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Checklist of the cestode parasites of wild birds of Argentina

Published online by Cambridge University Press:  17 August 2021

F.B. DragoOpen the ORCID record for F.B. Drago[Opens in a new window],
M. Dueñas Díaz,
R. DraghiOpen the ORCID record for R. Draghi[Opens in a new window] and
V. NúñezOpen the ORCID record for V. Núñez[Opens in a new window]
F.B. Drago*
Affiliation:
División Zoología Invertebrados, Museo de La Plata, Facultad de Ciencias Naturales y Museo, Paseo del Bosque, s/n, 1900 La Plata, Buenos Aires Province, ArgentinaComisión de Investigaciones Científicas de la provincia de Buenos Aires (CIC), Calle 526 e/10 y 11 (1900) La Plata, Buenos Aires, Argentina
M. Dueñas Díaz
Affiliation:
División Zoología Invertebrados, Museo de La Plata, Facultad de Ciencias Naturales y Museo, Paseo del Bosque, s/n, 1900 La Plata, Buenos Aires Province, ArgentinaConsejo Nacional de Investigaciones Científicas y Técnicas de Argentina, Godoy Cruz 2290 (C1425FQB) CABA, Argentina
R. Draghi
Affiliation:
División Zoología Invertebrados, Museo de La Plata, Facultad de Ciencias Naturales y Museo, Paseo del Bosque, s/n, 1900 La Plata, Buenos Aires Province, ArgentinaConsejo Nacional de Investigaciones Científicas y Técnicas de Argentina, Godoy Cruz 2290 (C1425FQB) CABA, Argentina
V. Núñez
Affiliation:
División Zoología Invertebrados, Museo de La Plata, Facultad de Ciencias Naturales y Museo, Paseo del Bosque, s/n, 1900 La Plata, Buenos Aires Province, ArgentinaComisión de Investigaciones Científicas de la provincia de Buenos Aires (CIC), Calle 526 e/10 y 11 (1900) La Plata, Buenos Aires, Argentina
*
Author for correspondence: F.B. Drago, E-mail: fdrago@fcnym.unlp.edu.ar
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Abstract

An annotated checklist of the cestode parasites of Argentinean wild birds is presented, as the result of a compilation of parasitological papers published between 1900 and April 2021. This review provides data on hosts, geographical distribution, sites of infection, location of material deposited in helminthological collections, references and taxonomic comments. A host/parasite list is also provided. During this period, 38 papers were published that gather information about 34 cestode nominal species and 11 taxa identified at generic level, belonging to three orders, ten families and 35 genera. The highest number of cestode taxa was recorded in the family Hymenolepididae, with 12 nominal species and two taxa identified at generic level, followed by Dilepididae, with eight nominal species and three taxa identified at generic level. Of the 1042 species of birds reported in Argentina, only 29 (2.8%) were reported as hosts of adult cestodes. The families of birds with the highest number of reported taxa were Laridae and Anatidae, with 20 and 14 taxa, respectively.

Keywords

HelminthsCestodaAvesArgentina

Information

Type
Research Paper
Information
Journal of Helminthology , Volume 95 , 2021, e43
Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press

Introduction

After digeneans, tapeworms (Cestoda) are the second most species-rich group of platyhelminths, and with over 5000 species described, represent one of the most successful groups of parasitic helminths. Due to their hidden existence in the bowels of many kinds of vertebrates, and as intermediate developmental stages are spent within a diversity of invertebrates and vertebrates, the known diversity is likely just a small fraction of the true numbers that exist (Waeschenbach et al., Reference Waeschenbach, Webster and Littlewood2012). Recent estimates of the global diversity of helminths indicate that only 16% of the cestodes are known, and that the number of species could reach 23,749, of which 10,257 would use birds as definitive hosts (Carlson et al., Reference Carlson, Dallas, Alexander, Phelan and Phillips2020).

Argentina possesses a high diversity of birds, with 1033 native species and nine introduced species (Roesler & González Táboas, Reference Roesler and González Táboas2016). The literature on the cestode parasites of Argentinean birds is scattered, and the studies have focused mainly on taxonomy and host–parasite associations.

The aim of this paper was to compile and summarize all the published reports about adult cestodes of wild birds from Argentina based on original records.

Material and methods

The data set was generated based on an extensive search of specialized literature published until April 2021. This information was obtained from the following databases: Host–Parasite Database of the Natural History Museum, London (Gibson et al., Reference Gibson, Bray and Harris2005), Global Cestoda Database (Caira et al., Reference Caira, Jensen and Barbeau2012), Google scholar, Scopus and Research Gate. We also made an exhaustive search for published literature in the Florentino Ameghino Library (Museo de La Plata, Argentina) and the FCAyF-FCV Library (Universidad Nacional de La Plata, Argentina). Those species reported in thesis, dissertations and scientific meetings were not listed, because they represent informal publications. Also, only wild birds were included on the list, domestic birds were not considered. Each taxonomic category of Cestoda is presented in alphabetical order. Each record contains information on the species or generic name, taxonomic authority, host(s), site of infection (SI), localities (particular locality, geographical coordinates when reported in the original paper and province) (Lo), lot numbers and collection acronyms when material was deposited, and bibliographical references. The classification for Cyclophyllidea (family and genus) and Tetrabothriidea (family, genus, subgenus and species) follows Caira & Jensen (Reference Caira and Jensen2017) and Diphyllobothriidea (family, genus and species) follows Waeschenbach et al. (Reference Waeschenbach, Brabec, Scholz, Littlewood and Kuchta2017). The taxonomy of birds follows AVIBASE (Lepage, Reference Lepage2019). Abbreviations used for the biological collections are as follows: CHIOC (Coleção Helmintológica do Instituto Oswaldo Cruz, Rio de Janeiro, Brazil); CNP–Par (Collection of the Centro Nacional Patagónico, Puerto Madryn, Argentina); IPCAS Helm. Coll (Helminthological Collection of the Institute of Parasitology, Biology Centre of the Czech Academy of Sciences, České Budějovice, Czech Republic); MNHG (Muséum d'Histoire Naturelle of Geneva, Switzerland); MLP–He, in some cases as CHMLP in the original papers (Colección Helmintológica del Museo de La Plata, Buenos Aires Province, Argentina); NHMUK (the Natural History Museum, London, UK), in some cases as BMNH (British Museum of Natural History) in the original papers; MACN–pa (colección de parasitología, Museo Argentino de Ciencias Naturales ‘Bernadino Rivadavia’, Buenos Aires, Argentina); USNM Helm. Coll. (US National Museum Helminthological Collection – currently, National Parasite Collection).

Results

At present, 38 papers have been published on some aspects of cestodes infecting Argentinean wild birds, most of them are related to morphological studies, taxonomic aspects and host–parasite associations. Only one study provides molecular data on Dibothriocephalus dendriticus (Nitzsch, 1824) parasitizing gulls (Casalins et al., Reference Casalins, Arbetman, Semenas, Veleizán, Flores and Viozzi2015), and another provides data on pathological effects caused by Confluaria podicipina (Szymanski, 1905) in grebes (Guagliardo et al., Reference Guagliardo, Graff, Gigola and Tanzola2020).

The checklist on cestode parasites of wild birds in Argentina comprises records on 34 nominal species and 11 taxa identified at generic level, belonging to three orders, ten families and 35 genera associated with 29 species of Argentinean birds (seven species of Anseriformes and Charadriiformes, four species of Pelecaniformes, two species of Cuculiformes, Podicipediformes and Tinamiformes; and one species of Gruiformes, Passeriformes, Piciformes, Sphenisciformes and Trogoniformes).

Reports of 62 host–parasite associations were found; 78% correspond to species of cestodes recovered from a single host species, 13%, 7% and 2% recovered from two, three and eight species of birds, respectively.

Parasite-host list

Class: Cestoda

Order: Cyclophyllidea

Acoleidae Fuhrmann, 1899

Acoleus Fuhrmann, 1899

Acoleus vaginatus (Rudolphi, 1819) Fuhrmann, 1900

Host. Vanellus chilensis lampronotus (Wagler) (cited as Belonopterus cayennense lampronotus).

SI. Small intestine.

Lo. La Plata Zoological Garden, Buenos Aires Province.

Reference. Boero & Led (Reference Boero and Led1968).

Diplophallus Fuhrmann, 1900

Diplophallus polymorpus (Rudolphi, 1819) Fuhrmann, 1900

Host. Himantopus melanurus Vieillot (cited as Himantopus himantopus melanurus).

SI. Small intestine.

Lo. La Plata Zoological Garden, Buenos Aires Province.

Reference. Boero & Led (Reference Boero and Led1968).

Davaineidae Braun, 1900

Davainea Blanchard 1891

Davainea himantopodis Johnston, 1911

Host. Himantopus melanurus Vieillot.

SI. Intestine.

Lo. Mar Chiquita coastal Lagoon and Chascomús lagoon, Buenos Aires Province; Mar Chiquita lagoon, Córdoba Province.

Reference. Tanzola (Reference Tanzola1989).

Raillietina Fuhrmann, 1920

Raillietina sp.

Host. Nothura maculosa annectens Conover.

SI. Small intestine.

Lo. Not reported.

Reference. Bump & Bump (Reference Bump and Bump1969).

Dilepididae Fuhrmann, 1907

Alcataenia Spasskaya, 1971

Alcataenia dominicana (Railliet & Henry, 1912) Hoberg, 1984

Host. Larus dominicanus Lichtenstein.

SI. Intestine.

Lo. Mar del Plata (38°05′S, 57°38′W), Buenos Aires Province.

Reference. Labriola & Suriano (Reference Labriola and Suriano2001).

Host. Chroicocephalus cirrocephalus (cited as Larus cirrocephalus).

SI. Small intestine.

Lo. Mar del Plata (38°05′S, 57°38′W), Buenos Aires Province.

Reference. Labriola & Suriano (Reference Labriola and Suriano2001).

Anomotaenia Cohn, 1900

Anomotaenia dominicana (Railliet & Henry, 1912) Schmidt, 1986

Host. Larus dominicanus Lichtenstein (cited as Larus marinus dominicanus).1

SI. Intestine.

Lo. Santa Fe Province1; San Carlos de Bariloche (41°03′S, 75°25′W), Río Negro Province1; Rosario Lake (43°15′S, 71°20′W)2 and Península Valdés (42°04′–42°53′S; 63°38′–64°30′W),3 Chubut Province.

Comment. Described as Paricterotaenia australis. 1 For synonyms, see Zdzitowiecki & Cielecka (Reference Zdzitowiecki and Cielecka1984) and Rocka (Reference Rocka, Klimpel, T and H2017).

References. 1Szidat (Reference Szidat1964), 2Kreiter & Semenas (Reference Kreiter and Semenas1997), 3Diaz et al. (Reference Diaz, Cremonte and Navone2011).

Apoliga Bona, 1994

Apoliga imperialis Bona, 1994

Host. Colaptes melanolaimus (Malherbe) (cited as Chrysoptilus melanolaimus).

SI. Intestine.

Lo. Monte, Buenos Aires Province.

Material deposited. MNHG 982.1859, 1861.

Reference. Bona (Reference Bona1994).

Apoliga sp.

Host. Colaptes melanolaimus (Malherbe) (cited as Chrysoptilus melanolaimus).

SI. Intestine.

Lo. Monte, Buenos Aires Province.

Reference. Bona (Reference Bona1994).

Choanotaenia Railliet 1896

Choanotaenia meridionalis Szidat, 1964

Host. Larus dominicanus Lichtenstein (cited as Larus marinus dominicanus).

SI. Small intestine.

Lo. Santa Fe Province; Puerto Quequén and Tandil, Buenos Aires Province.

Reference. Szidat (Reference Szidat1964).

Host. Chroicocephalus maculipennis (cited as Larus ridibundus maculipennis).

SI. Intestine.

Lo. Santa Fe Province; Puerto Quequén and Tandil, Buenos Aires Province.

Reference. Szidat (Reference Szidat1964).

Choanotaenia sp.

Host. Nothura darwinii darwinii Gray.

SI. Small intestine.

Lo. Not reported.

Reference. Bump & Bump (Reference Bump and Bump1969).

Cotylorhipis Blanchard, 1909

Cotylorhipis furnarii (Marco Del Pont, 1906) Blanchard, 1909

Host. Furnarius rufus (Gmelin).

SI. Small intestine.

Lo. Not reported.

Comment. This material was described as Taenia furnarii 1 and then transferred as type species of a new genus.2

References. 1Marcó del Pont (Reference Marcó del Pont1906), 2Blanchard (Reference Blanchard1909).

Liga Weinland, 1857

Liga sp.

Host. Oreopholus ruficollis (Wagler).

SI. Intestine.

Lo. La Plata Zoological Garden, Buenos Aires Province.

Reference. Boero & Led (Reference Boero and Led1968).

Monopylidium Fuhrmann, 1899

Monopylidium cayennense Fuhrmann, 1907

Host. Vanellus chilensis cayennensis (Gmelin) (cited as Vanellus cayennensis).

SI. Intestine.

Lo. Buenos Aires Province.

Reference. Parona (Reference Parona1900).

Monopylidium secundum Fuhrmann, 1907

Host. Vanellus chilensis cayennensis (Gmelin) (cited as Belonopterus cayennense).

SI. intestine.

Lo. Buenos Aires Province.

Reference. Parona (Reference Parona1900).

Paricterotaenia Fuhrmann, 1932

Paricterotaenia porosa (Rudolphi, 1810) Fuhrmann, 1932

Host. Chroicocephalus cirrocephalus (cited as Larus cirrocephalus).

SI. Intestine.

Lo. Mar del Plata (38°05′S, 57°38′W), Buenos Aires Province.

Reference. Labriola & Suriano (Reference Labriola and Suriano2001).

Host. Chroicocephalus maculipennis (Lichtenstein) (cited as Larus maculipennis).

SI. Intestine.

Lo. Mar del Plata (38°05′S, 57°38′W), Buenos Aires Province.

Reference. Labriola & Suriano (Reference Labriola and Suriano2001).

Host. Larus dominicanus Lichtenstein.

SI. Intestine.

Lo. Mar del Plata (38°05′S, 57°38′W), Buenos Aires Province.

Reference. Labriola & Suriano (Reference Labriola and Suriano2001).

Dioicocestidae Southwell, 1930

Dioicocestus Fuhrmann, 1900

Dioicocestus paronai Fuhrmann, 1900

Host. Plegadis chihi (Vieillot) (cited as Plegadis guarauna).

SI. Intestine.

Lo. Buenos Aires Province.

Comment. Mentioned by Parona (Reference Parona1900) as Dioecocestus paronai; Caira & Jensen (Reference Caira and Jensen2017) considered the spellings, Dioecocestus and Dioecocestidae, erroneous.

References. Fuhrmann (Reference Fuhrmann1900), Parona (Reference Parona1900).

Host. Rollandia rolland (Quoy & Gaimard).

SI. Small intestine.

Lo. Chascomús lagoon (35°35′29″S, 58°01′28″W), Mar Chiquita lagoon (37°46′S, 57°27′W), Villa Arias (38°52′00″S, 62°05′00″W) and Los Talas ponds (34°55′44″S, 57°43′04″W), Buenos Aires Province.

Material deposited. MLP-He 7567.

Comment. Mentioned as Dioecocestus paronai.

Reference. Tanzola et al. (Reference Tanzola, Guagliardo and Gigola2019).

Gyrocoelia Fuhrmann, 1899

Gyrocoelia leuce Fuhrmann, 1900

Host. Vanellus chilensis cayennensis (Gmelin) (cited as Vanellus cayennensis).

SI. Intestine.

Lo. Buenos Aires Province.

Comment. The specimens cited by Parona were sent to Fuhrmann, who described the species, but erroneously reported the locality as Brazil.

References. Fuhrmann (Reference Fuhrmann1900), Parona (Reference Parona1900).

Gryporhynchidae Spasskii & Spasskaya, 1973

Cyclorchida Fuhrmann, 1907

Cyclorchida sp.

Host. Larus dominicanus Lichtenstein (cited as Larus marinus dominicanus).

SI. Intestine.

Lo. Santa Fe Province.

Reference. Szidat (Reference Szidat1964).

Dendrouterina Fuhrmann, 1912

Dendrouterina pilherodiae Mahon, 1956

Dendrouterina pilherodiae meridionalis Bona, 1983

Host. Ardea alba Linnaeus (cited as Egretta alba).

SI. Intestine.

Lo. Corrientes, Corrientes Province, Villa Constitución (Paraná River), Santa Fe Province.

Material deposited. MACN–pa unnumbered (Syntypes), USNM Helm. Coll. 77,134 and 77,135 (Syntypes).

References. Bona (Reference Bona1983a, Reference Bonab).

Paradilepis Hsü, 1935

Paradilepis sp.

Host. Platalea ajaja Linnaeus (cited as Ajaia ajaia).

SI. Small intestine.

Lo. La Plata Zoological Garden, Buenos Aires Province.

Reference. Boero & Led (Reference Boero and Led1968).

Hymenolepididae Perrier, 1897

Aploparaksis Сlегс, 1903

Aploparaksis (Aploparaksis) americanensis Bondarenko & Kontrimavichus, 2001

Host. Gallinago paraguaiae (Vieillot) (cited as Gallinago paraguaica).

SI. Small intestine.

Lo. Patagonia.

Material deposited. NHMUK 203–212 (previously designated as A. filum (Goeze, 1782) in this collection).

References. Bondarenko & Kontrimavichus (Reference Bondarenko and Kontrimavichus2001, Reference Bondarenko and Kontrimavichus2018).

Cloacotaenia Wolffhügel, 1938

Cloacotaenia megalops (Nitzsch in Creplin, 1829) Wolffhügel, 1938

Host. Anas bahamensis rubrirostris Vieillot.

SI. Cloaca.

Lo. Saladillo, Buenos Aires Province.

Material deposited. MLP-He 3745-4.

Comment. Cited as Hymenolepis megalops.

Reference. Digiani (Reference Digiani2000).

Host. Probably Anas georgica spinicauda Vieillot (cited as pato maicero or Paecilonitta spinicauda).

SI. Cloaca.

Lo. 25 de Mayo, Buenos Aires Province.

Reference. Boero et al. (Reference Boero, Led and Brandetti1972b).

Host. Anas sp.

SI. Cloaca.

Lo. Punta Blanca, Buenos Aires Province.

Material deposited. MLP-He 3742.

Comment. Cited as Hymenolepis megalops.

Reference. Digiani (Reference Digiani2000).

Host. Cygnus melancoryphus (Molina).

SI. Cloaca.

Lo. Chascomús, Buenos Aires Province.

Material deposited. MLP-He 3744.

Comment. Cited as Hymenolepis megalops.

Reference. Digiani (Reference Digiani2000).

Host. Dendrocygna viduata (Linnaeus).

SI. Cloaca.

Lo. 25 de Mayo, Buenos Aires Province.

Reference. Boero et al. (Reference Boero, Led and Brandetti1972b).

Host. Netta peposaca (Vieillot).

SI. Cloaca.

Lo. General Belgrano, Buenos Aires Province.

Material deposited. MLP-He 3743-2.

Comment. Cited as Hymenolepis megalops.

Reference. Digiani (Reference Digiani2000).

Host. Plegadis chihi (Vieillot).

SI. Cloaca.

Lo. Punta Blanca, Buenos Aires Province.

Material deposited. MLP-He 3882-3, 3858-1, 3855-4, 3779-3, 3732-4.

Comment. Cited as Hymenolepis megalops.

Reference. Digiani (Reference Digiani2000).

Host. Spatula cyanoptera (Vieillot) (cited as Querquedula cyanoptera).

SI. Cloaca.

Lo. 25 de Mayo, Buenos Aires Province.

Reference. Boero et al. (Reference Boero, Led and Brandetti1972b).

Host. Spatula versicolor (Vieillot) (cited as Querquedula versicolor).

SI. Cloaca.

Lo. 25 de Mayo, Buenos Aires Province.

Reference. Boero et al. (Reference Boero, Led and Brandetti1972b).

Confluaria Ablasov in Spasskaya, 1966

Confluaria podicipina (Szymanski, 1905) Spasskaya, 1966

Host. Podiceps occipitalis Garnot.

SI. Crypts of Lieberkuhn, intestine.

Lo. Epecuén lagoon (37°08′04″S, 62°51′57″W), Buenos Aires Province.

Reference. Guagliardo et al. (Reference Guagliardo, Graff, Gigola and Tanzola2020).

Dicranotaenia Railliet, 1892

Dicranotaenia coronula (Dujardin, 1845) Railliet, 1892

Host. Butorides striata (Linnaeus) (cited as Butorides striatus).

SI. Intestine.

Lo. Salado River, Santa Fe Province.

Comment. Cited as Hymenolepis coronula.

Reference. Estebon de Ulibarrie & Beltzer (Reference Estebon de Ulibarrie and Beltzer1998).

Diorchis Clerc, 1903

Diorchis pararansomi Tanzola, 1992

Host. Fulica armillata Vieillot.

SI. Small intestine.

Lo. Pellegrini Lake (38°40′S, 68°00′W), Río Negro Province.

Material deposited. MLP-He 3153 (holotype and paratype).

Reference. Tanzola (Reference Tanzola1992).

Diploposthe Jacobi, 1896

Diploposthe laevis (Bloch, 1782) Jacobi, 1896

Host. Netta peposaca (Vieillot).

SI. Intestine (anterior jejunum–ileum).

Lo. Alvear (29°09′13″S, 56°54′34″W), Corrientes Province.

Material deposited. CHIOC 36,967.

Reference. Silveira & Amato (Reference Silveira and Amato2008).

Echinocotyle Blanchard, 1891

Echinocotyle echinocotyle (Fuhrmann, 1907) Yamaguti, 1959

Host. Cygnus melancoryphus (Molina).

SI. Small intestine.

Lo. Laguna del Monte, Buenos Aires Province.

Reference. Boero et al. (Reference Boero, Led and Brandetti1972a).

Echinocotyle sp.

Host. Dendrocygna viduata (Linnaeus).

SI. Small intestine.

Lo. 25 de Mayo, Buenos Aires Province.

Reference. Boero et al. (Reference Boero, Led and Brandetti1972b).

Host. Spatula cyanoptera (Vieillot) (cited as Querquedula cyanoptera).

SI. Small intestine.

Lo. 25 de Mayo, Buenos Aires Province.

Reference. Boero et al. (Reference Boero, Led and Brandetti1972b).

Host. Spatula versicolor (Vieillot) (cited as Querquedula versicolor).

SI. Small intestine.

Lo. 25 de Mayo, Buenos Aires Province.

Reference. Boero et al. (Reference Boero, Led and Brandetti1972b).

Gastrotaenia Wolffhügel, 1938

Gastrotaenia cygni Wolffhügel, 1938

Host. Cygnus melancoryphus (Molina).

SI. Small intestine.

Lo. Laguna del Monte, Buenos Aires Province.

Reference. Boero et al. (Reference Boero, Led and Brandetti1972a).

Hymenolepis Weinland, 1858

Hymenolepis sp.

Host. Nothura maculosa nigroguttata Salvadori.

SI. Not reported.

Lo. Buenos Aires Province.

Reference. Boero et al. (Reference Boero, Menéndez, Led and Brandetti1968).

Microsomacanthus López Neyra, 1942

Microsomacanthus hopkinsi (Schiller, 1951) Spasskaya, 1966

Host. Netta peposaca (Vieillot).

SI. Anterior portion of caeca.

Lo. Alvear (29°09′13″S, 56°54′34″W), Corrientes Province.

Material deposited. CHIOC 3745a-b.

Reference. Silveira & Amato (Reference Silveira and Amato2010).

Microsomacanthus shetlandicus Cielecka & Zdzitoweicki, 1981

Host. Chroicocephalus maculipennis (Lichtenstein) (cited as Larus maculipennis).

SI. Duodenum, ileum.

Lo. Mar del Plata (38°05′S, 57°38′W), Buenos Aires Province.

Reference. Labriola & Suriano (Reference Labriola and Suriano2001).

Host. Larus dominicanus Lichtenstein.

SI. Duodenum, ileum.

Lo. Mar del Plata (38°05′S, 57°38′W), Buenos Aires Province.

Reference. Labriola & Suriano (Reference Labriola and Suriano2001).

Wardium Mayhew, 1925

Wardium paucispinosum Labriola & Suriano, 2000

Host. Chroicocephalus maculipennis (Lichtenstein) (cited as Larus maculipennis).

SI. Ileum.

Lo. Mar del Plata (38°05′S, 57°38′W), Buenos Aires Province.

Material deposited. MACN–pa 380/1, 380/2 (holotype), IPCAS C-311 (paratypes).

References. Labriola & Suriano (Reference Labriola and Suriano2000, Reference Labriola and Suriano2001).

Wardium semiductilis (Szidat, 1964) Labriola & Suriano, 2000

Host. Chroicocephalus maculipennis (Lichtenstein) (cited as Larus ridibundus maculipennis,1 Larus maculipennis 2).

SI. Intestine.

Lo. Río Paraná, Santa Fé Province.

Comment. Originally described as Hymenolepis semiductilis by Szidat (Reference Szidat1964), Labriola & Suriano (Reference Labriola and Suriano2000) re-examined this material and transferred it to Wardium.

Material deposited. MACN–pa 50/1, 50/2.2

References. 1Szidat (Reference Szidat1964), 2Labriola & Suriano (Reference Labriola and Suriano2000).

Host. Larus dominicanus Lichtenstein (cited as Larus marinus dominicanus 1).

SI. Intestine.

Lo. Río Paraná, Santa Fé Province.

Material deposited. MACN–pa 50/1, 50/2.2

References. 1Szidat (Reference Szidat1964), 2Labriola & Suriano (Reference Labriola and Suriano2000).

Mesocestoididae Perrier, 1897

Mesocestoides Vaillant, 1863

Mesocestoides sp.

Host. Larus dominicanus Lichtenstein (cited as Larus marinus dominicanus).

SI. Intestine.

Lo. Santa Fe Province.

Reference. Szidat (Reference Szidat1964).

Paruterinidae Fuhrmann, 1907

Anonchotaenia Cohn, 1900

Anonchotaenia longiovata (Fuhrmann, 1901) Rausch & Morgan, 1947

Host. Plegadis chihi (Vieillot) (cited as Plegadis guaruana).

SI. Intestine.

Lo. Buenos Aires Province.

Comment. Mentioned – without description – as Taenia longiovata by Parona (Reference Parona1900), described as Anurina longiovata by Fuhrmann (Reference Fuhrmann1901) and moved to Anonchotaenia by Rausch & Morgan (Reference Rausch and Morgan1947).

References. Parona (Reference Parona1900), Fuhrmann (Reference Fuhrmann1901).

Francobona Georgiev & Kornyushin, 1994

Francobona similis (Ransom, 1909) Georgiev & Kornyushin, 1994

Host. Coccyzus melacoryphus Vieillot.

SI. Not reported.

Lo. Misiones Province.

Comment. Cited as Paruterina similis.

References. Bona & Maffi (Reference Bona and Maffi1984a, Reference Bona and Maffi1985).

Francobona similita (Bona & Maffi, 1984) Georgiev & Kornyushin, 1994

Host. Coccyzus melacoryphus Vieillot.

SI. Intestine.

Lo. Dos de Mayo, Misiones Province.

Material deposited. MACN–pa 70 (syntypes).

Comment. Described as Paruterina similita.

References. Bona & Maffi (Reference Bona and Maffi1984a, Reference Bona and Maffib).

Host. Piaya cayana mogenseni Peters.

SI. Intestine.

Lo. Río Tarija, Salta Province, and Yuto, Jujuy Province.

Material deposited. MACN–pa 74a, 58b (paratypes).

Comment. Described as Paruterina similita.

Reference. Bona & Maffi (Reference Bona and Maffi1984b).

Triaenorhina Spasskii & Shumilo, 1965

Triaenorhina sp.

Host. Piaya cayana (Linnaeus).

SI. Intestine.

Lo. Misiones Province.

Comment. Cited with doubts as Paruterina or Triaenorhina sp.

Reference. Bona & Maffi (Reference Bona and Maffi1984a).

Host. Piaya cayana mogenseni Peters.

SI. Intestine.

Lo. Río Tarija, Salta Province.

Material deposited. MACN–pa 74a.

Comment. The authors raise doubts about the validity of the genus and its possible synonymy with Paruterina.

Reference. Bona & Maffi (Reference Bona and Maffi1984b).

Troguterina Spasskii, 1991

Troguterina disparuncinata (Bona, Bosco & Maffi, 1986) Spasskii, 1991

Host. Trogon curucui Linnaeus.

SI. Intestine.

Lo. Río Tarija, Salta Province.

Material deposited. MACN–pa 80, USNM Helm. Coll. 78,751.

Comment. Described as Paruterina sp.1 and Paruterina disparuncinata. 2

References. 1Bona & Maffi (Reference Bona and Maffi1984a), 2Bona et al. (Reference Bona, Bosco and Maffi1986).

Order: Diphyllobothriidea Kuchta, Scholz, Brabec & Bray, 2008

Diphyllobothriidae Lühe, 1910

Dibothriocephalus Lühe, 1899

Dibothriocephalus dendriticus (Nitzsch, 1824) Lühe, 1899

Host. Larus dominicanus Lichtenstein (cited as Larus marinus dominicanus).1,2

SI. Small intestine.

Lo. Nahuel Huapi Lake, San Carlos de Bariloche, Río Negro Province1,2,4; San Carlos de Bariloche (41°03′S–75°25′W), Río Negro Province.3

Comment. Described as Diphyllobothrium microcordiceps by Szidat & Soria (Reference Szidat and Soria1957) and Szidat (Reference Szidat1964); reported as Diphyllobothrium dendriticum by Kreiter & Semenas (Reference Kreiter and Semenas1997). For synonyms see Semenas et al. (Reference Semenas, Viozzi and Arbetman2021).

References. 1Szidat & Soria (Reference Szidat and Soria1957), 2Szidat (Reference Szidat1964), 3Kreiter & Semenas (Reference Kreiter and Semenas1997), 4Casalins et al. (Reference Casalins, Arbetman, Semenas, Veleizán, Flores and Viozzi2015).

Order: Tetrabothriidea Baer, 1954

Tetrabothriidae Linton, 1889

Tetrabothrius Rudolphi, 1819

Tetrabothrius argentinum Szidat, 1964

Comment. Originally described by Szidat (Reference Szidat1964) as Tetrabothrium argentinum. Considered as Incertae sedis with respect to subgeneric assignment by Mariaux et al. (Reference Mariaux, Kuchta, Hoberg, Caira and K2017).

Host. Chroicocephalus cirrocephalus (cited as Larus cirrocephalus).

SI. Intestine.

Lo. Mar del Plata (38°05′S, 57°38′W), Buenos Aires Province.

Reference. Labriola & Suriano (Reference Labriola and Suriano2001).

Host. Chroicocephalus maculipennis (cited as Larus ridibundus maculipennis,1 Larus maculipennis 2).

SI. Intestine.

Lo. Santa Fé Province1; Puerto Quequén,1 Tandil1 and Mar del Plata (38°05′S, 57°38′W),2 Buenos Aires Province.

References. 1Szidat (Reference Szidat1964), 2Labriola & Suriano (Reference Labriola and Suriano2001).

Host. Larus dominicanus Lichtenstein (cited as Larus marinus dominicanus 1).

SI. Intestine.

Lo. Santa Fé Province1; Puerto Quequén,1 Tandil1 and Mar del Plata (38°05′S, 57°38′W)2, Buenos Aires.

References. 1Szidat (Reference Szidat1964), 2Labriola & Suriano (Reference Labriola and Suriano2001).

Tetrabothrius (Neotetrabothrius) lutzi Parona, 1901

Host. Spheniscus magellanicus (Forster).

SI. Small intestine.

Lo. La Plata Zoological Garden, Buenos Aires Province,1 Estancia San Lorenzo (42°04′S, 63°21′W)2 and Península Valdés (42°04′–42°53′S; 63°38′–64°30′W),3 Chubut Province.

Material deposited. MLP-He 6084.3

Comment. Cited as Tetrabothrius lutzi.

References. 1Boero et al. (Reference Boero, Led and Brandetti1972a), 2Pazos et al. (Reference Pazos, Laurenti and Diaz2003), 3Diaz et al. (Reference Diaz, Cremonte and Navone2010).

Tetrabothrius (Culmenamniculus) cylindraceus (Rudolphi, 1819)

Host. Larus dominicanus Lichtenstein.

SI. Intestine.

Lo. Península Valdés (42°04′–42°53′S; 63°38′–64°30′W), Chubut Province.

Material deposited. MLP-He 6304, CNP-Par 7.

Comment. Cited as Tetrabothrius cylindraceus.

Reference. Diaz et al. (Reference Diaz, Cremonte and Navone2011).

Tetrabothrius sp.

Host. Larus dominicanus Lichtenstein.

SI. Not reported.

Lo. San Carlos de Bariloche (41°03′S, 75°25′W), Río Negro Province.

Reference. Kreiter & Semenas (Reference Kreiter and Semenas1997).

Species inquirenda

Aploparaksis primus Szidat, Reference Szidat1964 (Hymenolepididae): this species was briefly described by Szidat (Reference Szidat1964) parasitizing Larus dominicanus Lichtenstein from Paraná River, Santa Fé Province. The original description lacks information about the scolex and other morphological features. Bondarenko & Kontrimavichus (Reference Bondarenko and Kontrimavichus2018) considered it as species inquirenda.

Host–parasite list

Order: Anseriformes

Anatidae

Anas bahamensis rubrirostris

Cloacotaenia megalops

Anas georgica spinicauda

Cloacotaenia megalops

Anas sp.

Cloacotaenia megalops

Cygnus melancoryphus

Echinocotyle echinocotyle

Cloacotaenia megalops

Gastrotaenia cygni

Dendrocygna viduata

Cloacotaenia megalops

Echinocotyle sp.

Netta peposaca

Cloacotaenia megalops

Diploposthe laevis

Microsomacanthus hopkinsi

Spatula cyanoptera

Cloacotaenia megalops

Echinocotyle sp.

Spatula versicolor

Cloacotaenia megalops

Echinocotyle sp.

Order: Charadriiformes

Charadriidae

Oreopholus ruficollis

Liga sp.

Vanellus chilensis cayennensis

Gyrocoelia leuce

Monopylidium cayennense

Monopylidium secundum

Vanellus chilensis lampronotus

Acoleus vaginatus

Laridae

Chroicocephalus cirrocephalus

Alcataenia dominicana

Paricterotaenia porosa

Tetrabothrius argentinum

Chroicocephalus maculipennis

Choanotaenia meridionalis

Microsomacanthus shetlandicus

Paricterotaenia porosa

Tetrabothrius argentinum

Wardium paucispinosum

Wardium semiductilis

Larus dominicanus

Alcataenia dominicana

Anomotaenia dominicana

Choanotaenia meridionalis

Cyclorchida sp.

Dibothriocephalus dendriticus

Mesocestoides sp.

Microsomacanthus shetlandicus

Paricterotaenia porosa

Tetrabothrius argentinum

Tetrabothrius (Culmenamniculus) cylindraceus

Tetrabothrius sp.

Wardium semiductilis

Recurvirostridae

Himantopus melanurus

Davainea himantopodis

Diplophallus polymorpus

Scolopacidae

Gallinago paraguaiae

Aploparaksis americanensis

Order Cuculiformes

Cuculidae

Coccyzus melacoryphus

Francobona similis

Francobona similita

Piaya cayana mogenseni

Francobona similita

Triaenorhina sp.

Order: Gruiformes

Rallidae

Fulica armillata

Diorchis pararansomi

Order: Passeriformes

Furnariidae

Furnarius rufus

Cotylorhipis furnariid

Order: Pelecaniformes

Ardeidae

Ardea alba

Dendrouterina pilherodiae meridionalis

Butorides striata

Dicranotaenia coronula

Threskiornithidae

Platalea ajaja

Paradilepis sp.

Plegadis chihi

Anonchotaenia longiovata

Cloacotaenia megalops

Dioecocestus paronai

Order: Piciformes

Picidae

Colaptes melanolaimus

Apoliga imperialis

Apoliga sp.

Order: Podicipediformes

Podicipedidae

Podiceps occipitalis

Confluaria podicipina

Rollandia rolland

Dioecocestus paronai

Order: Sphenisciformes

Spheniscidae

Spheniscus magellanicus

Tetrabothrius (Neotetrabothrius) lutzi

Order: Tinamiformes

Tinamidae

Nothura darwinii

Choanotaenia sp.

Nothura maculosa annectens

Raillietina sp.

Nothura maculosa nigroguttata

Hymenolepis sp.

Order: Trogoniformes

Trogonidae

Trogon curucui

Troguterina disparuncinata

Discussion

In this work, we found reports of 34 nominal species of cestodes from Argentinean birds. Probably this number does not reflect the true diversity in this group of vertebrates. Carlson et al. (Reference Carlson, Dallas, Alexander, Phelan and Phillips2020) estimated that only 16% of helminths parasites of birds are known, and that the group best represented are cestodes, followed by trematodes, nematodes and acanthocephalans. In Argentinean birds, the groups of helminths most studied are the digeneans and nematodes, with 112 and 64 nominal species reported, respectively (Drago & Lunaschi, Reference Drago and Lunaschi2015; Drago et al., Reference Drago, Núñez and Dueñas Díaz2020), while the acanthocephalans are the least frequent group, with only seven species recovered (Hernández-Orts et al., Reference Hernández-Orts, Kuchta, Semenas, Crespo, González and Aznar2019). The lower number of species of cestodes in Argentinean birds, compared to global estimates for this group of vertebrates, could be related to the low number of cestodologists working in birds, since most have focused their studies on marine and freshwater fishes (see Alves et al., Reference Alves, de Chambrier, Scholz and Luque2017).

The first reports of cestodes from Argentinean wild birds were carried out by an Italian scientist, Corrado Parona. This author reported several species of helminths parasitizing vertebrates from material that was sent to him by the director of the Museo Argentino de Ciencias Naturales, Carlos Berg (Parona, Reference Parona1900). In this publication, five species of cestodes were mentioned parasitizing wild birds, that were later described by Fuhrmann (Reference Fuhrmann1900, Reference Fuhrmann1901, Reference Fuhrmann1907). During the following 62 years (1901–1963) only two papers were published (Marcó del Pont, Reference Marcó del Pont1906; Szidat & Soria, Reference Szidat and Soria1957). Between 1964 and 1972, six papers were published on the cestodes of wild birds; in this period, the publication made by the European biologist Lothar Szidat is particularly remarkable. Szidat published an extensive work in which he described numerous species of flatworms parasitizing larid birds – among them, seven taxa of cestodes (Szidat, Reference Szidat1964). Also remarkable are the contributions of veterinarians, Juan José Boero and Jorge Eugenio Led (Boero & Led, Reference Boero and Led1968; Boero et al., Reference Boero, Menéndez, Led and Brandetti1968; Boero et al., Reference Boero, Led and Brandetti1972a, Reference Boero, Led and Brandettib). In the 1980s and 1990s the contributions of Franco Bona and Ruben Daniel Tanzola are notable (Bona, Reference Bona1983a, Reference Bonab, Reference Bona1994; Bona & Maffi, Reference Bona and Maffi1984a, Reference Bona and Maffib, Reference Bona and Maffi1985; Bona et al., Reference Bona, Bosco and Maffi1986; Tanzola, Reference Tanzola1989, Reference Tanzola1992). From 2000 to the present, only ten contributions have been made.

When comparing the number of species of cestodes in Argentinean birds with the richness found in other regions of South America – for example, Chile – with less than a half of the bird species reported in Argentina (443 vs. 1042 bird species), similar numbers of cestodes species can be observed. Oyarzún-Ruiz & González-Acuña (Reference Oyarzún-Ruiz and González-Acuña2021) found reports of 29 nominal species of cestodes and 16 taxa identified at generic level, parasitizing 38 bird species, which represents 8.6% of the birds present in Chile. In addition, they established that the best represented groups in Chilean birds were the nematodes followed by the cestodes and digeneans. In Brazil, a country with almost twice the number of reported bird species than in Argentina, the number of species of cestodes recovered is almost four times higher. Justo et al. (Reference Justo, Fernandes, Knoff, Cárdenas and Cohen2017) listed 126 nominal species of cestodes and 13 taxa identified at generic level, parasitizing 139 bird species, which represents 7.6% of the birds present in this country.

In Argentinean wild birds, the highest number of taxa of cestodes was recorded in the family Hymenolepididae, with 12 nominal species and two taxa identified at generic level, followed by Dilepididae, with eight nominal species and three taxa identified at generic level. Most of the hymenolepidids were associated with birds related to aquatic environments (14 species of aquatic birds and one terrestrial), while dilepidids were recovered both in birds with terrestrial and aquatic habits (four species of birds in each case). Dibothriocephalus dendriticus is the only species of cestode that has been molecularly characterized in both its definitive hosts (gulls) and its intermediate hosts (fishes) (Casalins et al., Reference Casalins, Arbetman, Semenas, Veleizán, Flores and Viozzi2015; Semenas et al., Reference Semenas, Viozzi and Arbetman2021).

Of the 1042 species of birds belonging to 86 families reported in Argentina (Roesler & González Táboas, Reference Roesler and González Táboas2016), only 29 bird species (2.8%) grouped into 14 families have been reported to be parasitized by adult cestodes.

Most of the parasitic taxa were reported in a single bird species (78%), followed by 20% recovered in two or three species of birds, and 2% recovered in eight species of birds (represented by a single species, C. megalops). This does not mean that most of these species are specialist species, since most of them have been reported in more than one species of birds in other regions.

The families of birds with the highest number of reported taxa are Laridae and Anatidae, with 20 and 14 taxa, respectively. The bird species with the highest number of taxa of cestodes reported are L. dominicanus and C. maculipennis, with 12 and 6 taxa reported, respectively. The helminths of L. dominicanus have been studied in numerous opportunities, being also the bird species with the highest number of digenean and nematode species reported in Argentina (Lunaschi et al., Reference Lunaschi, Cremonte and Drago2007; Drago & Lunaschi, Reference Drago and Lunaschi2015; Drago et al., Reference Drago, Núñez and Dueñas Díaz2020). This species is an abundant bird that inhabits a great diversity of environments and has a generalist and opportunistic diet (Yorio et al., Reference Yorio, Marinao, Retana and Suárez2013), which means that it would be more likely to acquire a wide variety of helminths with an indirect life cycle.

Reports of cestodes parasitizing wild birds were found in nine of the 23 Argentinean provinces. Most of the studies were carried out in Central Argentina, with 63 reports (23, 13 and three in Buenos Aires, Santa Fé and Córdoba provinces, respectively). In the Patagonian Region, 12 reports were found (six in Río Negro Province, five in Chubut Province and one unspecified locality). In the Northeast Region, five reports were found (three in Corrientes Province and two in Misiones Province). In the Northwest Region, four reports were found (three in Salta Province and one in Jujuy Province). In the Cuyo Region, no cestodes have been reported parasitizing wild birds. Similarly, most of the reports of digeneans and nematodes have been made in Buenos Aires Province. This seems to be more related to the development of these lines of work in scientific research centres in this province, than with the real diversity in each province.

These results highlight the need for further research on this group of parasites, expanding the number of bird species examined, especially in poorly explored regions.

Acknowledgements

The authors express their gratitude to Gergana P. Vasileva for selflessly providing the specific bibliography related to Franco Bona. The authors express their appreciation to the reviewers for the critical and rigorous assessment of the work done, as well as their human warmth. Their comments have contributed to improving the quality of this manuscript.

Financial support

This study was funded by UNLP (11/N880) and CIC (Res. 597/16).

Conflicts of interest

None.

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