmb.2017.03.02...
).

The tropical fowl mite is considered to be a common nest parasite of passerines (Proctor & Owens, 2000Proctor H, Owens I. Mites and birds: diversity, parasitism and coevolution. Trends Ecol Evol 2000; 15(9): 358-364. http://dx.doi.org/10.1016/S0169-5347(00)01924-8. PMid:10931667.
http://dx.doi.org/10.1016/S0169-5347(00)...
), affecting sparrows (Passer domesticus) and northern mockingbirds (Mimus polyglottos) in Florida, USA (Phillis & Cromroy, 1972Phillis WA 3rd, Cromroy HL. A preliminary survey of ectoparasitic mites (Acari) of the house sparrow and mockingbird in Florida. Fla Entomol 1972; 55(4): 258. http://dx.doi.org/10.2307/3493376.
http://dx.doi.org/10.2307/3493376...
), rock pigeons (Columba livia) in Colombia (Pérez-García et al., 2015Pérez-García J, Monsalve-Arcila D, Márquez-Villegas C. Presencia de parásitos y enterobacterias en palomas ferales (Columba livia) en áreas urbanas en Envigado, Colombia. Rev Fac Nac Salud Pública 2015; 33(3): 370-376. http://dx.doi.org/10.17533/udea.rfnsp.v33n3a06.
http://dx.doi.org/10.17533/udea.rfnsp.v3...
) and Spain (Mori et al., 2019Mori E, Sala JP, Fattorini N, Menchetti M, Montalvo T, Senar JC. Ectoparasite sharing among native and invasive birds in a metropolitan area. Parasitol Res 2019; 118(2): 399-409. http://dx.doi.org/10.1007/s00436-018-6174-2. PMid:30565194.
http://dx.doi.org/10.1007/s00436-018-617...
) and swallows (Hirundo rustica) in Denmark; in the latter it reduced clutch size (Moller, 1991Moller AP. Ectoparasite loads affect optimal clutch size in swallows. Funct Ecol 1991; 5(3): 351-359. http://dx.doi.org/10.2307/2389806.
http://dx.doi.org/10.2307/2389806...
). In New Zealand, it has been found to diminish the body size of chicks of North Island robins (Petroica longipes) and force them to fledge at an early age, thus increasing their vulnerability to predators (Berggren, 2005Berggren Å. Effect of the blood-sucking mite Ornithonyssus bursa on chick growth and fledging age in the North Island robin. N Z J Ecol 2005; 29(2): 243-250.).

Ornithonyssus bursa has been recently found at a high infectious rate (97%) in chicks of invasive monk parakeets in Barcelona, Spain (Mori et al., 2019Mori E, Sala JP, Fattorini N, Menchetti M, Montalvo T, Senar JC. Ectoparasite sharing among native and invasive birds in a metropolitan area. Parasitol Res 2019; 118(2): 399-409. http://dx.doi.org/10.1007/s00436-018-6174-2. PMid:30565194.
http://dx.doi.org/10.1007/s00436-018-617...
), and it was suggested that this was an invasive parasite. In addition, it seems that O. bursa is already established in Europe: human dermatitis cases have already been diagnosed in Sicily (Castelli et al., 2015Castelli E, Viviano E, Torina A, Caputo V, Bongiorno MR. Avian mite dermatitis: an Italian case indicating the establishment and spread of Ornithonyssus bursa (Acari: Gamasida: Macronyssidae) (Berlese, 1888) in Europe. Int J Dermatol 2015; 54(7): 795-799. http://dx.doi.org/10.1111/ijd.12739. PMid:25660724.
http://dx.doi.org/10.1111/ijd.12739...
), where free-ranging invasive monk parakeet populations have been established (ISSG, 2015Invasive Species Specialist Group – ISSG. Global Invasive Species Database. Myiopsita monachus (monk parakeet) [online]. 2015 [cited 2020 Nov 5]. Available from: http://www.iucngisd.org/gisd/speciesname/myiopsitta+monachus
http://www.iucngisd.org/gisd/speciesname...
), thus representing a potential source of the introduced mite. In Rome, introduced urban populations of monk parakeets have also been found to be parasitized by O. bursa (Ancillotto et al., 2018Ancillotto L, Studer V, Howard T, Smith VS, McAlister E, Beccaloni J, et al. Environmental drivers of parasite load and species richness in introduced parakeets in an urban landscape. Parasitol Res 2018; 117(11): 3591-3599. http://dx.doi.org/10.1007/s00436-018-6058-5. PMid:30167793.
http://dx.doi.org/10.1007/s00436-018-605...
). One alternative hypothesis could be that this mite reached these places carried by migratory birds such as the European starling or the barn swallow (Hirundo rustica), which are known to be hosts of tropical fowl mites (Moller, 2010Moller AP. Host – parasite interactions and vectors in the barn swallow in relation to climate change. Glob Change Biol 2010; 16(4): 1158-1170. http://dx.doi.org/10.1111/j.1365-2486.2009.02035.x.
http://dx.doi.org/10.1111/j.1365-2486.20...
; Lareschi et al., 2017Lareschi M, Cicuttin GL, De Salvo MN, Ibañez L, Montalti D. The tropical fowl mite Ornithonyssus bursa (Acari: Mesostigmata: Macronyssidae) parasitizing the European starling Sturnus vulgaris (Aves: Passeriformes: Sturnidae), an invasive bird in central Argentina. An approach to the bacterial fauna of this mite. Rev Mex Biodivers 2017; 88(2): 454-458. https://doi.org/10.1016/j.rmb.2017.03.022.
https://doi.org/10.1016/j.rmb.2017.03.02...
).

The dynamics of macronyssid mites are strongly influenced by the environment (Arce et al., 2018Arce SI, Manzoli DE, Saravia-Pietropaolo MJ, Quiroga MA, Antoniazzi LR, Lareschi M, et al. The tropical fowl mite, Ornithonyssus bursa (Acari : Macronyssidae): environmental and host factors associated with its occurrence in Argentine passerine communities. Parasitol Res 2018; 117(10): 32573267. http://dx.doi.org/10.1007/s00436-018-6025-1. PMid:30069828.
http://dx.doi.org/10.1007/s00436-018-602...
) and O. bursa has been shown to have decreasing virulence with increasing temperatures (Moller, 2010Moller AP. Host – parasite interactions and vectors in the barn swallow in relation to climate change. Glob Change Biol 2010; 16(4): 1158-1170. http://dx.doi.org/10.1111/j.1365-2486.2009.02035.x.
http://dx.doi.org/10.1111/j.1365-2486.20...
). This may be relevant in hot environments such as urban Santiago, where some meteorological stations report average maximum temperatures higher than 30 ºC in January and February (McPhee et al., 2014McPhee J, Cortés G, Rojas M, Garcia L, Descalzi A, Vargas L. Downscaling climate changes for Santiago: What effects can be expected? In: Krellenberg K, Hansjürgens B, editors. Climate adaptation Santiago. New York: Springer Berlin Heidelberg; 2014. p. 19-41. http://dx.doi.org/10.1007/978-3-642-39103-3_2.
http://dx.doi.org/10.1007/978-3-642-3910...
). Here, the tropical fowl mite might find relief in controlled environments. Nest chambers constructed by monk parakeets have been shown to be somewhat controlled environments in relation to external conditions. They are able to buffer maximum ambient temperatures such that the temperature in the nest may be as much as seven degrees lower than the ambient temperature during the breeding season (Viana et al., 2016Viana IR, Strubbe D, Zocche JJ. Monk parakeet invasion success: a role for nest thermoregulation and bactericidal potential of plant nest material? Biol Invasions 2016; 18(5): 1305-1315. http://dx.doi.org/10.1007/s10530-016-1068-7.
http://dx.doi.org/10.1007/s10530-016-106...
).

Monk parakeets are known to share space and interact with other birds at the same trees or feeding sites (Briceño et al., 2019Briceño C, Sandoval-Rodríguez A, Yévenes K, Larraechea M, Morgado A, Chappuzeau CV, et al. Interactions between invasive Monk Parakeets (Myiopsitta monachus) and Other Bird Species during Nesting Seasons in Santiago, Chile. Animals (Basel) 2019; 9(11): 923. http://dx.doi.org/10.3390/ani9110923. PMid:31694253.
http://dx.doi.org/10.3390/ani9110923...
; Mori et al., 2019Mori E, Sala JP, Fattorini N, Menchetti M, Montalvo T, Senar JC. Ectoparasite sharing among native and invasive birds in a metropolitan area. Parasitol Res 2019; 118(2): 399-409. http://dx.doi.org/10.1007/s00436-018-6174-2. PMid:30565194.
http://dx.doi.org/10.1007/s00436-018-617...
). Because O. bursa is known to be abundant on monk parakeet chicks and in their nests (Aramburú et al., 2003Aramburú R, Calvo S, Alzugaray ME, Cicchino A. Ectoparasitic load of monk parakeet (Myiopsitta monachus, Psittacidae) nestlings. Ornitol Neotrop 2003; 14(3): 415-418.), there is therefore a risk for other birds that use parakeets’ nests, given that these ectoparasites can overwinter in nesting holes (Mori et al,. 2019). In Santiago, both native and introduced bird species occupy monk parakeets’ nest for breeding (Briceño et al., 2019Briceño C, Sandoval-Rodríguez A, Yévenes K, Larraechea M, Morgado A, Chappuzeau CV, et al. Interactions between invasive Monk Parakeets (Myiopsitta monachus) and Other Bird Species during Nesting Seasons in Santiago, Chile. Animals (Basel) 2019; 9(11): 923. http://dx.doi.org/10.3390/ani9110923. PMid:31694253.
http://dx.doi.org/10.3390/ani9110923...
). Introduced rock pigeons and house sparrows, which are both synanthropic species, are known to become infested with O. bursa mites (Phillis & Cromroy, 1972Phillis WA 3rd, Cromroy HL. A preliminary survey of ectoparasitic mites (Acari) of the house sparrow and mockingbird in Florida. Fla Entomol 1972; 55(4): 258. http://dx.doi.org/10.2307/3493376.
http://dx.doi.org/10.2307/3493376...
; Pérez-García et al., 2015Pérez-García J, Monsalve-Arcila D, Márquez-Villegas C. Presencia de parásitos y enterobacterias en palomas ferales (Columba livia) en áreas urbanas en Envigado, Colombia. Rev Fac Nac Salud Pública 2015; 33(3): 370-376. http://dx.doi.org/10.17533/udea.rfnsp.v33n3a06.
http://dx.doi.org/10.17533/udea.rfnsp.v3...
; Santillán et al., 2015Santillán MÁ, Grande JM, Liébana MS, Martínez P, Díaz LA, Bragagnolo LA, et al. New hosts for the mite Ornithonyssus bursa in Argentina. Med Vet Entomol 2015; 29(4): 439-443. http://dx.doi.org/10.1111/mve.12129. PMid:26258483.
http://dx.doi.org/10.1111/mve.12129...
; Mori et al., 2019Mori E, Sala JP, Fattorini N, Menchetti M, Montalvo T, Senar JC. Ectoparasite sharing among native and invasive birds in a metropolitan area. Parasitol Res 2019; 118(2): 399-409. http://dx.doi.org/10.1007/s00436-018-6174-2. PMid:30565194.
http://dx.doi.org/10.1007/s00436-018-617...
). It is therefore likely that populations of these two introduced species are already affected by this parasite in Santiago. O. bursa was also found in 16% of a sample of free-ranging native eared doves (Zenaida auriculata) in Brazil (Goulart et al., 2011Goulart TM, Moraes DL, Prado AP. Mites associated with the eared dove, Zenaida auriculata (Des Murs, 1847), in São Paulo State, Brazil. Zoosymposia 2011; 6(1): 267-274. http://dx.doi.org/10.11646/zoosymposia.6.1.36.
http://dx.doi.org/10.11646/zoosymposia.6...
), although it was not found in an extensive study on the same species in Chile, some 400 km south of Santiago (González et al., 2004González D, Daugschies A, Rubilar L, Pohlmeyer K, Skewes O, Mey E. Fauna parasitaria de la tórtola común (Zenaida auriculata, de Murs 1847) (Columbiformes: Columbidae) en Ñuble, Chile. Parasitol Latinoam 2004; 59(1-2): 37-41. http://dx.doi.org/10.4067/S0717-77122004000100007.
http://dx.doi.org/10.4067/S0717-77122004...
). Eared doves are known to breed in monk parakeets’ nests in Santiago (Briceño et al., 2019Briceño C, Sandoval-Rodríguez A, Yévenes K, Larraechea M, Morgado A, Chappuzeau CV, et al. Interactions between invasive Monk Parakeets (Myiopsitta monachus) and Other Bird Species during Nesting Seasons in Santiago, Chile. Animals (Basel) 2019; 9(11): 923. http://dx.doi.org/10.3390/ani9110923. PMid:31694253.
http://dx.doi.org/10.3390/ani9110923...
), so it is also likely that populations in sympatry with monk parakeets may have the mite already.

The American kestrel and Harris’s hawk (Parabuteo unicinctus) are predators of monk parakeets (Celis-Diez, 2016Celis-Diez J. Observación de cernícalos (Falco sparverius) depredando polluelos de cotorra Argentina (Myiopsitta monachus) en parques urbanos de Santiago. Bol Chileno Ornitol 2016; 20(1-2): 23-24.; Briceño et al., 2019Briceño C, Sandoval-Rodríguez A, Yévenes K, Larraechea M, Morgado A, Chappuzeau CV, et al. Interactions between invasive Monk Parakeets (Myiopsitta monachus) and Other Bird Species during Nesting Seasons in Santiago, Chile. Animals (Basel) 2019; 9(11): 923. http://dx.doi.org/10.3390/ani9110923. PMid:31694253.
http://dx.doi.org/10.3390/ani9110923...
), even though other birds of prey such as the Austral pigmy owl (Glaucidium nana) and aplomado falcon (Falco femoralis) have been found breeding in monk parakeets’ nests (Briceño et al., 2019Briceño C, Sandoval-Rodríguez A, Yévenes K, Larraechea M, Morgado A, Chappuzeau CV, et al. Interactions between invasive Monk Parakeets (Myiopsitta monachus) and Other Bird Species during Nesting Seasons in Santiago, Chile. Animals (Basel) 2019; 9(11): 923. http://dx.doi.org/10.3390/ani9110923. PMid:31694253.
http://dx.doi.org/10.3390/ani9110923...
): These raptors may be at risk through predation on parakeet chicks in an mite-infested environment before nest occupation. In fact, populations of the ferruginous pigmy owl and aplomado falcon in Argentina have been described as hosts of O. bursa (Santillán et al., 2015Santillán MÁ, Grande JM, Liébana MS, Martínez P, Díaz LA, Bragagnolo LA, et al. New hosts for the mite Ornithonyssus bursa in Argentina. Med Vet Entomol 2015; 29(4): 439-443. http://dx.doi.org/10.1111/mve.12129. PMid:26258483.
http://dx.doi.org/10.1111/mve.12129...
). Other species that have been found to breed in monk parakeets’ nests in Santiago are the American kestrel and the house wren (Troglodytes aedon) (Briceño et al., 2019Briceño C, Sandoval-Rodríguez A, Yévenes K, Larraechea M, Morgado A, Chappuzeau CV, et al. Interactions between invasive Monk Parakeets (Myiopsitta monachus) and Other Bird Species during Nesting Seasons in Santiago, Chile. Animals (Basel) 2019; 9(11): 923. http://dx.doi.org/10.3390/ani9110923. PMid:31694253.
http://dx.doi.org/10.3390/ani9110923...
), which are both species on which O. bursa has been found in Argentina (Santillán et al., 2015Santillán MÁ, Grande JM, Liébana MS, Martínez P, Díaz LA, Bragagnolo LA, et al. New hosts for the mite Ornithonyssus bursa in Argentina. Med Vet Entomol 2015; 29(4): 439-443. http://dx.doi.org/10.1111/mve.12129. PMid:26258483.
http://dx.doi.org/10.1111/mve.12129...
). The chimango caracara (Milvago chimango), an abundant bird species that is suspected of thriving in urban and periurban areas and is known to share space and interact with monk parakeets (Briceño et al., 2019Briceño C, Sandoval-Rodríguez A, Yévenes K, Larraechea M, Morgado A, Chappuzeau CV, et al. Interactions between invasive Monk Parakeets (Myiopsitta monachus) and Other Bird Species during Nesting Seasons in Santiago, Chile. Animals (Basel) 2019; 9(11): 923. http://dx.doi.org/10.3390/ani9110923. PMid:31694253.
http://dx.doi.org/10.3390/ani9110923...
), has been found to be parasitized by O. bursa in Argentina, in both chicks and adults (Santillán et al., 2015Santillán MÁ, Grande JM, Liébana MS, Martínez P, Díaz LA, Bragagnolo LA, et al. New hosts for the mite Ornithonyssus bursa in Argentina. Med Vet Entomol 2015; 29(4): 439-443. http://dx.doi.org/10.1111/mve.12129. PMid:26258483.
http://dx.doi.org/10.1111/mve.12129...
).

Monk parakeets are highly gregarious, and O. bursa has been found to be more abundant in denser populations of monk parakeets (Ancillotto et al., 2018Ancillotto L, Studer V, Howard T, Smith VS, McAlister E, Beccaloni J, et al. Environmental drivers of parasite load and species richness in introduced parakeets in an urban landscape. Parasitol Res 2018; 117(11): 3591-3599. http://dx.doi.org/10.1007/s00436-018-6058-5. PMid:30167793.
http://dx.doi.org/10.1007/s00436-018-605...
; Mori et al., 2019Mori E, Sala JP, Fattorini N, Menchetti M, Montalvo T, Senar JC. Ectoparasite sharing among native and invasive birds in a metropolitan area. Parasitol Res 2019; 118(2): 399-409. http://dx.doi.org/10.1007/s00436-018-6174-2. PMid:30565194.
http://dx.doi.org/10.1007/s00436-018-617...
). Also, introduced populations of monk parakeets seem to have higher reproductive rates, resulting in denser populations than in their areas of native distribution (Senar et al., 2019Senar JC, Carrillo-Ortiz JG, Ortega-Segalerva A, Dawson Pell FSE, Pascual J, Arroyo L, et al. The reproductive capacity of Monk Parakeets Myiopsitta monachus is higher in their invasive range. Bird Study 2019; 66(1): 136-140. http://dx.doi.org/10.1080/00063657.2019.1585749.
http://dx.doi.org/10.1080/00063657.2019....
). Rock pigeons have been shown to have higher abundance of ectoparasites in areas of higher monk parakeet densities (Mori et al., 2019Mori E, Sala JP, Fattorini N, Menchetti M, Montalvo T, Senar JC. Ectoparasite sharing among native and invasive birds in a metropolitan area. Parasitol Res 2019; 118(2): 399-409. http://dx.doi.org/10.1007/s00436-018-6174-2. PMid:30565194.
http://dx.doi.org/10.1007/s00436-018-617...
), and this could apply to other species as well. Moreover, in Barcelona, the O. bursa infection rate in rock pigeons was 10%. Because this is a wide ranging bird, it has the potential to spread O. bursa over large areas, even outside urban settlements (Mori et al., 2019Mori E, Sala JP, Fattorini N, Menchetti M, Montalvo T, Senar JC. Ectoparasite sharing among native and invasive birds in a metropolitan area. Parasitol Res 2019; 118(2): 399-409. http://dx.doi.org/10.1007/s00436-018-6174-2. PMid:30565194.
http://dx.doi.org/10.1007/s00436-018-617...
).

Although field studies have determined that the tropical fowl mite has some degree of affinity for certain host species, the bird species with the highest mite prevalences are not the ones presenting the highest mite intensity. Additionally, it appears that nestlings of bird species with higher mite prevalences are the ones with higher encounter rates (Arce et al., 2018Arce SI, Manzoli DE, Saravia-Pietropaolo MJ, Quiroga MA, Antoniazzi LR, Lareschi M, et al. The tropical fowl mite, Ornithonyssus bursa (Acari : Macronyssidae): environmental and host factors associated with its occurrence in Argentine passerine communities. Parasitol Res 2018; 117(10): 32573267. http://dx.doi.org/10.1007/s00436-018-6025-1. PMid:30069828.
http://dx.doi.org/10.1007/s00436-018-602...
). This could also be relevant in relation to gregarious species such as the monk parakeet, which in its invasive distribution seems to have higher densities of nestlings, as well as longer reproductive periods (Senar et al., 2019Senar JC, Carrillo-Ortiz JG, Ortega-Segalerva A, Dawson Pell FSE, Pascual J, Arroyo L, et al. The reproductive capacity of Monk Parakeets Myiopsitta monachus is higher in their invasive range. Bird Study 2019; 66(1): 136-140. http://dx.doi.org/10.1080/00063657.2019.1585749.
http://dx.doi.org/10.1080/00063657.2019....
).

Even though in this study we did not quantify the intensity of mite infestation, it appears that the abundance was greater (we retrieved many mites from the chicks) than the one mite that was found among ninety-two adult monk parakeets collected in Santiago during 2006 and 2007 (Briceño et al., 2017Briceño C, Surot D, González-Acuña D, Martínez FJ, Fredes F. Parasitic survey on introduced monk parakeets (Myiopsitta monachus) in Santiago, Chile. Rev Bras Parasitol Vet 2017; 26(2): 129-135. http://dx.doi.org/10.1590/s1984-29612017023. PMid:28746442.
http://dx.doi.org/10.1590/s1984-29612017...
). This finding is consistent with the biology of the parasite, which mainly affects non-flying chicks (Aramburú et al., 2003Aramburú R, Calvo S, Alzugaray ME, Cicchino A. Ectoparasitic load of monk parakeet (Myiopsitta monachus, Psittacidae) nestlings. Ornitol Neotrop 2003; 14(3): 415-418.). Nonetheless, a couple of mite individuals on adult birds is all that is required for mite abundance to increase rapidly (Arce et al., 2018Arce SI, Manzoli DE, Saravia-Pietropaolo MJ, Quiroga MA, Antoniazzi LR, Lareschi M, et al. The tropical fowl mite, Ornithonyssus bursa (Acari : Macronyssidae): environmental and host factors associated with its occurrence in Argentine passerine communities. Parasitol Res 2018; 117(10): 32573267. http://dx.doi.org/10.1007/s00436-018-6025-1. PMid:30069828.
http://dx.doi.org/10.1007/s00436-018-602...
).

O. bursa has been found at high prevalence in native and invasive populations of monk parakeet nestlings in Argentina (48%) (Aramburú et al., 2003Aramburú R, Calvo S, Alzugaray ME, Cicchino A. Ectoparasitic load of monk parakeet (Myiopsitta monachus, Psittacidae) nestlings. Ornitol Neotrop 2003; 14(3): 415-418.) and Barcelona (97%) (Mori et al., 2019Mori E, Sala JP, Fattorini N, Menchetti M, Montalvo T, Senar JC. Ectoparasite sharing among native and invasive birds in a metropolitan area. Parasitol Res 2019; 118(2): 399-409. http://dx.doi.org/10.1007/s00436-018-6174-2. PMid:30565194.
http://dx.doi.org/10.1007/s00436-018-617...
), respectively. Moreover, these parakeets’ nests are occupied by several other species (Briceño et al., 2019Briceño C, Sandoval-Rodríguez A, Yévenes K, Larraechea M, Morgado A, Chappuzeau CV, et al. Interactions between invasive Monk Parakeets (Myiopsitta monachus) and Other Bird Species during Nesting Seasons in Santiago, Chile. Animals (Basel) 2019; 9(11): 923. http://dx.doi.org/10.3390/ani9110923. PMid:31694253.
http://dx.doi.org/10.3390/ani9110923...
). It therefore seems more likely that O. bursa is a co-introduced parasite (with M. monachus), with the potential to become a co-invasive parasite that infects native birds (Lymbery et al., 2014Lymbery AJ, Morine M, Kanani HG, Beatty SJ, Morgan DL. Co-invaders: the effects of alien parasites on native hosts. Int J Parasitol Parasites Wildl 2014; 3(2): 171-177. http://dx.doi.org/10.1016/j.ijppaw.2014.04.002. PMid:25180161.
http://dx.doi.org/10.1016/j.ijppaw.2014....
).

This was the first report of O. bursa in Chile, found in monk parakeets’ nestlings. The monk parakeet is considered to be one of the most invasive bird species, in part due to its condition of being an ecosystem engineer (Briceño et al., 2019Briceño C, Sandoval-Rodríguez A, Yévenes K, Larraechea M, Morgado A, Chappuzeau CV, et al. Interactions between invasive Monk Parakeets (Myiopsitta monachus) and Other Bird Species during Nesting Seasons in Santiago, Chile. Animals (Basel) 2019; 9(11): 923. http://dx.doi.org/10.3390/ani9110923. PMid:31694253.
http://dx.doi.org/10.3390/ani9110923...
). Invasive monk parakeet populations produce economic losses (Iriarte et al., 2005Iriarte JA, Lobos GA, Jaksic FM. Invasive vertebrate species in Chile and their control and monitoring by governmental agencies. Rev Chil Hist Nat 2005; 78(1): 143-154. http://dx.doi.org/10.4067/S0716-078X2005000100010.
http://dx.doi.org/10.4067/S0716-078X2005...
; Senar et al., 2019Senar JC, Carrillo-Ortiz JG, Ortega-Segalerva A, Dawson Pell FSE, Pascual J, Arroyo L, et al. The reproductive capacity of Monk Parakeets Myiopsitta monachus is higher in their invasive range. Bird Study 2019; 66(1): 136-140. http://dx.doi.org/10.1080/00063657.2019.1585749.
http://dx.doi.org/10.1080/00063657.2019....
), although little is known about their impact on animal or public health (Briceño et al., 2017Briceño C, Surot D, González-Acuña D, Martínez FJ, Fredes F. Parasitic survey on introduced monk parakeets (Myiopsitta monachus) in Santiago, Chile. Rev Bras Parasitol Vet 2017; 26(2): 129-135. http://dx.doi.org/10.1590/s1984-29612017023. PMid:28746442.
http://dx.doi.org/10.1590/s1984-29612017...
). This species continues to expand its distribution in Santiago, with consequent potential spread of the tropical fowl mite. This hematophagous mite has the potential to affect the conservation of native and/or endangered bird species through increased predation, due to forced early fledging of nestlings (Berggren, 2005Berggren Å. Effect of the blood-sucking mite Ornithonyssus bursa on chick growth and fledging age in the North Island robin. N Z J Ecol 2005; 29(2): 243-250.). It also has the potential to affect the health status of resident birds, not only through blood sucking but also as a potential vector of pathogens, with possible risk for other animals, including humans (Fox, 1957Fox I. Ornithonyssus bursa (Berlese) attacking man in Puerto Rico. J Econ Entomol 1957; 50(6): 838. http://dx.doi.org/10.1093/jee/50.6.838.
http://dx.doi.org/10.1093/jee/50.6.838...
; Oliveira et al., 2012Oliveira CB, Tonin AA, Monteiro SG. Parasitismo do ácaro Ornithonyssus bursa em humanos no Sul do Brasil. Acta Sci Vet 2012; 40(4): 1091.; Castelli et al., 2015Castelli E, Viviano E, Torina A, Caputo V, Bongiorno MR. Avian mite dermatitis: an Italian case indicating the establishment and spread of Ornithonyssus bursa (Acari: Gamasida: Macronyssidae) (Berlese, 1888) in Europe. Int J Dermatol 2015; 54(7): 795-799. http://dx.doi.org/10.1111/ijd.12739. PMid:25660724.
http://dx.doi.org/10.1111/ijd.12739...
; Mentz et al., 2015Mentz MB, Silva GL, Silva CE. Dermatitis caused by the tropical fowl mite Ornithonyssus bursa (Berlese) (Acari: Macronyssidae): a case report in humans. Rev Soc Bras Med Trop 2015; 48(6): 786-788. http://dx.doi.org/10.1590/0037-8682-0170-2015. PMid:26676510.
http://dx.doi.org/10.1590/0037-8682-0170...
; Bassini-Silva et al., 2019Bassini-Silva R, Jacinavicius FC, Hernandes FA, Ochoa R, Bauchan GR, Dowling APG, et al. Dermatitis in humans caused by Ornithonyssus bursa (Berlese 1888) (Mesostigmata: Macronyssidae) and new records from Brazil. Rev Bras Parasitol Vet 2019; 28(1): 134-139. http://dx.doi.org/10.1590/s1984-296120180097. PMid:30785556.
http://dx.doi.org/10.1590/s1984-29612018...
). Finally, our finding is also of concern for the poultry industry, which may become affected by this introduced parasite. These impacts may already be happening and further studies to understand them in detail are warranted.

Acknowledgements

This research was funded by FONDECYT Initiation No. 11160852 from the National Commission for Science and Technology of Chile (CONICYT). We are grateful to Ramón Molina, Fernando Navarrete, Patricio Toro, Pablo Dufflocq, Catalina Chappuzzeau, Angello Morgado and Florencia Olivares.

The authors express their gratitude to the communes of La Reina, Peñalolén, Las Condes, Providencia, La Pintana, San Miguel, La Florida, La Cisterna, La Granja, Recoleta, Santiago, Puente Alto, San Bernardo, Maipú, Huechuraba, Independencia, Macul and Conchalí for their logistic support and collaboration during the sampling process. Finally, the authors would also like to thank all citizens who provided valuable information on monk parakeet nest locations.

  • How to cite: Briceño C, Yévenes K, Larraechea M, Sandoval-Rodríguez A, Silva-de la Fuente MC, Fredes F, et al. First record of Ornithonyssus bursa (Berlese, 1888) (Mesostigmata: Macronyssidae) parasitizing invasive monk parakeets in Santiago, Chile. Braz J Vet Parasitol 2021; 30(1): e024020. https://doi.org/10.1590/S1984-29612021023
  • In memoriam

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Publication Dates

  • Publication in this collection
    09 Apr 2021
  • Date of issue
    2021

History

  • Received
    13 Oct 2020
  • Accepted
    08 Feb 2021
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