Helminths of introduced house sparrows (Passer domesticus) in Brazil: does population age affect parasite richness?

Species introductions have altered host and parasite diversity throughout the world. In the case of introduced hosts, population age appears to be a good predictor of parasite richness. Habitat alteration is another variable that may impact host-parasite interactions by affecting the availability of intermediate hosts. The house sparrow (Passer domesticus (Linnaeus, 1758)) is a good model to test these predictions. It was introduced in several parts of the world and can be found across rural-urban gradients. A total of 160 house sparrows from Porto Alegre, state of Rio Grande do Sul, Brazil, were necropsied. Thirty house sparrows (19 %) were parasitized with at least one out of five helminth species (Digenea: Tamerlania inopina Freitas, 1951 and Eumegacetes sp.; Eucestoda: Choanotaenia passerina (Fuhrmann, 1907) Fuhrmann, 1932; Nematoda: Dispharynx nasuta (Rudolphi, 1819) Stiles & Hassall, 1920 and Cardiofilaria pavlovskyi Strom, 1937). Overall, there was no difference in prevalence and intensity of infection of any parasite species, parasite richness and community diversity between adult males and females and adults and juveniles. The number of infected sparrows among seasons, the richness of helminths and the abundance of species were also similar between rural and urban landscapes. Only the prevalence of C. passerina varied seasonally (p=0.0007). A decrease in the number of parasite species from the original range of P. domesticus (13) to its port of entrance in Brazil, the city of Rio de Janeiro (nine), to Porto Alegre (five) is compatible with the hypothesis that host population age is a good predictor of parasite richness.

A large number of species has been displaced from their original ranges as a consequence of striking manmade environmental changes, especially during the last two centuries.The intentional and accidental introduction and the expansion of the distribution of species after the break-down of biogeographic barriers by humans have altered host and parasite diversity throughout the world (POULIN & MORAND, 2004;TARASCHEWSKI, 2006).Although introduced host species may acquire new parasites in their new ranges, their parasitic fauna is often reduced, and may contain only about half the richness found in native species (HAIR & FORRESTER, 1970;TORCHIN et al., 2003;POULIN & MORAND, 2004).This reduction may favour the population growth of invasive species (TORCHIN et al., 2003) and give them a competitive advantage against native species (PRENTER et al., 2004).The time since the introduction also plays an important role in the composition of parasite communities.EBERT et al. (2001), for example, observed that the age of Daphnia magna Straus, 1820 populations is the best predictor of their parasite richness.
The qualitative reduction of parasites seen in introduced hosts takes place because several parasite species are lost when (a) individuals in the founding population, a sample of the original population, are not infected (this is particularly relevant for less prevalent species), (b) some parasites do not find their intermediate hosts or the interaction between intermediate and definitive hosts is compromised or missing in the new area, (c) native parasite species are unable to adapt to exotic hosts due to their high host specificity and (d) the environmental conditions required for completing their cycles are lacking (HAIR & FORRESTER, 1970;TORCHIN et al., 2003).
Habitat alteration is particularly strong in urban landscapes, where vegetation structure and the diversity and abundance of animals are changed radically compared to natural landscapes (MARZLUFF, 2001;MCKINNEY, 2002;MILLER & HOBBS, 2002).The high level of pollution of some urban environments may also promote changes in parasite communities by decreasing the efficiency of the immune system of hosts (COMBES, 2001).Albeit several native host or parasite species cope well with urban landscapes, most of them do not adapt to the new environmental conditions and go locally extinct (MCKINNEY, 2002).Therefore, despite the high resource availability capable of sustaining high animal densities in towns, local diversity tends to decrease with increasing urbanization (MCDONNELL & PICKETT, 1990).
The house sparrow Passer domesticus (Linnaeus, 1758) is a good model for testing the influence of introduction latency and urbanization on a species parasite richness.It is native to Eurasia and northern Africa, but currently is found well established in the Americas (LEVER, 1987).It is also highly adaptable to urban landscapes.Whereas SICK (1997) states house sparrows arrived in Brazil in 1906 through the city of Rio de Janeiro, EFE et al. (2001) believe the species was already introduced in the country in the 18 th century.Irrespective of the actual date of introduction of house sparrows in Brazil, their high degree of adaptation to urban environments allowed them to spread throughout the Brazilian territory during the last century (EFE et al., 2001).Passer domesticus is host to 13 helminth species (eight cestodes, four digeneans and one nematode) in its original range (MEGGITT, 1916;JOSZT, 1962;BAUGH & SAXENA, 1975, 1976;MARTINEZ et al., 1977;ILLESCAS-GOMEZ & LOPEZ-ROMAN, 1980).In Brazil, nine helminth species (five digeneans, two nematodes, one cestode and one acanthocephalan) have been identified at the species port of entrance, the city of Rio de Janeiro (AMATO & BRASIL, 1990;BRASIL & AMATO, 1992).
In this paper we describe the helminth fauna of P. domesticus in the metropolitan region of Porto Alegre, southern Brazil, where it was first recorded around 1920 (FONTANA, 2005), and test the prediction that the richness of its helminth community is lower than that observed in populations living in its original distribution and in the city of Rio de Janeiro.In addition, we estimate the structure of its helminth community and test whether host sex and age, season and landscape (rural vs. urban) affect helminth richness and composition.

MATERIAL AND METHODS
A total of 160 house sparrows were collected using mist nets in 10 sites in the metropolitan region of Porto Alegre, state of Rio Grande do Sul, Brazil, between March 2003 andMarch 2006.The technique for euthanasia involved an overdose with gaseous anesthetic (GAUNT & ORING, 1999) Because habitat heterogeneity varied widely among sites, five environmental types were quantified in an area with a radius of 564 m around each trapping location (=1 km 2 ): buildings, wood, grassland, bare soil and water.This quantification involved orbital image processing and treatment routines using the software Idrisi Andes 15.0 for Windows.Collection sites were classified into urban and rural landscapes based on their degree of urbanization, that is, their area covered by buildings.Sites <50 % urbanized were treated as rural, whereas sites >63 % urbanized were treated as urban.About half house sparrows were collected in each landscape type.
Prevalence, mean intensity of infection, mean abundance and range of intensity of infection were calculated following BUSH et al. (1997).In addition, each helminth species was classified based on its importance value (I) as suggested by THUL et al. (1985) as dominant (I≥1.0),co-dominant (0.01≤I<1), subordinate (0<I<0.01)and unsuccessful pioneer (I=0).Helminth species richness was evaluated using a sampling sufficiency curve (SANTOS, 2003).Shannon's diversity index (log e ) of the host species helminth community, as well as of adult male and female sparrows, was also calculated (BROWER & ZAR, 1984).
The qualitative similarity of the parasite communities of adult males and females was estimated based on Jaccard similarity index, whereas the quantitative similarity was evaluated by the Morisita-Horn similarity index (MAGURRAN, 1988).The prevalence of each helminth species in the parasite communities of adult and juvenile sparrows (identified based on the presence or absence of the bursa of Fabricius, respectively; PROCTOR & LYNCH, 1993), and of adult male and female individuals were compared with a G-test with Yates' correction, while parasite intensity of infection were compared with a Mann-Whitney test.In the absence of differences between classes, data were pooled for further analyses.
The climate of the study region is subtropical humid, CFA type in Koeppen's classification, with the four seasons well defined (LIVI, 1998).Fourty house sparrows were collected in each season, evenly distributed between urban and rural landscapes and years.The prevalence and intensity of infection for each helminth species were compared among seasons, respectively, with the G-test and the Kruskal-Wallis analysis of variance.The Student-Newman-Keuls posthoc test was used to determine which pairs of seasons differed statistically when appropriate.Parasite richness and abundance of hosts living in urban and rural landscapes were compared with a Kruskal-Wallis analysis of variance.
Variables with sample sizes ≥20 were tested for normality with a D'Agostino Pearson test, whereas those variables whose sample sizes fell between 10 and 19 were tested with a D'Agostino test (AYRES et al., 2005).Variables with a normal distribution were tested with the parametric Student t test when variances were similar, and with a Z test when variances differed.In the absence of a normal distribution, and when data could not be normalized with transformation, non-parametric tests were used.Unless otherwise stated a significance level of 5 % was used for all tests.When multiple tests were performed on the same variable, the significance level was adjusted following LEIGH & JUNGERS (1994).Tests were performed using BioEstat 4.0 (AYRES et al., 2005) and Systat 5.0 (WILKINSON, 1990).

RESULTS
Twenty nine house sparrows (18.1 %) were parasitized with a single helminth species and one (0.6 %) was parasitized with two species out of 160 necropsied birds (mean richness = 0.19 helminth species per host).A total of 143 helminth individuals belonging to five species (digeneans Tamerlania inopina (Freitas, 1951) (Fuhrmann, 1907) Fuhrmann, 1932) were collected (mean intensity of infection = 0.90 helminths per host).Choanotaenia passerina showed the highest prevalence, range of intensity of infection and mean abundance (Tab.I).On the other hand, Eumegacetes sp. was found in a single juvenile individual, whereas D. nasuta was found in a single adult male.The sufficiency curve stabilized after the 87 th necropsy when the fifth helminth species of this low diversity community (Shannon's H'=1.235) was found.Four species were classified as dominant (C.passerina, I=78.95; C. pavlovskyi, I=12.43;T. inopina, I=7.37; and D. nasuta, I=1.18) and one as co-dominant (Eumegacetes sp., I=0.07).

DISCUSSION
The helminth parasite fauna of P. domesticus living in the metropolitan region of Porto Alegre reached sampling sufficiency when the fifth species was found after about half the necropsies had been completed.Although rarer species would likely be found with increasing sample size, this richness represents a reliable estimate of the local helminth fauna of P. domesticus.Therefore, there is a parasite species richness reduction from its original distribution (13 species; MEGGITT, 1916;JOSZT, 1962;BAUGH & SAXENA, 1975, 1976;MARTINEZ et al., 1977;ILLESCAS-GOMEZ & LOPEZ-ROMAN, 1980) to Rio de Janeiro (9 species; AMATO & BRASIL, 1990;BRASIL & AMATO, 1992) to Porto Alegre (5 species; this study) that is compatible with the hypothesis that host population age is a good predictor of parasite richness (EBERT et al., 2001).The percentage of infected house sparrows showed the same pattern: 47 % in the original range (JOSZT, 1962), 34 % in Rio de Janeiro (AMATO & BRASIL, 1990;BRASIL & AMATO, 1992), and 19 % in Porto Alegre (this study).Three helminth species found in the Porto Alegre population were present in Rio de Janeiro (T.inopina, C. passerina, and D. nasuta), but only C. passerina was also found in the original distribution of house sparrows (Tab.III).
Most parasites of P. domesticus present a heteroxen cycle.Therefore, house sparrows get infected by eating invertebrate intermediate hosts such as snails, isopodes and flies.Consequently, at least three hypotheses may help explain the overall low prevalence observed in this study: intermediate hosts present a naturally low infection rate with these parasites, there is a low availability of intermediate hosts, and the consumption of intermediate prey hosts by house sparrows is low.The available data do not allow to test these non-mutually exclusive hypotheses.On the other hand, the filariid nematode C. pavlovskyi shows a different cycle, does not present a high host specificity, and is transmitted by vectors directly to several bird species (ANDERSON, 1992).
The relationship between the diet of a species and its parasite fauna is well exemplified by house sparrows infection with C. passerina, the most characteristic species of P. domesticus helminth community both in Rio de Janeiro (BRASIL & AMATO, 1992) and Porto Alegre (this study).House sparrows use of domestic garbage as a food source is likely to be directly linked to their infection with this cestode species, whose intermediate hosts are domestic flies (Musca domestica Linnaeus, 1758) that feed on the decomposing organic matter found in human waste (YAMAGUTI, 1958).Therefore, the high association of both house sparrows and domestic flies with humans helps explain why C. passerina is the only species found in all regions where the parasite fauna of P. domesticus has been studied.Because C. passerina presents a high especificity to P. domesticus as definitive host, its geographic distribution probably matches the range of house sparrows from Europe, northern Africa and part of Asia to North America, South America, and Australia (BRASIL & AMATO, 1992).
The highest prevalence of C. passerina in the  (Travassos, 1914) Travassos, 1915 X spring may be related to seasonal differences in the availability of domestic flies, their degree of infection or their importance in the diet of house sparrows.
Considering the cysticercoid of C. passerina takes about seven weeks to develop into an adult helminth, as observed in Choanotaenia infundibulum Linnaeus, 1758(REID & ACKERT, 1937), it is possible to estimate the infection of house sparrows is higher at the end of the winter and the beginning of the spring.Although domestic flies mature throughout the year in Porto Alegre, there are seasonal differences in their ontogenetic development, such as an increase in the duration of prepupa and pupa stages during the coldest months (TORRES et al., 2002), which are likely to result in a lower availability of domestic flies at the time of higher C. passerina prevalence.Therefore, differences in domestic fly availability are unlikely to explain seasonal differences in the prevalence of C. passerina.It is possible, then, that domestic flies are a more important food item for house sparrows at coldest times of the year when the availability of other prey is lower, or that they are more easily captured under lower ambient temperatures.
The overall low helminth prevalence in house sparrows is compatible with their highly granivorous diet complemented with human food remains and prey (SICK, 1997).The likely lower importance of prey in the host habitual diet helps explain, for example, the low prevalence of D. nasuta in the Brazilian populations.Whereas BRASIL & AMATO (1992) observed only six out of 142 house sparrows from Rio de Janeiro infected with this acuariid nematode, only one individual was infected in the Porto Alegre population.Isopodes, orthopterans, coleopterans, and diplopods serve as intermediate hosts to D. nasuta, a parasite found in both aquatic and terrestrial birds (ANDERSON, 1992).
An understanding of the intermediate hosts involved in the life cycle of a parasite also sheds light into the niche overlap and partitioning between-and within-species.In this sense, the high similarity of the helminth communities of adult male and female house sparrows supports the contention that there is no difference in the animal portion of their diets.
Knowledge on the behaviour, ecology, and environmental requirements of hosts and parasites are also important for evaluating the role that the landscape plays in determining the helminth fauna of a species.Despite the fact that the urbanization changes drastically the environment and may have profound influences for both hosts and parasites, such as population density declines particularly for species with complex life cycles (LAFFERTY & KURIS, 2005), no differences in parasite richness and species abundances were found in the present study between house sparrows living in rural and urban landscapes.The previously mentioned granivorous-omnivorous diet and the high association of house sparrows with human settlements may account for this lack of difference.Therefore, it is likely that host diet is similar in rural and urban landscapes.The fact that no house sparrow was captured in trapping sites containing <40 % urbanization (seven sites ranging from <1 to 34 % urbanization) and the general low parasite prevalence support the idea that grains and human food remains are responsible for the bulk of the diet of P. domesticus in both landscapes.
Future studies on the parasite fauna of P. domesticus in areas where it was introduced more recently are needed to confirm the hypothesis that the age of a population is a good predictor of its parasite richness.In addition, as stated by COMBES (2001), studies on the parasite-environment relationship offer a challenge to parasitological research and the landscape influence on parasite community structure needs to be enlightened for hosts belonging to different guilds.Finally, a more thoroughly comprehension of this multi-species ecological interaction will require research focusing on both definitive and intermediate hosts, their relationships, densities, and interactions with parasite species.
In this research was found a decrease in parasite species richness from its original distribution to Rio de Janeiro to Porto Alegre that is compatible with the contention host population age is a good predictor of parasite richness.The percentage of infected house sparrows showed the same pattern.No differences in parasite richness and species abundances were found between house sparrows living in rural and urban landscapes, despite the fact that the urbanization changes drastically the environment and may have profound influences for both hosts and parasites.The previously mentioned granivorous-omnivorous diet and the high association of house sparrows with human settlements may account for this lack of difference.Therefore, it is likely that the host diet is similar in rural and urban landscapes.The high similarity of the helminth communities of adult male and female house sparrows supports the contention that there is no difference in the animal portion of their diets.

Table I .
Helminth prevalence, range of intensity, mean intensity of infection and mean abundance in house sparrows Passer domesticus (Linnaeus, 1758) introduced in the metropolitan region of Porto Alegre, Rio Grande do Sul, Brazil (n=160 necropsied birds).

Table III .
List of parasite helminth species of Passer domesticus (Linnaeus, 1758) found in its original range, in the city of Rio de Janeiro, state of Rio de Janeiro, and in the metropolitan region of Porto Alegre, state of Rio Grande do Sul, Brazil.