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Revista mexicana de biodiversidad

versão On-line ISSN 2007-8706versão impressa ISSN 1870-3453

Rev. Mex. Biodiv. vol.84 no.4 México Dez. 2013 

Taxonomía y sistemática


New records and a checklist of trematodes from Butorides striata (Aves: Ardeidae)


Nuevos registros y una lista de tremátodos de Butorides striata (Aves: Ardeidae)


Hudson Alves Pinto*, Vitor Luís Tenorio Mati and Alan Lane de Melo


Laboratório de Taxonomía e Biologia de Invertebrados, Departamento de Parasitología, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, CP 486, 31270-901 Belo Horizonte, Minas Gerais, Brazil. *


Recibido: 24 noviembre 2012
Aceptado: 12 junio 2013



Seven species of trematodes were identified during the study of helminths found in Butorides striata (Linnaeus, 1758) from Belo Horizonte, Minas Gerais, Brazil: Ascocotyle (Phagicola) angrense (Travassos, 1916), Ascocotyle (Phagicola) pindoramensis (Travassos, 1928), Centrocestus formosanus (Nishigori, 1924), Clinostomum heluans Braun, 1899, Clinostomum marginatum (Rudolphi, 1819), Posthodiplostomum nanum Dubois, 1937, and Prosthogonimus ovatus (Rudolphi, 1803). Butorides striata is a new host for C. heluans, P. ovatus, A. (P.) pindoramensis, and C. formosanus. This last species is reported for the first time in a naturally infected definitive host in South America. Additionally, an updated checklist with 31 species of trematodes already reported in B. striata is presented.

Key words: Brazil, Clinostomidae, Digenea, Diplostomidae, Heterophyidae, Prosthogonimidae, trematodes.



Se identificaron 7 especies de tremátodos durante el estudio de los helmintos hallados en Butorides striata (Linnaeus, 1758) de Belo Horizonte, Minas Gerais, Brasil: Ascocotyle (Phagicola) angrense (Travassos, 1916), Ascocotyle (Phagicola) pindoramensis (Travassos, 1928), Centrocestus formosanus (Nishigori, 1924), Clinostomum heluans Braun, 1899, Clinostomum marginatum (Rudolphi, 1819), Posthodiplostomum nanum Dubois, 1937, Prosthogonimus ovatus (Rudolphi, 1803). Butorides striata es un nuevo huésped definitivo para C. heluans, P. ovatus, A. (P.) pindoramensis y C. formosanus. Esta última especie se registra por primera vez en un huésped definitivo naturalmente infectado en América del Sur. Además, se presenta un listado actualizado con 31 especies de tremátodos ya documentados para B. striata.

Palabras clave: Brasil, Clinostomidae, Digenea, Diplostomidae, Heterophyidae, Prosthogonimidae, tremátodos.



Studies on digenetic trematodes of Neotropical birds have been carried out since the early nineteenth century, and dozens of species of these parasites have been described in Latin America (reviewed by Travassos et al., 1969; Thatcher, 1993; Pérez-Ponce de León et al., 2007; Lunaschi et al., 2007). Despite the diversity of species of trematodes already known, it is possible that several interactions involving birds and trematodes are still unknown in the Neotropics.

Factors related to habitat destruction, climate change, food web alterations, as well as illegal hunting may contribute to population reduction and extinction of bird species, and consequently can cause changes in populations of parasite species, sometimes their co-extinction. Thus, trematodes are more vulnerable to such alterations than other helminths, in part due to their complex life cycle involving intermediate hosts (Dobson et al., 2008). In this regard, studies to expand knowledge about trematodes from birds are still desirable.

Among the bird species that are potential definitive host of trematodes in the Neotropics is the striated heron, Butorides striata (Linnaeus, 1758), a small ardeid distributed mainly in South America, but also found in tropical regions of the Old World (Hayes, 2002). Studies on helminth fauna of B. striata were performed in different countries, but data on these birds infected with trematodes are relatively scarce and scattered in the scientific literature. In the present study, new host and geographical records as well as a checklist of trematodes reported in B. striata are presented.


Materials and methods

A young specimen of B. striata was found dead on the banks of the Pampulha Reservoir (43°59'35" W, 19°50'50" S), Belo Horizonte, State of Minas Gerais, Brazil in May 2010. The bird was transported to the laboratory, identified according to Hayes (2002), and necropsied (authorization number 21590 from the Brazilian Institute of Environment and Renewable Natural Resources - IBAMA). At necropsy, organs were separated, placed in Petri dishes containing saline solution (0.85% NaCl) and examined with the aid of a stereomicroscope. The trematodes found were compressed between glass slides, fixed in 10% formalin at 70° C, stained with alum acetocarmine, dehydrated in ascending series of ethanol, cleared in beechwood creosote, and mounted in Canada balsam. Measurements of the parasites were obtained with the aid of an ocular micrometer and photographs were taken with a Leica ICC50 HD digital camera attached to a light microscope. Taxonomic identifications were based on morphological characters following several authors (Travassos et al., 1969; Kohn and Fernandes, 1972; Ostrowski-de Nunez, 1973; Gibson et al., 2002; Simöes et al., 2006; Bray et al., 2008; Caffara et al., 2011). The specimens studied were deposited in the collection of the Laboratory of Taxonomy and Biology of Invertebrates (DPIC), Department of Parasitology, Federal University of Minas Gerais. Furthermore, a checklist was compiled based on the new and previous reports of trematode species from B. striata.



Morphological analyses of parasites permitted the identification of 7 species of trematodes belonging to 5 genera and 4 families. The family and species of the trematodes found in B. striata in the present study, as well as taxonomic summaries containing the intensity of infection, site of infection, accession number of deposited specimens, and taxonomic comments for each parasite species are presented below. Measurements of the parasites are given in micrometers with the mean (when possible) followed by the standard deviation and amplitude in parentheses (Table 1).

Clinostomidae Lühe, 1901

Clinostomum heluans Braun, 1899 (Fig. 1)

Taxonomic summary

Intensity of infection: 1.

Site of infection: oral cavity.

Specimen deposited: DPIC 6240.

Remarks. Trematode species of the genus Clinostomum Leidy, 1856 are parasites of the oral cavity and esophagus of fish-eating birds. Three species, namely C. heluans, C. marginatum (Rudolphi, 1819), and C. detruncatum Braun, 1899, have been reported in Brazil (Travassos et al., 1969; Thatcher, 1993). Clinostomum heluans was described from a Brazilian specimen of Egretta caerulea (Linnaeus, 1758), and differs from other South American species of the genus mainly by the arrangement of reproductive structures in the posterior region of the body and in the position of the genital pore on the margin of anterios testis. The species was later recorded in Ardea cocoi Linnaeus, 1766 and Nyctanassa violacea (Linnaeus, 1758) in Brazil (Travassos et al., 1969), and in Ardea herodias Linnaeus, 1758 and Ardea alba egreta Gmelin, 1789 from Cuba (Pérez-Vigueras, 1955), in A. herodias from Mexico (Bravo-Hollis, 1947; Pérez-Ponce de León et al., 2007), in Ardea alba Linnaeus, 1758 from Venezuela (Caballero and Diaz-Ungria, 1958), and recently in A. alba from the Czech Republic (Sitko, 2012).

The life cycle of C. heluans remains unknown. Lutz (1934) was believed to have elucidated the life cycle of this parasite, when in fact, he had used material of C. marginatum (Travassos et al., 1969). Two species of fish, Cichla temensis Humboldt, 1821 and Geophagus proximus (Castelnau, 1855), were reported harboring metacercariae of C. heluans in Brazil (Vicente et al., 1978; Zago et al., 2012). Butorides striata is here registered as a new definitive host for C. heluans.

Clinostomum marginatum (Rudolphi, 1819) (Fig. 2)

(Syn: Distoma marginatum Rudolphi, 1819)

Taxonomic summary

Intensity of infection: 1.

Site of infection: oral cavity.

Specimen deposited: DPIC 6239.

Remarks. Clinostomum marginatum is widely distributed throughout the Americas, and it has been reported in 13 species of birds from Brazil (Travassos et al., 1969; Arruda et al., 2001; Dias et al., 2003). The species was previously found in B. striata in the State of Mato Grosso, Brazil by Travassos (1945) and since then it has not been recorded in this host. Later, C. marginatum was reported in Tigrisoma lineatum (Boddaert, 1783) from Argentina (Lunaschi and Drago, 2009), and in at least 10 species of birds from Mexico (as C. complanatum) (Ramos-Ramos, 1995; Pérez-Ponce de León et al., 2007). Clinostomum marginatum had previously been considered a junior synonym of C. complanatum (Rudolphi, 1809), a species reported in birds from the Old World. However, morphological and molecular studies showed that C. marginatum is a distinct American species (Dzikowski et al., 2004; Caffara et al., 2011). The morphological differences, in particular body width, distance between the suckers, and shape of the sexual organs of the specimen studied are in agreement with those ascribed to C. marginatum (Caffara et al., 2011). Moreover, measurements and the disposition of reproductive structures of the specimen of C. marginatum reported in the present study differ significantly from that verified in C. heluans. The life cycle of C. marginatum involves planorbid mollusks of the genera Biomphalaria Preston, 1910 in South America, and Helisoma Swainson, 1840 in North America, as first intermediate hosts (Lutz, 1934; Krull, 1934; Dias et al., 2003). Metacercariae of C. marginatum were reported in several species of fish from the Americas, including more than 20 species of these hosts from Brazil (Pinto and Melo, 2012a).

Diplostomidae Poirier, 1886

Posthodiplostomum nanum Dubois, 1937 (Fig. 3)

(Syn: Posthodiplostomum antillanum Pérez-Vigueras, 1944)

Taxonomic summary

Intensity of infection: 183.

Site of infection: small intestine.

Specimens deposited: DPIC 6233.

Remarks. Species of Posthodiplostomum Dubois, 1936 are intestinal trematodes of birds; 5 species (P. grande (Diesing, 1850), P. macrocotyle Dubois, 1937, P. microsicya Dubois, 1936, P. prosostomum Dubois and Rausch, 1948, and P. nanum) were reported in Brazil (Travassos et al., 1969; Thatcher, 1993). Posthodiplostomum nanum was described from B. striata in Brazil and later recorded in several species of birds in Argentina (Boero et al., 1972; Ostrowski-de Núñez, 1973; Digiani, 2000; Lunaschi et al., 2007; Drago and Lunaschi, 2011), Cuba (Pérez-Vigueras, 1944), and Paraguay (Dubois, 1985). The life cycle of P. nanum was studied in Argentina by Ostrowski-de Núñez (1973), who obtained strigeid cercariae in experimentally infected Uncancylus concentricus (d'Orbigny, 1835). Metacercariae of the parasite were found in fishes, mainly poeciliids, in Argentina (Ostrowski-de Núñez, 1973; Doma and Ostrowski-de Núñez, 1994) and Brazil (Dubois, 1970; Pinto and Melo, 2012a). Metacercariae found in fishes and identified as P. nanum in Africa (Fitschal and Thomas, 1968; Williams, 1967) are conspecific with Posthodiplostomum biellipticum Dubois, 1958, and therefore the area of occurrence of P. nanum is possibly restricted to the Americas (Ostrowski-de Núñez, 1973).

Heterophyidae Leiper, 1909

Ascocotyle (Phagicola) angrense Travassos, 1916 (Fig. 4)

(Syn: Phagicola angrense (Travassos, 1916))

Taxonomic summary

Intensity of infection: 7.

Site of infection: small intestine.

Specimens deposited: DPIC 6236.

Remarks. Species of Ascocotyle Looss, 1899 are intestinal parasites of birds and mammals with a worldwide distribution. In Brazil, 6 species (A. angrense, A. felippei Travassos, 1928, A. arnaldoi (Travassos, 1928), A. angeloi (Travassos, 1929), A. pindoramensis (Travassos, 1928), and A. longa Ransom, 1920) are currently known (Travassos et al., 1969; Thatcher, 1993; Simöes et al., 2006; Santos et al., 2007). Ascocotyle (P.) angrense was described from B. striata in Brazil and later reported in Ixobrychus exilis (Gmelin, 1789) and Ardea cocoi Linnaeus, 1766 (Travassos, 1930; Arruda et al., 2001), and in Ajaia ajaja (Linnaeus, 1758), Ardea alba Linnaeus, 1758, Ardea alba egretta Gmelin, 1789 and Ixobrychus involucris (Vieillot, 1823) from Argentina (Ostrowski-de Núñez, 1993; Lunaschi et al., 2007). This heterophyid species presents as differential features the presence of a crown with 20 acicular spines, 18 in a single row and 2 accessories spines (Travassos, 1930; Ostrowski-de Núñez, 1993). The complete life cycle of A. (P.) angrense is unknown (Ostrowski-de Núñez, 1993). Metacercariae of the parasite have been found in the gills of Phallocerus caudimaculatus (Hensel, 1868) from Brazil and Argentina (Travassos, 1931; Ostrowski-de Núñez, 1974). Although A. (P.) angrense has been reported in birds and fishes in the United States and Mexico (Sogandares-Bernal and Lumsden, 1963; Salgado-Maldonado and Aguirre-Macedo, 1991), further studies demonstrated that these records correspond to A. (P.) diminuta (Stunkard and Haviland, 1924) and A. (P.) nana Ransom, 1920, and the area of occurrence of A. (P.) angrense is possibly restricted to South America (Ostrowski-de Núñez, 1993; Scholz et al., 1997; Scholz et al., 2001). This is the only report of A. (P.) angrense in B. striata from Brazil since the description of the species by Travassos (1916).

Ascocotyle (Phagicola) pindoramensis (Travassos, 1928) (Fig. 5)

(Syn: Pygidiopsis pindoramensis Travassos, 1928; A. (P.) mollienisicola (Sogandares-Bernal and Bridgman, 1960); Pseudascocotyle mollienisicola Sogandares-Bernal and Bridgman, 1960)

Taxonomic summary

Intensity of infection: 4.

Site of infection: small intestine.

Specimens deposited: DPIC 6237.

Remarks. Ascocotyle (P.) pindoramensis was described based on parasites found in I. exilis from Brazil, and was later reported in Brazilian specimens of N. violacea and Nycticorax nycticorax (Linnaeus, 1758) (Travassos, 1928; Arruda et al., 2001). This species was redescribed from parasites obtained experimentally in Mesocricetus auratus (Simöes et al., 2006). Metacercariae of A. (P.) pindoramensis were reported in Poecilia latipinna (Lesueur, 1821) in the United States, P. velifera (Regan, 1814) in Nicaragua, and Poecilia vivipara Bloch and Schneider, 1801 and Phalloptychus januarius (Hensel, 1868) in Brazil (Sogandares-Bernal and Bridgman, 1960, 1963; Aguirre-Macedo et al., 2001; Simöes et al., 2006).

Parasites found in some bird species (including B. striata) in Argentina (Ostrowski-de Núñez, 1976) and metacercariae obtained in poeciliids in Mexico (Scholz et al., 2001) were identified as Pygidiops pindoramensis; however, they differ from A. (P.) pindoramensis sensu Travassos, 1928 mainly by the presence of an acicular crown of spines, and are currently considered an undetermined species of Pygidiopsis (Simöes et al., 2006; Lunaschi et al., 2007; Pérez-Ponce de León et al., 2007). The first intermediate host of A. (P.) pindoramensis also remains unknown. Butorides striata is here reported as a new host to A. (P.) pindoramensis.

Centrocestus formosanus (Nishigori, 1924) (Fig. 6)

(Syn: Stamnosoma formosanus Nishigori, 1924)

Taxonomic summary

Site of infection: small intestine.

Intensity of infection: 10.

Specimens deposited: DPIC 6235.

Remarks. Centrocestus Looss, 1899 comprises species of intestinal small flukes from birds and mammals, including humans in Asia. Centrocestus formosanus is native to Asia; after its introduction in the American continent in the late 1950s it was reported in its first intermediate host, the thiarid Melanoides tuberculata (Müller, 1774), so far in 5 countries of this continent (reviewed by Pinto and Melo, 2011). Moreover, the parasite was reported in several fish species in different countries and can cause mortality and losses to fish farming (Scholz and Salgado-Maldonado, 2000; Mitchell et al., 2005; Arguedas-Cortés et al., 2010). Although there are several records of C. formosanus in the intermediate hosts in the Americas, studies related to natural definitive hosts are scarce. In fact, the only record is from a bird species identified as B. striata in Mexico (Scholz and Salgado-Maldonado, 2000; Pérez-Ponce de León et al., 2007). However, in view of the current knowledge related to the distribution of Butorides spp. (Hayes, 2002), the Mexican host of C. formosanus from the above record may be Butorides virescens (Linnaeus, 1758), the only species of Butorides endemic in North America. The present study is the first report of the natural infection of B. striata with C. formosanus in South America. In Brazil, C. formosanus was previously reported in naturally infected M. tuberculata (Pinto and Melo, 2010; Paula-Andrade et al., 2012) and fishes, Australoherosfacetus (Jenyns, 1842) and Poecilia reticulata Peters, 1859 (Pinto and Melo, 2012a, b). Aspects of the interaction between the parasite and experimentally infected mice were recently evaluated (Mati et al., 2013). Given the known non-specificity of C. formosanus, possibly other Neotropical species of fish-eating birds are involved in the maintenance of the parasite in the Americas.

Prosthogonimidae Lühe, 1909

Prosthogonimus ovatus (Rudolphi, 1803) (Fig. 7)

(Syn: Fasciola ovata Rudolphi, 1803; Distoma ovatum (Rudolphi, 1803); Cephalogonimus ovatus Stossich, 1892; Prymnoprion ovatus Looss, 1899)

Taxonomic summary

Intensity of infection: 1.

Site of infection: cloaca.

Specimens deposited: DPIC 6238.

Remarks. Species of the genus Prosthogonimus Lühe, 1899 are parasites of the oviduct and cloaca of birds with a worldwide distribution. Prosthogonimus ovatus, the type species of the genus, has a cosmopolitan distribution and has already been reported in several countries of the Americas, Europe, Africa, and Asia (Jones, 2008). In Brazil, this species was found for the first time in Gallus gallus (Linnaeus, 1758) by Travassos (1920). Later, it was found in about 30 species of birds, and it is considered a species with wide morphological variety and low host specificity (Travassos et al., 1969; Kohn and Fernandes, 1972; Monteiro et al., 2007; Mascarenhas et al., 2009). Despite the diversity of vertebrate hosts already reported infected with P. ovatus, this species has not been yet found in B. striata. The life cycle of this parasite was elucidated in Europe and involves aquatic mollusks (Bithynia tentaculata (Linnaeus, 1758)); xiphidiocercariae are formed, and after emerging, penetrate into dragonfly larvae and develop into metacercariae (Boddeke, 1960a, b). The first intermediate hosts and larval stages have not yet been identified in the Americas.

A checklist of trematodes species from B. striata based on 29 previous reports available in the literature and the data obtained in this study are presented in Table 2. To date, trematodes belonging to 11 families, 22 genera, and 31 species were reported infecting B. striata in 8 countries. The highest number species of trematodes from B. striata (22; 71%) was reported in South America, and over half of these species (16; 52%) were registered in B. striata from Brazil. Moreover, Heterophyidae was the family with the highest number of species recorded in B. striata (9), followed by Echinostomatidae (5) and Diplostomidae (4). Postodiplostomum nanum was the species with the widest distribution, and was recorded to date in 3 countries (Brazil, Argentina, and Paraguay). Interestingly, none of the 9 species of trematodes recorded in B. striata in Asia, or the trematodes species reported in this ardeid in Africa, have been recorded for the same host in the Americas. The converse is also true for species reported in the Americas.

Among the 7 species of trematodes found in a single specimen of B. striata evaluated in this study, C. heluans, P. ovatus, A. (P.) pindoramensis, and C. formosanus are here recorded in a new host and locality. Overall, there are 16 species of trematodes reported in this host in Brazil, a number significantly higher than that reported for nematodes (4 species) and cestodes (5 species) (Rego and Rolas, 1972; Vicente et al., 1995; Anuda et al., 2001; Pinto et al., 2004, 2012).

Previous extrapolations of the global parasite species richness show that 3 species of the trematodes are estimated for each bird species (Poulin and Morand, 2004; Dobson et al., 2008). However, the fauna of trematodes reported in B. striata (31 species) is very high compared to these estimates. Factors such as close contact with aquatic collections may be related to higher parasite richness of trematodes verified in birds (Bush et al., 1990; Gregory et al., 1991; Poulin, 1995; Poulin and Morand, 2004), apparently linked to a greater exposure to a variety of prey species, including different groups of invertebrates, amphibians, and fish, potential intermediate hosts of trematodes. Thus, the habitat and feeding habits of B. striata may also be related to the parasite richness observed in this specimen, which may be true for other species of Ardeidae.

Knowledge of the species of trematodes found in birds may still be underestimated, especially in the Neotropics. Therefore, additional parasitological surveys are needed in order to better understand the complex interrelationships among parasites and birds.


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