Introduction

Parasitism is the most successful interspecific relationship in nature, measured by the frequency with which it evolved and by the parasite diversity currently recognized (^{Poulin & Morand, 2000}). Parasites are among the most common organisms and represent various members of all the biological communities (^{Hoberg & Kutz, 2013}), being extremely important in ecological and evolutionary processes (^{Gómez & Nichols, 2013}). Birds are hosts of a variety of parasites, among which helminths are found with complex biological cycles, and most of the time birds act as definitive hosts (^{Crompton, 1997}).

Passer domesticus (Linnaeus, 1758) (Passeriformes: Passeridae) is a bird from Eurasia and North Africa, which was intentionally introduced to the Americas (^{Global Invasive Species Database, 2018}). In Brazil, it was introduced in 1906, for biological control of insects (^{Sick, 1997}). Currently, it is found dispersed throughout Brazil. It is a non-migratory, terricolous bird that adapts easily to the agricultural environment, urban and suburban, taking advantage of anthropogenic action, occupying built-up areas that serve for shelter and nesting (^{Major et al., 2004}).

The diversity of helminths associated with P. domesticus was studied in the USA (^{Cooper & Crites, 1974}; ^{Hamer & Muzzall, 2013}; ^{Hopkins & Wheaton, 1935}; ^{Kintner, 1938}; ^{Koch & Huizinga, 1971}), in Brazil (^{Brasil & Amato, 1992}; ^{Calegaro-Marques & Amato, 2010a}) and in Europe (^{Illescas-Gomez & Lopez-Roman, 1980}; ^{Joszt, 1962}; ^{Ozmen et al., 2013}; ^{Sciumilo, 1963}). However, in spite of being a synanthropic bird with wide geographic distribution and found in several environments, there are few helminthological studies in different habitats, where the birds were introduced.

Parasitological studies of introduced host species are important, because these generally have their parasitic fauna reduced, and may contain only half of the richness found in native species, although they may acquire new parasites. This reduction may favor the population growth of invasive species and give them a competitive advantage over endemic species (^{Calegaro-Marques & Amato, 2010a}). However, the sparrow has the potential to transport invasive species (vector), including important pathogens and parasites that impact biodiversity, economy and public health, causing damage to the native fauna throughout its geographic distribution (^{Conabio, 2017}).

In this context, the study aimed to identify the species of helminth parasites of P. domesticus and to analyze the infection rates in relation to sex, body mass and total length of hosts, coming from an urban área of Rio Grande do Sul state, extreme southern of Brazil.

Material and methods

One hundred specimens [90 adults (52 males: 38 females), 9 juveniles (7 males: 2 females) and 1 indeterminate juvenile] of P. domesticus were captured with the use of mist nets (30 mm mesh), in 13 locations (squares, gardens of private properties and wasteland), in an urban area of Pelotas city, Rio Grande do Sul, Brazil, between March 2016 and February 2018. The capture, transportation and euthanasia of birds was licensed by Instituto Chico Mendes de Conservação da Biodiversidade (ICMBio nº 51118-3) and approved by the Comissão de Ética em Experimentação Animal at Universidade Federal de Pelotas (CEEA/UFPel nº 4915).

After being transported in an appropriate cage to UFPel’s Parasitology Laboratory, each specimen was weighed and measured, and the information recorded was: body mass and total body length, sex and age (adult and/or young). Thereafter, the hosts were euthanized separately by administration of a overdose of inhalational anesthetic Isoflurane as recommended by the Resolution nº 1000 of May 2012 of Conselho Federal de Medicina Veterinária (^{CFMV, 2012}). Subsequently, the birds were individually packed in properly identified plastic bags and refrigerated at approximately 7 ºC until necropsy, that occurred within 2 days after capture.

During the necropsy, eyeball, oral cavity, nasal cavity, esophagus, proventriculus, gizzard, cecum, intestine, trachea, lungs, liver, gall bladder, kidneys, gonads and cloaca were examined. They were individualized in Petri plates containing physiological solution, opened and inspected separately under the stereomicroscope, along with the contents and mucous. The helminths were fixed in AFA (70% alcohol, 37% formalin and glacial acetic acid) and preserved in 70% alcohol, according to techniques recommended by ^{Amato and Amato (2010)}.

For identification, helminths from Nematoda were clarified in Amann’s lactophenol, studied in temporary preparations and identified according to ^{Pereira and Vaz (1933)}, ^{Anderson and Bain (2009)}, and ^{Bartmann and Amato (2009)}. The parasites belonging to Trematoda and Cestoda and to Acanthocephala were dyed with Langeron Carmine or Delafiled Hematoxylin and individually set on permanent blades with Canada balsam (^{Amato & Amato, 2010}). Identifications were made according to ^{Freitas (1951)}, ^{Kanev et al. (2002)}, ^{Monteiro et al. (2007)}, ^{Lotz and Font (2008)}, and ^{Jones (2008)} for Trematoda; ^{Kintner (1938)} for Cestoda; and ^{Van Cleave (1916)} for Acanthocephala.

The parasitological parameters of prevalence (P%), mean abundance (MA) and mean intensity of infection (MII) were calculated according to ^{Bush et al. (1997)}. Helminth infections among male and female hosts, independent of sexual maturity stage, were compared through prevalence by Chi-square test (χ²) and the mean intensity of infection by t-test via “bootstrap” (BC_a p < 0.05) in Quantitative Parasitology 3.0 program (^{Rózsa et al., 2000}). In order to verify the existence of a correlation between helminth abundance and body mass, such as the total length of the hosts, a regression analysis was performed (RA) according to the model y = a+bx, as well as determination coefficient (r ²), whose limit is ≥ 0 or ≤ 1, and Pearson’s correlation coefficient (r), whose limit is ≥ -1 or ≤ 1 (^{Mukaka, 2012}). A nestling host was disregarded for this analysis. Regression analysis and Chi-square test, as well as the t-test were performed for helminths that presented a prevalence greater than or equal to 10% (^{Bush et al., 1990}).

Vouchers were deposited in Coleção Helmintológica do Instituto Oswaldo Cruz - CHIOC (numbers 40074a-f; 40075 - 40080a-b - 40086) from Rio de Janeiro, and Coleção de Helmintos do Laboratório de Parasitologia de Animais Silvestres - CHLAPASIL (numbers 759 - 778) at Departamento de Microbiologia e Parasitologia, Instituto de Biologia, Universidade Federal de Pelotas, Brazil.

Results

Among the 100 specimens of P. domesticus examined, 40 were parasitized by at least 1 helminth taxon. Among the parasitized birds, 67.5% (n = 27) were male (4 juveniles) and 32.5% (n = 13) were females (1 juvenile).

The helminth fauna of P. domesticus was composed of Synhimantus (Dispharynx) nasuta (Rudolphi, 1819) (Nematoda: Acuariidae) and Aproctella sp. (Nematoda: Onchocercidae); Prosthogonimus ovatus (Rudolphi, 1803) (Digenea: Prosthogonimidae), Eumegacetes sp. (Digenea: Eumegacetidae) and Tanaisia zarudnyi (Skrjabin, 1924) (Digenea: Eucotylidae); Choanotaenia passerina (Fuhrmann, 1907) (Cestoda: Dilepididae), and Mediorhynchus sp. (Acanthocephala: Gigantorhynchidae).

Cestoda was the most prevalent group, occurring in 26% of the hosts, followed by Trematoda with 13%. Nematoda and Acanthocephala occurred in only 2% of the birds. Most helminths were found in the gastrointestinal system, however, 1 species was found parasitizing the kidneys of the hosts. Found helminths and their respective infection sites and parasitological parameters are presented in tables 1 and 2.

Choanotaenia passerina presented a higher prevalence (26%), where as T. zarudnyi occurred with higher mean intensity of infection (96 helminths/host). Two species, P. ovatus and Eumegacetes sp., were found parasitizing the cloaca of P. domesticus, both with low infection rates (Table 1). Co-infection by these 2 digenetics occurred in a single host, which presented 1 helminth of each species. The remaining helminths found showed low infection rates (Table 1).

Males were parasitized by 6 taxa, while females were parasitized by 4 taxa. Prosthogonimus ovatus, T. zarudnyi and C. passerina occurred in both genders (Table 2). The prevalence (P%) and mean intensity of infection (MII) by C. passerina in male hosts (P% = 27.1%, MII = 4.25 helminths/host) and females (P% = 25%, MII = 2.9 helminths/host), independent of the maturity stage, did not present a significant difference (p > 0.05).

The correlations among the abundance of C. passerina, body mass (grams) and total length (millimeters) of the hosts showed low magnitude. It was not possible to identify functional relationship among variables, because Pearson’s correlation coefficient (r) presented positive values close to zero (Fig. 1).

Figure 1 Dispersal abundance pattern of Choanotaenia passerina (Fuhrmann, 1907) (Cestoda: Dilepididae) in relation to the body mass (g) and to the total length of hosts (mm) belonging to the Passer domesticus (Linnaeus, 1758) (Passeriformes: Passeridae) from urban area of Pelotas, Rio Grande do Sul, Brazil. 

Discussion

The fauna of helminths found in P. domesticus in this study is similar to records made in other regions of Brazil (^{Brasil & Amato, 1992}; ^{Calegaro-Marques & Amato, 2010a}; ^{Freitas, 1951}), as well as in the USA (^{Cooper & Crites, 1974}; ^{Hopkins & Wheaton, 1935}; ^{Kintner, 1938}) and in Europe (^{Joszt, 1962}).

Choanotaenia passerina is part of the original distribution of the helminth assembly of P. domesticus, as there are records of their occurrence in sparrows from various locations in Europe (^{Illescas-Gomez & Lopez-Roman, 1980}; ^{Joszt, 1962}; ^{Sciumilo, 1963}) and North America (^{Hopkins & Wheaton, 1935}; ^{Kintner, 1938}; ^{Stunkard & Milford, 1937}). Ever since, C. passerina was the only species found in all regions where helminth fauna of sparrows was studied (^{Calegaro-Marques & Amato, 2010a}). In studies conducted in Brazil, C. passerina was the most prevalente species in Rio de Janeiro (21.1% of 142 sparrows) (^{Brasil & Amato, 1992}) and in Porto Alegre (10% of 160 birds) (^{Calegaro-Marques & Amato, 2010a}), with mean infection intensity of 2.96 and 4.69, respectively. These results corroborate the parasitism of this cestode observed in P. domesticus in the region of the present study. This fact can be explained by the high association of P. domesticus and house flies (Musca domestica Linnaeus, 1758) (intermediate hosts) with humans, since the use of human food residues by sparrows may be related to their infection by this cestoid, once they are constantly preying on domestic flies, which feed on decaying organic matter present in the waste (^{Yamaguti, 1959}).

Tanaisia zarudnyi was described in Passer monatanus (Linnaeus, 1758) in Turkestan, Central Asia (^{Byrd & Denton, 1950}; ^{Freitas, 1951}). The species was cited in Brazil in 1935, parasitizing P. domesticus, however the location of registration was not specified (^{Freitas, 1951}). In American continet, T. zarudnyi was also recorded in several Passeriformes in Texas (USA) (^{Byrd & Denton, 1950}). The records of T. zarudnyi are related to taxonomic studies, with no data on parasitological indices. Another species from the same group, Tanaisia inopina (= Tamerlania inopina) (^{Freitas, 1951}) was reported in P. domesticus in Rio de Janeiro and Rio Grande do Sul, with prevalences similar to the one found in the present study, for T. zarudnyi. However, the mean infection intensity was lower, ranging from 12.47 helminths/host (^{Brasil & Amato, 1992}) and 7 helminths/host (^{Calegaro-Marques & Amato, 2010a}). The species of Tanaisia Skrjabin, 1924, may use as intermediate hosts, terrestrial gastropods molluscs, which must be ingested by birds for infection with the metacercariae (^{Ahmad & Gabrion, 1975}). The low prevalence of T. inopina and T. zarudnyi in P. domesticus suggest a low infection by metacercariae, indicating that possibly gastropod moluscs are not a preferred item in the diet of this granivorous passeriform. This hypothesis corroborates the information about the diet of the species, which feeds mainly on seeds in the winter and insects in the spring (^{Sánchez-Aguado, 1986}).

According to ^{Monteiro et al. (2007)}, P. ovatus has records parasitizing a wide variety of hosts around the world (poultry and wild birds). In Rio Grande do Sul, the species was reported in aquatic birds with the respective values of prevalence and mean intensity of infection in Dendrocygna bicolor (Vieillot, 1816) (n = 33), P = 3% and MII = 1 helminth/host; Netta peposaca (Vieillot, 1816) (n = 20), P = 15% and MII = 4.3 helminths/host (Anseriformes: Anatidae) and Phalacrocorax brasilianus (Gmelin, 1789) (Suliformes: Phalacrocoracidae) (n = 47), P = 2.1% and MII = 1 helminth/host (^{Monteiro et al., 2007}). Prosthogonimus ovatus was recorded in the southern region of the state, parasitizing Passeriformes: Paroaria coronata (Miller, 1776) (Thraupidae) (n = 40) with P = 7.5% and MII = 3 helminths/host (^{Mascarenhas et al., 2009}); Molothrus bonariensis (Gmelin, 1789) (Icteridae) (n = 5) with P = 20% and MII = 5 helminths/ host (^{Bernardon et al., 2016}); and Chrysomus ruficapillus (Vieillot, 1819) (Icteridae) (n = 122) with P = 14.75% and MII = 1.38 helminths/host (^{Bernardon et al., 2018}). The infection of the birds occurs by the ingestion of young or adult dragonflies (second intermediate hosts) containing the encrusted metacercariae; the first intermediate host is a mollusk (^{Boddeke, 1960}).

The life cycle of helminths belonging to Eumegacetes Looss, 1900, involves Odonata larvae (dragonflies) (^{Pinto & Melo, 2013}). They are parasites of the intestinal tract, including rectum, cloaca and renal system of the birds (^{Lotz & Font, 2008}). In Rio Grande do Sul, Eumegacetes sp. was mentioned in P. domesticus (^{Calegaro-Marques & Amato, 2010a}) and in C. ruficapillus (^{Bernardon et al., 2018}). The low infection rates in these Passeriformes corroborate those found in the present study.

Synhimantus (Dispharynx) nasuta was described by Rudolphi (1819) in the proventriculus of P. domesticus in Austria (Europe), and it is a parasite commonly found in the proventriculus and gizzard of several species of birds (aquatic and terrestrial) in different continents (^{Goble & Kutz, 1945}). Only in Rio Grande do Sul, this nematode was mentioned parasitizing species of Passeriformes, Cuculiformes, Columbiformes and Charadriiformes. The infection rates of S. (D.) nasuta in Passeriformes from the same geographic region resemble those recorded in the present study, the nematode was found in P. coronata (n = 40) with P = 5% and MII = 5 helminths/host (^{Mascarenhas et al., 2009}); Pitangus sulphuratus (Linnaeus, 1766) (Tyramidae) (n = 78) with P = 3.85% and MII = 2.66 helminths/host (^{Mendes, 2011}); and M. bonariensis (Gmelin, 1789) (Icteridae) (n = 5) with P = 20% and MII = 2 helminths/host (^{Bernardon et al., 2016}). In P. domesticus (n = 160), from the metropolitan area of Porto Alegre, a mean infection intensity of 18 helminths/host was observed (^{Calegaro-Marques & Amato, 2010a}), higher than that registered in this host in the southern region of the state. Similarly, ^{Coimbra et al. (2009)} observed higher mean infection intensity in Columbina picui (Temminck, 1813) (Columbidae) (n = 34), in with MII was 19.5 helminths/ host. In Cuculiformes, Guira guira (Gmelin, 1788) (n = 120) and Crotophaga ani Linnaeus, 1758 (Cuculidae) (n = 120), as well as in the Charadriiforme Vanellus chilensis (Molina, 1782) (Charadriidae) (n = 28), the prevalence of S. (D.) nasuta was higher than that registered in P. domesticus, ranging from 26.6% to 28.6% and the MII from 5.1 to 14.38 helminths/host (^{Avancini, 2009}; ^{Bartmann & Amato, 2009}). The divergent parameters among the different families of birds may be related to the food habits of each species, since this nematode utilizes terrestrial crustaceans as intermediate hosts (^{Permin & Hansen, 1998}), which are not a preferred item in the diet of P. domesticus.

According to ^{Pereira and Vaz (1933)}, there are 2 species of Aproctella (Cram, 1931) in Passeriformes in Brazil, A. carinii (^{Pereira & Vaz, 1933}) and A. stoddardi (Cram, 1931). In Rio Grande do Sul, A. carinii was reported in P. coronata (^{Mascarenhas et al., 2009}); A. stoddardi was found in Turdus rufiventris (Vieillot, 1818) (Passeriformes: Turdidae) (^{Calegaro-Marques & Amato, 2010b}), and Aproctella sp. in P. sulphuratus (^{Mendes, 2011}). In these passerines the infection rates were higher than those found in P. domesticus. This filarid has as host Culicidae mosquitoes, the microfilariae develop in the thoracic muscles and hemocele of the insect (^{Bain et al., 1981}).

The species of Mediorhynchus^{Van Cleave, 1916}, are common in terrestrial birds (^{Smales, 2002}). Acanthocephala have complex biological cycles, where the infection of the definitive hosts (vertebrate) occurs through the ingestion of arthropods (invertebrate intermediate hosts) containing infective larvae (cystacants) (^{Moore, 1962}). In Brazil, M. papillosus Van Cleave, 1916 was registered for the first time in 1.4% of 142 sparrows (^{Brasil & Amato, 1992}). In other Passeriformes from the same region of study, the low prevalence of Mediorhynchus species resemble those found in P. domesticus: ^{Mascarenhas et al. (2009)} obtained a prevalence of 5% of Mediorhynchus sp. in P. coronata (n = 40); and ^{Bernardon et al. (2018)}, P = 2.46% of M. micracanthus (Rudolphi, 1819) in C. ruficapillus (n = 122).

In the present study, there was no significant difference in the prevalence and intensity of infection by C. passerina in relation to the sexual gender of the hosts. Similar results were found by ^{Brasil and Amato (1992)} and ^{Calegaro-Marques and Amato (2010 a}, ^b), indicating that male and female sparrows enjoy the same ecological niche, with no preference for types of food. These results contrast the hypothesis that some authors defend, which suggests that the rates of helminth infection in different taxons (fish, birds and mammals) are generally higher in male hosts compared to females due to immunological, genetic and behavioral differences (^{Klein, 2004}; ^{Poulin, 1996}; ^{Reimchen & Nosil, 2001}; ^{Zuk & McKean, 1996}; ^{Zuk & Stoehr, 2010}).

In addition, the abundance of C. passerina in relation to the body mass and the total length of the studied hosts, showed that there was no functional correlation, that is, the amount of this cestoid does not vary as the weight and the size of the birds increase. Divergent results were found by ^{Monteiro et al. (2011)}, in which 5 of the 20 species of helminths found in P. brasilianus had their infection rates influenced by the variables weight, gender and sexual maturity status of hosts. According to ^{Poulin (1996)}, such variation may be related to territorialism and to social interaction of birds.

Generally, we could observe that the helminth fauna and their respective rates of infection in P. domesticus in the present study corroborates other studies around the world and may be related to the feeding and synanthropic habits of the host species. Because it is a wild bird with a wide world distribution, it is necessary to study the parasitic fauna of this passeriform, since its dispersion favors a greater exposure to new parasites, as well as a dissemination of new parasites in new geographical areas, affecting native fauna; even though the parasite richness of introduced host species may be reduced and the period since its introduction also influences the composition of parasite communities (^{Calegaro-Marques & Amato, 2010a}).

The fauna of helminths and their infection rates in Passer domesticus in the southern region of Rio Grande do Sul is similar to that registered in this host in other regions. However, a filarid belonging to Aproctella is recorded for the first time parasitizing this host and the occurrence of Prosthogonimus ovatus for the first time in P. domesticus in Brazil. Also recorded are the infection rates of Tanaisia zarudnyi in P. domesticus, since the only report of the digenetic in this host species in Brazil did not address aspects related to parasitological parameters. The sexual gender of the hosts, as well as the body mass and total length of the birds did not influence the infections by the cestoid Choanotaenia passerina.