Mites Macronyssidae parasites of Passer domesticus (Linnaeus, 1758) (Passeriformes: Passeridae) in the Southern of Brazil

Laboratório de Parasitologia, Departamento de Microbiologia e Parasitologia, Instituto de Biologia, Universidade Federal de Pelotas, Capão do Leão, RS, Brasil. Laboratório de Parasitologia de Animais Silvestres, Departamento de Microbiologia e Parasitologia, Instituto de Biologia, Universidade Federal de Pelotas, Capão do Leão, RS, Brasil. Centro Nacional de Pesquisa para a Conservação das Aves Silvestres (CEMAVE), Instituto Chico Mendes de Conservação da Biodiversidade (ICMBio), Pelotas, RS, Brasil.


INTRODUCTION
The birds are hosts of many symbiotic animals and some of the most diverse are the mites (Arachnida: Acariformes and Parasitiformes) (Knee & Galloway, 2017). There are approximately 3,000 species of mites described, distributed in 40 families (Proctor & Owens, 2000). Among these are haematophagous mites Macronyssidae (Acari: Mesostigmata), which parasitize domestic and wild birds worldwide, being found on the body and/or nest of their hosts (Stoehr et al., 2000;Berggren, 2005).
The house sparrow, Passer domesticus (Linnaeus, 1758) (Passeriformes: Passeridae), is a nonmigratory bird, terrestrial, which can adapt itself easily to agricultural, urban and suburban environments, taking advantage of human action, occupying constructed areas which can serve as shelter and nesting (Major et al., 2004). These species come from Eurasia and the north of Africa, and has intentionally been introduced in America (Global Invasive Species Database, 2018). It was inserted in Brazil in 1906 for biological control of insects and, currently, are scattered across all Brazilian territory (Sick, 1997).
Due to the presence of synanthropic bird's nests near the residences, Macronyssidae mite (such as Ornithonyssus spp.) may occasionally bite humans and cause pruritic dermatitis (Knee & Proctor, 2007;Oliveira et al., 2012). This study aimed to investigate the occurrence of Macronyssidae mites related to P. domesticus and analyze the infestation rates regarding to gender, as well as the effects of mites in the body mass and total length of hosts native to urban areas, in the state of Rio Grande do Sul, southern of Brazil.

MATERIAL AND METHODS
A total of 100 specimens of P. domesticus [90 adults (52 males, 38 females), nine juveniles (seven males, two females) and one undetermined nestling] were captured using mist-nets (30 mm mesh) at 13 sites (public squares, gardens of private properties and empty lots) of the urban area of Pelotas After being transported in appropriate cages to the UFPel's Parasitology Laboratory, each specimen was weighed and measured, and the data assessed were: body mass, total length of the body, wings, and beak, gender and age (adult and/or juvenile). Then, using a technique called "dust-ruffing" by Walther and Clayton (1970), lice-killing talc commercially known as Piolhaves (ProvetS® Simões) (chemical compound: permethrin and sulfur) was individually applied in the bodies of the passerines, according to the manufacturer's instructions, which indicate that a thin layer of talc must be put on the body of the birds in order to repel ectoparasites, facilitating their collection. Afterward, the collected parasites were retained in 70% alcohol in containers labeled according to the host number.
The Macronyssidae mites were clarified in Amann Lactophenol, mounted on Hoyer's medium between slide and coverslip, according to Krantz (1978), photographed using an Olympus BX 41 microscope with attached camera, and the images were prepared using Adobe Photoshop CS5.
The infestations of the mites between male and female adult hosts were compared by prevalence using the Chi-square test (χ 2 ) and by mean infestation intensity by the t-test via "Bootstrap" (BCa p < 0.05) in the program Quantitative Parasitology 3.0 (Rózsa et al., 2000). In order to verify the presence of correlations between the abundance of the mites and body mass, as well as total length of the hosts, a Regression Analysis (RA) was performed in accordance with the model y = a + bx, as well as the determination coefficient (r 2 ), whose range is ≥ 0 or ≤ 1, and Pearson's correlation coefficient (r), whose range is ≥ -1 or ≤ 1 (Mukaka, 2012). For this analysis, a nestling host was disregarded. Both the regression analysis, the Chi-square test and the t-test were performed for mites, which presented prevalence greater or equal to 10% (Bush et al., 1990).

RESULTS
Among the 100 hosts examined, 31 (15 males and 14 females, one male juvenile and one unde-venile contained three mites). On the other hand, Ornithonyssus bursa (Berlese, 1888) was found only in two (n = 2) male adult hosts, totaling six mites. Only one male adult host presented co-infestation by these two mite species, where infestation intensity was three mites/host for P. reedi and two mites/host for O.

bursa.
Some of the main morphological characteristics observed in the identification of mites were: for P. reedi, sternal shield with a reticulate pattern, with the presence of three pairs of setae; opisthonotal shield with three pairs of posterior marginal setae; peritreme ending over between coxae II and III; with anterior spur on coxa II well developed (Till, 1963;Radovsky & Estébanes-González, 2001); and for O. bursa, sternal shield gradually narrowing backward, with the presence of three pairs of smaller setae, never of the width of the shield and always on the plate (Guimarães et al., 2001;Denmark & Cromroy, 2003) (Figure 1).    (1952) as Steatonyssus reedi. Shortly after, the species was taxonomically replaced by Clark and Yunker (1956) by the name Pellonyssus passeri and later synonymized as P. reedi by Till (1963). According to Rosa and Flechtmann (1981), there are records of this mite associated with several species of birds, including P. domesticus, in Africa and North America, with the first occurrence in South American house sparrow nests registered by those same authors.
The infestation by P. reedi in P. domesticus showed lower values than the ones recorded in Hungary, where 12,213 specimens were removed from 188 house sparrows in nestlings spread across 46 nests (Szabó et al., 2008). In P. domesticus' nests, studies carried out in Brazil and in Europe describe differences in infestations, where in São Paulo, 42 mites were found in three (03) out of 20 nests (Rosa & Flechtmann, 1981); and in Slovakia, 2,598 specimens were detected in only one (01) nest (Mašán et al., 2014).
In the present study, the number of mites did not influence the weight and size of the birds. Similarly, Szabó et al. (2002) observed no significant effects of infestations of these mites in the body mass and general size of the in nestlings. However, conflicting results were reported by Weddle (2000) and Stoehr et al. (2000). Weddle (2000) notes a negative correlation between the parasitizing load and the body mass of all 127 house sparrow in nestlings among 37 evaluated nests, that is, nestlings with higher infestations had lower total body masses than less infested nestlings; while Stoehr et al. (2000) observed that high levels of parasitism by P. reedi in Carpodacus mexicanus (Statius Muller, 1776) (Passeriformes: Fringillidae) in Alabama, USA, were associated with lower hematocrit and body mass values of this host.
Such results may be related to the permanent presence of the offsprings in the nests during parental care, once these mites are considered nidicolous, with high demographic density in bird nests (Berggren, 2005).
In this sense, the low infestation rates by Macronyssidae mites in P. domesticus, as well as the lack of positive correlation among P. reedi abundance, body mass and total length of birds may be related to sexual maturity of the hosts examined in the present study which were adults (n = 90) and possibly were not nesting when captured. Although the species reproduces all yearlong (Long, 1981), it is important to highlight that only females incubate eggs (Romero et al., 2008). In the present study, although there was no significant difference in P. reedi infestations between males and females, we observed that prevalence values and mean infestation intensity were higher in females.
The mites associated with birds and their nests require attention, especially in regards to synanthropic birds, which build their nests near human residences, because when young birds leave their nests, the mites seek other sources of food (Oliveira et al., 2012). There are records of dermatitis caused by O.
bursa in various regions of the world, such as the United States (Fox, 1957), India (Lodha, 1969), Argentina (Semenas & Rocha, 1998) and Italy (Castelli et al., 2015). In Brazil, there are reports of cases of O. bursa parasitism in humans, causing dermatitis with intense pruritus (Ribeiro et al., 1992;Oliveira et al., 2012; (Passeriformes: Tyrannidae) in air from the air conditioner of an apartment in Santa Maria (Oliveira et al., 2012); and an abandoned Furnarius rufus nest (Gmelin, 1788) (Passeriformes: Furnariidae) built outside an apartment in a residential county of Porto Alegre (Mentz et al., 2015). There are no records of P. reedi causing cutaneous infections in humans, although its haematophagous habits and intense infestations in birds may serve as warnings for public health and poultry farming.

CONCLUSION
This work reports on Passer domesticus acting as hosts for Pellonyssus reedi and Ornithonyssus bursa in Rio Grande do Sul, Brazil, and its respective infestation rates in house sparrows from urban areas.
Moreover, it is noted that P. reedi infestations are similar between male and female hosts, and these mite's abundance does not influence the total length and body mass of birds.

ACKNOWLEDGMENTS
To professor Cristina Helena Carneiro and to the student Álvaro Daniel Almonfrey of the Laboratório de Tradução, Versão e Revisão em Inglês, from the Instituto Federal do Espírito Santo, Campus Guarapari, Brazil, for providing this extension service.