versión On-line ISSN 2007-8706
Rev. Mex. Biodiv. vol.81 no.3 México dic. 2010
Parasites as secret files of the trophic interactions of hosts: the case of the rufousbellied thrush
Los parásitos como archivos secretos en las interacciones tróficas con sus hospederos: el caso del Zorzal Colorado
Cláudia CalegaroMarques1* and Suzana B. Amato2
1 Departamento de Zoologia, Instituto de Biociências, Universidade Federal do Rio Grande do Sul, Av. Bento Gonçalves, 9500, Pd. 43435, Sala 202, Porto Alegre, RS, Brazil. *Correspondent: firstname.lastname@example.org
2 Laboratório de Helmintologia, Departamento de Zoologia, Instituto de Biociências, Universidade Federal do Rio Grande do Sul, Av. Bento Gonçalves, 9500, Pd. 43435, Sala 209, Porto Alegre, RS, Brazil
Recibido: 14 octubre 2009
Aceptado: 25 marzo 2010
Helminths with heteroxenous cycles provide clues for the trophic relationships of definitive hosts, representing important sources of information for assessing niche overlap between males and females of nondimorphic species. We necropsied 151 rufousbellied thrushes (Turdus rufiventris) captured in a metropolitan region in southern Brazil to analyze whether the structure of parasite communities is influenced by host sex or age. Most thrushes (93%) were parasitized by at least 1 species. The helminth community of Turdus rufiventris was composed of 15 species with prevalences from <1% to 60%. Although the prevalence of Conspicuum conspicuum, Microtetrameres pusilla and Aproctella stoddardi was higher in adults, Syngamus trachea was more prevalent in juveniles. Adults showed greater species richness of parasites than juveniles, probably as a consequence of an increase in the opportunities of infection with a larger set of parasites with aging. Adult males and females presented similar species richness of helminths and quite similar communities, allowing us to conclude that they prey upon the same invertebrates, including earthworms, snails, isopods, millipedes, cockroaches and grasshoppers. Therefore, trophic niche overlap between adult males and females is greater than between adults and juveniles.
Key words: Turdus rufiventris, passeriform, helminth, diet, dimorphism.
Los helmintos que presentan ciclos heterogéneos proveen pistas importantes sobre las relaciones tróficas que mantienen con sus hospederos definitivos. Estas pistas son además importantes fuentes de información que permiten evaluar el sobrelapamiento de sus nichos cuando comparamos machos y hembras en especies no dimórficas. Así, se practicaron necropsias en 151 zorzales colorados (Turdus rufiventris) que fueron capturados en una región metropolitana al sureste de Brasil, a fin de analizar de qué manera la estructura de la comunidad de parásitos podría estar influenciada por la edad o sexo del hospedero. La mayoría de los zorzales (93%) fueron parasitados por al menos 1 especie. La comunidad de helmintos de Turdus rufiventris estuvo compuesta por 15 especies, con prevalencias entre 1% a 60%. Aunque la prevalencia de Conspicuum conspicuum, Microtetrameres pusilla y Aproctella stoddardi fue más alta en adultos, Syngamus trachea tuvo una mayor prevalencia en juveniles. Los adultos mostraron una mayor riqueza de parásitos que los juveniles. Probablemente, ésto sea consecuencia de una mayor posibilidad de infectarse conforme avanza la edad de los individuos; sin embargo, machos y hembras adultos presentaron una riqueza similar en la concentración de helmintos en comunidades semejantes. Esto podría apoyar a concluir que podrían estar alimentándose del mismo tipo de invertebrados como son: lombrices, caracoles, isópodos, ciempiés, cucarachas y saltamontes. Concluimos que la sobreposición del nicho trófico es mas clara entre machos y hembras adultos que entre los juveniles.
Palabras clave: Turdus rufiventris, paseriforme, helmintos, dieta, dimorfismo.
Parasites are important players in the ecosystem, but our knowledge of this fascinating and significant biodiversity component is surprisingly poor (Windsor, 1997; McLaughlin, 2001; Hudson et al., 2006). Although actual global species richness for most higherlevel taxa or functional groups is unknown, Price (1980) suggests that there are more parasite species than freeliving ones. As a result, parasitism is the commonest interspecific interaction (Poulin and Morand, 2004). Furthermore, species richness of parasites will not be fully known until all hosts have been described and studied (Windsor, 1998).
In addition to the role played in ecosystems, parasites are important sources of data on host behavior and ecology, including trophic relationships. The complex life cycles of parasites may be integrated into intricate food webs and give us clues on food web structure and on the food preferences and foraging strategies of hosts (Marcogliese and Cone, 1997). Diet is a key factor in studies of avian biology and ecology and has been investigated via analysis of stomach contents, forced regurgitation and flushing, fecal samples and direct observation among others (Rosenberg and Cooper, 1990). Considering food digestion time ranges from 45 minutes to 6 hours in birds (Karasov, 1990), the most used method, the analysis of stomach contents, is often inefficient in identifying food remains found in the gut. Consequently, while studies based on gut contents only reflect the last hours of feeding prior to capture, helminths can stay for months or years within a bird host as evidence of longterm trophic relationships. Age and body size can affect the fauna of helminths of a host, revealing ontogenetic changes in feeding behavior (Marcogliese and Cone, 1997).
Therefore, helminths found in the gut and other organs open up a new dimension in the study of avian diet. Because a substantial number of helminths that parasitize birds have a heteroxenous cycle, transmission occurs when the bird (definitive host) preys on an intermediate host infected with the immature stage of the parasite. In this case, the finding of a helminth inside the body of a bird is evidence that the intermediate host belongs in its diet. As a consequence, the more we know about the helminth parasites of a species, the better we will solve its trophic jigsaw.
Several factors determine the structure of parasite communities. Bush (1990) considers the environment as the major determinant of the structure of parasite communities of birds through an influence on the survival and potential transmission of helminths that have direct life cycles or intermediate stages. However, Kennedy et al. (1986) suggest that these factors are related to host traits, such as the complexity of the digestive system, the amount and diversity of food items and host movement. Other factors that can play important roles in the pattern of distribution of helminths among species of hosts include environmental seasonality, and distribution, age, sex (Bush, 1990), and population density (Price, 1990) of the host. Among birds and mammals, for example, the sex of the host can affect parasitism (Isomursu et al., 2006). Many studies have shown that males carry heavier parasite loads than females (Poulin, 1996; Zuk and McKean, 1996; Schalk and Forbes, 1997; Robinson et al., 2008). Among mammals, this pattern is a product of life history differences between males and females: males tend to demand more energy and resources for growing, whereas females tend to show a greater investment in immunity. Thus, this male bias in parasitism among mammals is associated with sexual size dimorphism (Moore and Wilson, 2002). Among birds, the sex of the host influences parasitism both in species showing body size sexual dimorphism (Robinson et al., 2008) and those nondimorphic species (Isomursu et al., 2006). Sexbased differences in foraging strategy (Morse, 1990) influence the exposure of hosts to parasites transmitted through the food chain, and appear to be more important than physiological differences in determining male and female parasitism (Robinson et al., 2008).
The rufousbellied thrush (Turdus rufiventris Vieillot, 1818) is a nonsexually dimorphic passeriform. Male and female rufousbellied thrushes are visually indistinguishable, a characteristic that hampers sex comparisons in studies on the ecology and behavior based on field observations of unmarked and unsexed individuals. This bird is found in woodlands and on city streets and gardens, where it is welladapted to human contact (Efe et al., 2001; Fontana, 2001). In forests it often occupies the intermediate stratum of the canopy, whereas the ground is highly used in city gardens (Belton, 1994), where it feeds on fruits and invertebrates such as insects and earthworms (Efe et al., 2001; Fontana, 2001). This thrush is a resident species in the State of Rio Grande do Sul (hereafter RS), Brazil (Belton, 1976), and is a member of the avifauna of the city of Porto Alegre at least since the 1920's, when it used to be found in areas less populated by humans; currently, it is among the commonest species of urban birds and shows a more homogeneous pattern of city occupation (Fontana, 2005).
Passeriform birds are parasitized by trematodes, digeneans, cestodes, acanthocephalans and nematodes (Borgstede et al., 2000). Interspecific differences in the fauna of helminths are evidence of differences in habitat use, food preferences and resource partitioning and interactions with intermediate hosts (Ching, 1993). Turdus rufiventris is known to host only 5 helminth species: the digeneans Conspicuum conspicuum (Faria, 1912) Bhalerao, 1936 (Travassos et al., 1969), Lutztrema obliquum (Travassos, 1917) Travassos, 1941 (Travassos et al., 1969; Fabio and Ferreira, 1999) and Prosthogonimus sp. (Travassos et al., 1969) and the nematodes Tetrameres pusilla (Travassos, 1915) Chabaud, 1975 and Tetrameres sp. (Vicente et al., 1995).
In this paper we describe the structure of the helminth community of rufousbellied thrushes living in the metropolitan region of Porto Alegre, State of Rio Grande do Sul, Brazil, analyze whether sex and age influence the structure of the parasite community of individual hosts, and discuss what helminths reveal about host ecology and behavior.
Materials and methods
A total of 151 rufousbellied thrushes were collected using mist nets in the metropolitan region of Porto Alegre, RS (29o50'57"30o09'25"S, 50o01'20"51o18'45"W), Brazil, between March 2003 and March 2006. The technique for euthanasia involved an overdose with gaseous anesthetic (Gaunt and Oring, 1999). Necropsy of birds and processing of helminths follow Amato et al. (1991). Voucher specimens were deposited in the Coleção Helmintológica do Instituto Oswaldo Cruz (CHIOC), Rio de Janeiro, Brazil (see Table 1).
Sex identification was based on gonadal analysis during necropsy, whereas juveniles were identified by the presence of bursa of Fabricius, an organ that is atrophic in adults (Proctor and Lynch, 1993). All individuals were weighed with an accuracy of 1g using 60g Pesola© scales before necropsy.
Data on parasite infrapopulations were used to calculate prevalence, range and mean intensity of infection and mean abundance (Bush et al., 1997). In addition, helminths were classified based on their importance value (I) into dominant (I ≥ 1.0; species characteristic of the community), codominant (0.01 ≤ I < 1; contributes significantly to the community, but to a lesser degree than dominants), subordinate (0 < I < 0.01; uncommon and although it breeds and develops in the host, it does not contribute significantly to the community) or unsuccessful pioneer (I = 0; has access to the host, but does not develop or reproduce, contributing little to the community because it is characteristic of another host species) (Thul et al., 1985).
A species accumulation curve (Santos, 2003) was used to evaluate whether the observed species richness of helminths was representative of the actual fauna of helminths of rufousbellied thrushes. Shannon's index of diversity of the helminth community was calculated using the natural logarithm (loge) in the formula (Brower and Zar, 1984) and compared using the t test. The similarity of the parasite communities of adult males and females was assessed qualitatively using the Jaccard's index of similarity (Magurran, 1988), as performed by Brasil and Amato (1992), and quantitatively using the MorisitaHorn index of similarity (Magurran, 1988).
The prevalence and the intensity of infection of each helminth species was compared between adults and juveniles and between adult males and females. Data on prevalence were compared using the Gtest with Yates correction by organizing the number of positive and negative necropsies in each class into 2x2 contingency tables, whereas the intensity of infection was compared using the MannWhitney U test. Linear regression was applied to evaluate whether species richness of parasites (independent variable) compromises the health of hosts estimated by a proxy measure, body weight (dependent variable).
Variables with sample sizes ≥20 were tested for normality using a D'Agostino Pearson test, whereas those variables with sample sizes from 10 to 19 were tested using a D'Agostino test (Ayres et al., 2005). Variables with a normal distribution were tested using the parametric Student t test when variances were similar, and using a Z test when variances differed. In the absence of a normal distribution and when transformations were not capable of normalizing the data, nonparametric 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 and Jungers (1994). Tests were performed using BioEstat 4.0 (Ayres et al., 2005), Systat 5.0 (Wilkinson, 1990), and PAST 1.81 (Hammer et al., 2001).
A total of 140 out of the 151 necropsied rufousbellied thrushes (92.7%) were parasitized by at least 1 helminth species. The helminths recorded (N= 2 387 specimens) belonged to Nematoda (56%), Digenea (20%), Eucestoda (17%) and Acanthocephala (7%), showing a mean intensity of infection of 15.8 helminths per host. The helminth community was composed of 15 species (Table 1) and had a Shannon's index of diversity of H'= 2.139. The species accumulation curve indicates that such species richness is representative of the fauna of helminths of rufousbellied thrushes. After finding the 15th species of helminth in the 52nd necropsied specimen, no new species were found in the last 99 necropsies. Species richness of parasites per individual host ranged from 0 to 8, showing an average richness of 2.92 species/host. Nine species were classified as dominant, 5 as codominant, and only 1 as subordinate in the helminth community of T. rufiventris (Table 1).
Adult weight ranged from 50 to 87 g (mean= 65.6, s.d.= 6.3, n= 115), it did not differ between the sexes (males: mean= 64.9, s.d.= 5.3, n= 63; females: mean= 66.6, s.d.= 7.2, n=52; H= 2.1087, d.f.= 1, p= 0.1465) and was not affected significantly by the species richness of parasites (F [regression]= 2.1716, p= 0.1395, Fig. 1). An analysis of the influence of the abundance of each species of parasite (independent variable) on the weight of adults (n= 115, dependent variable) suggests that an increase in the frequency of Fernandezia spinosissima (Linstow, 1894) LópezNeyra, 1936 (F= 5.2646, p= 0.0222, r2= 4.45%), Wardium fernandensis (Nybelin, 1929) (F= 4.2604, p= 0.0388, r2= 3.63%) and Cardiofilaria sp. (F= 5.2620, p= 0.0223, r2= 4.45%) relates to a decrease in individual weight. Considering that these coefficients of determination are very low (<5%), an analysis of the influence of the intensity of infection with each species on the weight of thrushes was performed. The weight of thrushes was not related to the intensity of infection with W. fernandensis (F= 2.9341, p= 0.0943, r2= 9.48%, n= 30) or Cardiofilaria sp. (F= 3.2000, p= 0.1048, r2= 26.23%, n= 11), but the intensity of infection with F. spinosissima affected the weight of thrushes (F= 7.1635, p= 0.0359, r2= 54.42%, n= 8). Excluding the single outlier from the sample (18 F. spinosissima specimens in a 55 g thrush), however, results in a marginally significant relationship (F= 6.3425, p= 0.0525, r2= 55.92%, n= 7). The abundance and intensity of infection of none of the other 12 species presented a significant relationship with the weight of adult thrushes.
Adult males and females showed similar species richness of parasites, which ranged from 0 to 8 species (males: mean= 3.0, s.d.= 2.0, n= 63; females: mean= 3.2, s.d.= 2.0, n= 53; Student's t test: t= 0.6105, d.f.= 114, p= 0.5427), and quite similar helminth communities, both qualitatively (Jaccard's index of similarity= 92.9%) and quantitatively (MorisitaHorn index of similarity= 84.6%). However, the diversity of the helminth community of adult males (H'= 2.225) was higher than that of adult females (H'= 1.801; t= 9.7061, p<0.0001).
The species richness of parasites of juvenile males ranged from 0 to 5 species (mean= 2.4, s.d.= 1.5, n= 19), whereas in juvenile females it ranged from 1 to 5 (mean=2.3, s.d.=1.5, n=16). Species richness of parasites was similar between juvenile males and females (t= 0.2340, d.f.= 33, p= 0.8164). Compared to adults, juveniles showed a lower species richness of parasites (adults: mean= 3.1, s.d.= 2.0, n= 116; juveniles: mean= 2.3, s.d.= 1.5, n= 35; Z= 2.5505, p= 0.0108).
The prevalence of a few parasite species also differed between adult and juvenile thrushes (Table 2). Whereas adults showed a higher prevalence of C. conspicuum (64.66% vs. 42.86%), Microtetrameres pusilla (37.07% vs. 14.29%) and Aproctella stoddardi Cram, 1931 (26.72% vs. 0%), juveniles showed a higher prevalence of Syngamus trachea (Montagu, 1811) Chapin, 1925 (22.86% vs. 3.45%). However, the intensity of infection of all species of parasites found in both adult and juvenile individuals was similar between these classes (Table 3).
The prevalence of parasite species was more similar between adult males and females than between adult and juvenile individuals (Table 2). Only Oxyspirura petrowi Skrjabin, 1929 was more prevalent in males (19.05%) than in females (3.77%). The intensity of infection of adult male and adult female thrushes with each species of parasite also was similar (Table 4).
The fauna of helminths of rufousbellied thrushes was known from opportunistic reports to comprise only 5 species (Travassos et al., 1969; Vicente et al., 1995; Fabio and Ferreira, 1999). Our study increased it to 16 species, elevating the diversity of parasites of T. rufiventris to the level found in intensively studied congeneric species, the North American Turdus migratorius Linnaeus, 1766 (e.g., Webster, 1943; Slater, 1967; Cooper and Crites, 1976a, 1976b; Ching, 1993) and the European Turdus merula Linnaeus, 1758 (e.g., Pojmanska, 1969; Schmidt, 1975; Machalska, 1980; Okulewicz and Wesoowska, 2003; Misof, 2005). Whereas the former is known to be parasitized by 6 nematode species, 3 cestodes, 1 digenean and 1 acanthocephalan, the latter is host to 7 nematodes, 4 digeneans, 3 cestodes and 1 acanthocephalan. The proportion of individuals parasitized by at least 1 species of helminth was also similar among these 3 thrushes: T. rufiventris (92.7%, this study), T. migratorius (93.5%, Slater 1967) and T. merula (82.0% based on fecal sample screening, Misof, 2005).
The fauna of parasites of T. rufiventris largely reflects its diet, which is composed of invertebrates such as earthworms, terrestrial snails, terrestrial isopods, millipedes, cockroaches and grasshoppers (Table 5). Therefore, the low prevalence shown by some species of helminths can be related to several nonmutually exclusive factors, including (a) a low natural infection of intermediate hosts, (b) a low availability of intermediate hosts or (c) a low consumption of particular intermediate hosts by the birds. Research on the density of intermediate hosts and their relationships with parasites are important for reaching a better understanding of this multispecies interaction. It is also critical to take into account the variety of life cycles shown by helminths. For example, the filariids A. stoddardi and Cardifilaria sp. are transmitted by vectors and the strongiloidid Strongyloides oswaldoi Travassos, 1930 has a monoxenous (without intermediate host) cycle.
The relationship between the size and age of hosts and the species richness of helminths in the infracommunity and the component community is a major issue in parasite ecology (Bush, 1990, Simberloff and Moore, 1997, but see Poulin and Morand, 2004). Studies have shown that lowly pathogenic intestinal parasites cause a marked weight loss in hosts by strongly changing their energy flow (Connors and Nickol, 1991). Despite the assumption that parasites compromise the health of the host, the species richness of parasites found in the specimens necropsied in the current study did not show a significant relationship with adult weight. This likely absence of influence of species richness of parasites on host morbidity suggests that helminths found in the population of rufousbellied thrushes do not show intensities of infection high enough to compromise the health of individuals, though histopathological analyses were not conducted.
The higher species richness of parasites of adults in comparison with juvenile thrushes is compatible with an increase in the opportunities of infection with a large number of parasites as an effect of age as suggested by Dogiel (1964 apud Simberloff and Moore, 1997). This hypothesis is based on the assumption that the older the host, the longer its exposure to a greater number and diversity of prey species, vectors, eggs and infectant larvae. This relationship can also explain the higher prevalence of some parasite species (C. conspicuum, M. pusilla, A. stoddardi and, possibly, S. oswaldoi and Cardiofilaria sp.) observed in adults. The adultjuvenile difference in the prevalence of C. conspicuum and M. pusilla can be related to the aforementioned factors or to actual differences in food preference. Diet composition is a better candidate for explaining the higher percentage of S. trachea in juveniles (22.86% vs. 3.45% in adults). The highest intensity of infection with S. trachea (36) was found in a fledgling individual. Because S. trachea presents a heteroxenous cycle and can be transmitted directly to the definitive host via ingestion of eggs or of a paratenic host (an earthworm, for example), it is reasonable to suggest that parents can offer earthworms to nestlings.
On the other hand, age is a better variable for explaining the pattern of infection seen with S. oswaldoi, since this monoxenous parasite species depends on the contact of a host with its larvae to be transmitted. In this case, time of exposition is critical. But, the lack of difference between adults and juveniles in the intensity of infection of all species of parasites does not support Dogiel's (1964) hypothesis. This interpretation is based on the rationale that if age affects the probability of infection with a greater number of species, it also should influence the intensity of parasite infection.
The high qualitative and quantitative similarity between the helminth communities of adult males and females permits the conclusion that they prey upon the same invertebrates and highlights a wide overlap in the animal dimension of the trophic niches of males and females. These findings are compatible with Schoener's (1974) ecological postulate that body size influences how species exploit resources. The few differences in prevalence, however, suggest subtle differences in preference for particular food items by males and females. The higher prevalence of O. petrowi in adult males (19.05% vs. 3.77% in females), for example, may derive from a higher consumption of cockroaches.
In sum, parasites proved to be important tools for contributing to our knowledge on the trophic interactions between definitive and intermediate hosts, an approach particularly promising for nondimorphic or secretive species, whose field observations on unmarked individuals is difficult or produces limited data. Future studies may integrate modern techniques of DNA fingerprinting for sexing marked individuals with methods of behavioral observation for comparing microhabitat selection, foraging techniques and diet composition of male and female rufousbellied thrushes.
We thank Luis Cláudio Muniz Pereira, Carla Suertegaray Fontana and Inga Ludmila Veitenheimer Mendes for their comments on this research; Philip J. Scholl for reviewing the English version; the Federal University of Rio Grande do Sul for logistical support; the IBAMA and SMAM for the federal and municipal licenses to collect the birds. CCM also thanks Júlio César, Gabriel and Ana Beatriz for their support and help in all steps of this project, and the Higher Education Authority (CAPES) and the Brazilian National Research Council (CNPq) for the doctoral scholarship. This research comply with current Brazilian laws (federal and municipal licenses, respectively, Instituto Brasileiro do Meio Ambiente e dos Recursos Naturais Renováveis/IBAMA #051/2002/RS, 005/2004/RS and 004/2005/RS, and Secretaria Municipal do Meio Ambiente/SMAM #176/04 and 049/05) and were approved by the Commission of Research Ethics of the Universidade Federal do Rio Grande do Sul.
Acholonu, A. D. 1976. Helminth fauna of saurians from Puerto Rico with observations on the life cycle of Lueheia inscripta (Westrumb, 1821) and description of Allopharynx puertoricensis sp.n. Proceedings of the Helminthological Society of Washington 43:106116. [ Links ]
Amato, J. F. R., W. A. Boeger and S. B. Amato. 1991. Protocolos para Laboratório Coleta e Processamento de Parasitos de Pescado. Imprensa Universitária, Universidade Federal Rural do Rio de Janeiro, Seropédica. 81 p. [ Links ]
Anderson, R. C. 2000. Nematode Parasites of Vertebrates: Their Development and Transmission. CABI Publishing, Wallingford. 650 p. [ Links ]
Ayres, M., M. Ayres Jr., D. L. Ayres and A. S. Santos. 2005. BioEstat 4.0. Aplicações estatísticas nas áreas das Ciências Biológicas e Médicas. Sociedade Civil Mamirauá, Belém. 324 p. [ Links ]
Belton, W. 1976. Alguns aspectos da migração e distribuição das aves no Estado do Rio Grande do Sul, Brasil. Iheringia 5:6980. [ Links ]
Belton, W. 1994. Aves do Rio Grande do Sul: Distribuição e Biologia. Editora Unisinos, São Leopoldo. 584 p. [ Links ]
Borgstede, F. H. M., A. Okulewicz and J. Okulewicz. 2000. A study of the helminth fauna of birds belonging to the Passeriformes in the Netherlands. Acta Parasitologica 45:1421. [ Links ]
Brasil, M. C. and S. B. Amato. 1992. Faunistic analysis of the helminths of sparrows (Passer domesticus L., 1758) captured in Campo Grande, Rio de Janeiro, RJ. Memórias do Instituto Oswaldo Cruz 87:4348. [ Links ]
Brower, J. E. and J. H. Zar. 1984. Field and Laboratory Methods for General Ecology. Wm. C. Brown Company Publishers, Dubuque. 226 p. [ Links ]
Bush, A. O. 1990. Helminth communities in avian hosts: determinants of pattern. In Parasite communities: patterns and processes, G. W. Esch, A. O. Bush and J. M. Aho (eds.). Chapman & Hall, New York. P. 197232. [ Links ]
Bush, A. O., K. D. Lafferty, J. M. Lotz and A. W. Shostak. 1997. Parasitology meets ecology on its own terms: Margolis et al. revisited. Journal of Parasitology 83:575583. [ Links ]
Ching, H. L. 1993. Helminths of varied thrushes, Ixoreus naevius and robins Turdus migratorius, from British Columbia. Journal of the Helminthological Society of Washington 60:239242. [ Links ]
Connors, V. A. and B. B. Nickol. 1991. Effects of Plagiorhynchus cylindraceus (Acanthocephala) on the energy metabolism of adult starlings, Sturnus vulgaris. Parasitology 103:395402. [ Links ]
Cooper, C. L. and J. L. Crites. 1976a. Community ecology of helminth parasitism in an insular passerine avifauna. Journal of Parasitology 62:105110. [ Links ]
Cooper, C. L. and J. L. Crites. 1976b. A check list of the helminth parasites of the robin, Turdus migratorius Ridgway. The American Midland Naturalist 95:194198. [ Links ]
Cram, E. B. 1934. Orthopterans and pigeons as secondary and primary hosts, respectively, for the crow stomachworm Microtetrameres helix (Nematoda: Spiruridae). Proceedings of the Helminthological Society of Washington 1:50. [ Links ]
Efe, M. A., L. M. Mohr and L. Bugoni. 2001. Guia Ilustrado das Aves de Porto Alegre. PROAVES, SMAN, COPESUL, CEMAVE, Porto Alegre. 144 p. [ Links ]
Fabio, S. P. and I. Ferreira. 1999. Parasitismo por Lutztrema obliquum (Travassos,1917)(Digenea, Dicrocoeliidae) em Turdus albicollis (Vieillot, 1818), sabiácoleira, da Ilha da Marambaia, Rio de Janeiro. Contribuições Avulsas sobre a História Natural do Brasil, Série Zoologia 4:13. [ Links ]
Fielding, J. W. 1926. Preliminary note on the transmission of the eyeworms of Australian poultry. Australian Journal of Experimental Biology and Medical Science 3:225232. [ Links ]
Fielding, J. W. 1927. Further observations of the life history of the eyeworm of poultry. Australian Journal of Experimental Biology and Medical Science 4:273281. [ Links ]
Fontana, C. S. 2001. Aves. In Flora e Fauna do Parque Natural Morro do Osso Porto Alegre/RS, S. R. Mirapalhete (coord.). SMAM, Porto Alegre. p. 8295. [ Links ]
Fontana, C. S. 2005. A ornitofauna de Porto Alegre no Século XX: status de ocorrência e conservação. Comunicações do Museu de Ciência e Tecnologia da PUCRS, Série Zoologia 18:161206. [ Links ]
Gaunt, A.S. and L. W. Oring. 1999. Guidelines to the Use of Wild Birds in Research. The Ornithological Council, Washington. 115 p. [ Links ]
Hammer, Ø, D. A. T. Harper and P. D. Ryan. 2001. PAST: Paleontological Statistics Software Package for Education and Data Analysis. http://palaeoelectronica.org/2001_1/past/issue1_01.htm. 27.IX.2006 [ Links ]
Hudson, P. J., A. P. Dobson and K. D. Lafferty. 2006. Is a healthy ecosystem one that is rich in parasites? Trends in Ecology and Evolution 21:381385. [ Links ]
Isomursu, M., O. Rätti, P. Helle and T. Hollmén. 2006. Sex and age influence intestinal parasite burden in three boreal grouse species. Journal of Avian Biology 37:516522. [ Links ]
Karasov, W. H. 1990. Digestion in birds: Chemical and physiological determinants and ecological implications. Studies in Avian Biology 13:391415. [ Links ]
Kennedy, C. R., A. O. Bush and J. M. Aho. 1986. Patterns in helminth communities: why are birds and fish different? Parasitology 93:205215. [ Links ]
Kingston, N. 1965. On the morphology and life cycle of the trematode Tanaisia zarudnyi (Skrjabin, 1924) Byrd and Denton, 1950, from the ruffed grouse, Bonasa umbellus L. Canadian Journal of Zoology 43:935969. [ Links ]
Krissinger, W.A. 1984. The life history of Lutztrema monenteron (Price and McIntosh, 1935) Travassos, 1941 (Trematoda: Dicrocoeliidae). Proceedings of the Helminthological Society of Washington 51:275281. [ Links ]
Leigh, S. R. and W. L. Jungers. 1994. A reevaluation of subspecific variation and canine dimorphism in wooly spider monkeys (Brachyteles arachnoides). American Journal of Physical Anthropology 95:435442. [ Links ]
Machalska, J. 1980. Helminth fauna of the genus Turdus L., examined during their spring and autumn migration. I. Digenea. Acta Parasitologica Polonica 27:153172. [ Links ]
Magurran, A. E. 1988. Ecological Diversity and its Measurement. Princeton University Press, Princeton. 179 p. [ Links ]
Marcogliese, D. J. and D. K. Cone. 1997. Food webs: a plea for parasites. Trends in Ecology and Evolution 12:320325. [ Links ]
McLaughlin, J. D. 2001. EMAN Protocols for Measuring Biodiversity: Parasites of Birds. Canadian Society of Zoologists, Montreal. 84 p. [ Links ]
Misof, K. 2005. Eurasian blackbirds (Turdus merula) and their gastrointestinal parasites: a role for parasites in lifehistory decisions? Dissertation zur Erlangung des Doktorgrades der MathematischNaturwissenschaftlichen Fakultat der Rheinischen FriedrichWilhelmsUniversitat Bonn. 115 p. [ Links ]
Moore, S. L. and K. Wilson. 2002. Parasites as a viability cost of sexual selection in natural populations of mammals. Science 297:20152018. [ Links ]
Moravec, F., J. Prokopic and A. V. Shlikas. 1987. The biology of nematodes of the family Capillariidae NeveuLemaire, 1936. Folia Parasitologica 34:3956. [ Links ]
Morse, D. H. 1990. Food exploitation by birds: some current problems and future goals. Studies in Avian Biology 13:134143. [ Links ]
Mourad, A. R. 1967. Beetles as intermediate hosts of cestodes of the family Hymenolepididae. Folia Parasitologica 14:379380. [ Links ]
Okulewicz, J. and M. Wesoowska. 2003. Rediscovery of Leyogonimus postgonoporus (Neiland, 1951) (Trematoda, Stomylotrematidae) in Central Europe. Acta Parasitologica 48:233236. [ Links ]
Patten, J. A. 1952. The life cycle of Conspicuum icteridorum Denton and Byrd, 1951, (Trematoda: Dicrocoelliidae). Journal of Parasitology 38:165182. [ Links ]
Pojmanska, T. 1969. Leucochloridium perturbatum sp. n. (Trematoda: Brachylaimidae), morphology, individual variability and life cycle. Acta Parasitologica 16:153178. [ Links ]
Poulin, R. 1996. Sexual inequalities in helminth infections: a cost of being a male? American Naturalist 147:287295. [ Links ]
Poulin, R. and S. Morand. 2004. Parasite Biodiversity. Smithsonian Books, Washington. 216 p. [ Links ]
Price, P. W. 1980. Evolutionary Ecology of Parasites. Princeton University Press, Princeton. 237 p. [ Links ]
Price, P. W. 1990. Host populations as resources defining parasite community organization. In Parasite communities: patterns and processes, G. W. Esch, A. O. Bush and J. M. Aho (eds.). Chapman & Hall, New York. p. 2340. [ Links ]
Proctor, N. S. and P. J. Lynch. 1993. Manual of Ornithology: avian structure & function. Yale University Press, New Haven. 340 p. [ Links ]
Quentin, J. C., C. Seureau and S. D. Kulo. 1986. Cycle biologique de Tetrameres (Microtetrameres) inermis (Linstow, 1879) nématode Tetrameridae parasite du Tisserin Ploceus aurantius au Togo. Annales de Parasitologie Humaine et Comparée 61:321332. [ Links ]
Robinson, S. A., M. R. Forbes, C. E. Hebert and J. D. McLaughlin. 2008. Malebiased parasitism by common helminthes is not explained by sex differences in body size or spleen mass of breeding cormorants Phalacrocorax auritus. Journal of Avian Biology 39:272276. [ Links ]
Rosenberg, K. V. and R. J. Cooper. 1990. Approaches to avian diet analysis. Studies in Avian Biology 13:8090. [ Links ]
Rysavy, B. 1973. Enseniella tetraedra (Savigny)(Oligochaeta), a new intermediate host of the cestode Dilepis undula (Schrank, 1782). Folia Parasitologica 20:16. [ Links ]
Santos, A. J. 2003. Estimativas de riqueza em espécies. In Métodos de Estudos em Biologia da Conservação e Manejo da Vida Silvestre, Jr. L. Cullen, R. Rudran and C. B. ValladaresPádua (eds.). Editora da Universidade Federal do Paraná, Curitiba. p. 1941. [ Links ]
Schalk, G and M. R. Forbes. 1997. Male biases in parasitism of mammals: effects of study type, host age, and parasite taxon. Oikos 78:6774. [ Links ]
Schmidt, G. D. 1975. Sphaerirostris wertheimae sp. n., and other Acanthocephala from vertebrates of Israel. Journal of Parasitology 61:298300. [ Links ]
Schoener, A. P. 1974. Resource partitioning in ecological communities. Science 185:2739. [ Links ]
Simberloff, D. and J. Moore. 1997. Community ecology of parasites and freeliving animals. In HostParasite Evolution: general principles and avian models, D. H. Clayton and J. Moore (eds.). Oxford University Press, Oxford. p. 174197. [ Links ]
Slater, R. L. 1967. Helminths of the robin, Turdus migratorius Ridgway, from Northern Colorado. American Midland Naturalist 77:190199. [ Links ]
Thul, J. E., D. J. Forrester and C. L. Abercrombie. 1985. Ecology of parasitic helminths of wood ducks, Aix sponsa, in the Atlantic flyway. Proceedings of the Helminthological Society of Washington 52:297310. [ Links ]
Travassos, L., J. F. T. Freitas and A. Kohn. 1969. Trematódeos do Brasil. Memórias do Instituto Oswaldo Cruz 67:1886. [ Links ]
Vicente, J. J., H. O. Rodrigues, D. C. Gomes and R. M. Pinto. 1995. Nematóides do Brasil. Parte IV: Nematóides de Aves. Revista Brasileira de Zoologia 12:1273. [ Links ]
Webster, J. D. 1943. Helminths from the robin, with the description of a new nematode, Porrocaecum brevispiculum. Journal of Parasitology 29:161163. [ Links ]
Wehr, E. E. 1937. Observations on the development of the poultry gapeworm Syngamus trachea. Transactions of the American Microscopical Society 56:7277. [ Links ]
Wilkinson, L. E. 1990. Systat. Systat Inc, Evanston. 677 p. [ Links ]
Windsor, D. A. 1997. Stand up for parasites. Trends in Ecology and Evolution 12:32. [ Links ]
Windsor, D. A. 1998. Most of the species on Earth are parasites. International Journal for Parasitology 28:19391941. [ Links ]
Yamaguti, S. 1975. A Synoptical Review of Life Histories of Digenetic Trematodes of Vertebrates. Keigaku Publishing Co, Tokyo. 590 p. [ Links ]
Zuk, M. and K. A. McKean. 1996. Sex differences in parasite infections: patterns and processes. International Journal for Parasitology 26:10091024. [ Links ]