New records of chewing lice (Insecta: Phthiraptera) parasites of Brazilian Anhimidae, Threskiornithidae, and Aramidae (Aves)

Kuabara, Kamila M.D.; Valim, Michel P.; Silveira, Luís Fábio

doi:10.11606/1807-0205/2023.63.020

Abstract

We present records of chewing lice collected from bird skins of the families Anhimidae, Threskiornithidae, and Aramidae deposited at the Museum of Zoology of University of São Paulo (MZUSP). Twenty-one chewing lice species from the suborders Amblycera and Ischnocera were identified, seven of which are new records for Brazil. These species belong to the genera Ardeicola (1), Colpocephalum (3), Ibidoecus (1), and Plegadiphilus (2). Furthermore, ten species were recorded from new localities in Brazil, and Colpocephalum cayennensisPrice & Emerson, 1967 is for the first time recorded with precise locality in the country. Lastly, the bird host subspecies Phimosus infuscatus nudifrons (Spix, 1825) (Threskiornithidae) was for the first time found to harbor lice species.

Keywords
Ibises; Limpkins; Louse; Screamers; Spoonbills

INTRODUCTION

The order Phthiraptera (chewing and sucking lice) consists of approximately 5,000 valid species (Price et al., 2003), that are permanent ectoparasites of mammals and birds (Johnson & Clayton, 2003; Grimaldi & Engel, 2005). Phthiraptera is divided into four suborders: Amblycera, Ischnocera, Rhynchophthirina, and Anoplura, of which only Amblycera and Ischnocera occur on birds (Price et al., 2003). Among the 25 families that constitute the order Phthiraptera, more than 75% of the diversity belongs to the families Menoponidae (suborder Amblycera) and Philopteridae (suborder Ischnocera) with 1,039 and 2,698 described species, respectively (Johnson & Clayton, 2003). Recently efforts have been made to build the Brazilian faunal list. So far, 148 species of Menoponidae and 190 species of Philopteridae have been recorded (Valim & Kuabara, 2022).

This group of ectoparasites is still very poorly studied in Brazil, and many of the expectedly common species have still not been formally recorded. Even though Brazil has one of the richest avifauna in the world, only a tiny fraction of the number of chewing lice that occur in the country have been recorded and/or described. One of the largest surveys of these ectoparasites for Brazil was made by Kuabara & Valim (2017), that recorded 20% of the total fauna for bird lice in the country and reported 34 species new to Brazil (Valim & Kuabara, 2022). Focusing on this disparity, we collected and analyzed samples of chewing lice from museum bird skins of the families Anhimidae (order Anseriformes), Threskiornithidae (order Pelecaniformes), and Aramidae (order Gruiformes). These records increase what is known about avian chewing lice diversity in Brazil as argued by Oniki (2002), that claims that bird collections provide an unique opportunity for collecting ectoparasites from historical specimens.

Much of the knowledge about these parasitic insects in Brazil must be credited to Lindolpho Rocha Guimarães (1908-1998), who was active between the years 1930-1980 and described more than 70 species (Arzua & Valim, 2010). Nevertheless, only a couple publications provided faunal surveys in Brazil; Oniki (1990, 1999) for Amazonas state with twenty louse species from seventeen bird host species, and Mato Grosso state, with sixty-one louse species from thirty-eight bird host species. For Pernambuco state, Roda & Farias (1999) registered fifteen louse species on fifteen bird species; de Lyra-Neves et al. (2000, 2005), collected a total of eighty-nine louse specimens from nine bird hosts, but did not identify the louse to species level. Freitas et al. (2002), recorded amblycerans (Menoponidae and Ricinidae) from three bird hosts. Valim et al. (2004, 2005) recorded three louse species from one mammal host in Rio de Janeiro state, and twenty-eight louse species in twenty-three bird host species in São Paulo state. Lastly Kuabara & Valim (2017) recorded one hundred and nine louse species from sixty-eight bird host species for Espírito Santo, Goiás, Mato Grosso, and Pará states.

MATERIAL AND METHODS

All bird skin specimens from the families Anhimidae (two species), Threskiornithidae (eight species), and Aramidae (one species) occur in Brazil (Pacheco et al., 2021), and were examined for chewing lice (Table 1). Louse specimens were obtained using the method outlined in Mey (2002), which, for large-bodied hosts, consists of ruffling the fingertips among the body and wing feathers of the specimen, dislodging the lice, which then fall on a white surface (e.g., paper sheet), and are collected in 70% ethanol. Louse specimens were then mounted in a permanent slide following Palma’s (1978) protocol.

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Table 1
Host-parasite list for species of chewing lice found on museum bird skins in the families Anhimidae (Anseriformes), Threskiornithidae (Pelecaniformes), and Aramidae (Gruiformes), in Brazil. * New Brazilian locality record; ** First Brazilian record; *** First Brazilian record with precise locality information.

Collecting ectoparasites from museum skins has a high risk of contamination because lice can be transferred from one host to another by placing the host skins in the same museum tray (Mey, 2002). Also, contaminants are found in a low number. Therefore, identified contaminants (two specimens) were discarded and only specimens that were truly attributable to the host or whose presence was to-be-expected were further considered. All examined material (both lice and birds) are deposited in the ectoparasitological and ornithological collections at the Museum of Zoology of the University de São Paulo (MZUSP), respectively.

Louse specimens were morphologically identified using the available literature for each genus or species, and the cited references are listed under a short paragraph about each louse genus. For each species account, the first line provides the name, authorship, and the figure number of the species. The second line describes the world distribution of the species, then the distribution in Brazil, followed by the host(s) species in which the louse species was previously recorded. Subsequently, the specimen list, counting the number and sex of specimens, louse voucher number, host name, host voucher number, locality, collection date, and collector is cited. Lice nomenclature follows Price et al. (2003). Sampling locations were gathered from the original label of each species with coordinates and additional locality information obtained and/or cross-referenced in Paynter & Traylor (1991). Abbreviations of Brazilian State names used herein are as follows: BA, Bahia; GO, Goiás; MA, Maranhão; MS, Mato Grosso do Sul; MT, Mato Grosso; PA, Pará; PR, Paraná; RS, Rio Grande do Sul; SC, Santa Catarina; and SP, São Paulo.

RESULTS

In total, we examined 10 host species and 45 bird skins. Lice were collected from 9 bird species, consisting of 21 bird skins (Table 1). The species that yielded a louse-negative result were Eudocimus ruber (Linnaeus, 1758), and Cercibis oxycerca (Spix, 1825), the latter on account of not having skins at MZUSP. Both of avian hosts are Threskiornithidae.

Order PHTHIRAPTERA Haeckel, 1896 Suborder AMBLYCERA Kellogg, 1896 Family MENOPONIDAE Mjöberg, 1910

Colpocephalum Nitzsch, 1818

Species in this genus are typical ectoparasites of 15 bird orders (Accipitriformes, Cariamiformes, Cathartiformes, Ciconiiformes, Columbiformes, Cuculiformes, Falconiformes, Galliformes, Gruiformes, Passeriformes, Pelecaniformes, Phoenicopteriformes, Piciformes, Psittaciformes, and Strigiformes, sensuPacheco et al., 2021). This large assemblage is a distinct group of species, considered here as Colpocephalum s.l., has 136 valid species (Price et al., 2003; Mey, 2013). For a detailed taxonomic review of the species parasitic on Threskiornithidae see Price & Beer (1965).

Colpocephalum ajajae Ewing, 1930 : 126 ( Fig. 1A )

Figure 1
Habitus in most dorsal view: A = Colpocephalum ajajae male (note a dilatation of pre-ocular region on right side of specimen as result of a teratology); B = Colpocephalum cayennensis male; C = Colpocephalum harpiprioni male; D = Colpocephalum infuscati male; E = Colpocephalum leptopygos female; F = Colpocephalum trispinum male. All photos are in same scale.

Distribution: Argentina, Brazil (present study), Guyana, Panama, USA.

Distribution in Brazil: RS, SP (present study).

Host:Platalea ajaja Linnaeus, 1758 (type host) (Threskiornithidae).

Material examined: 1♂ (#7148) ex Platalea ajaja (#14955), Tabatinguara (25°01′S, 47°57′W), Cananéia, São Paulo, Brazil, 20.IX.1934, C. Camargo col. 1♀1N (#7149-50) ex P. ajaja (#9106), Rio Grande do Sul, Brazil, no further data.

Colpocephalum cayennensis Price & Emerson, 1967 : 875 ( Fig. 1B )

Distribution: Argentina, Brazil, Colombia.

Distribution in Brazil: no further data (Price & Emerson, 1967), GO, PA (present study).

Host:Mesembrinibis cayennensis (Gmelin, 1789) (type host) (Threskiornithidae).

Material examined: 1♂1♀ (#7145-46) ex Mesembrinibis cayennensis (#30659), Rio Aricá, Fazenda Aricá (Expedição ao Alto Tapajós) (17°57′S, 55°56′W), Aruanã, Goiás, Brazil, 26.VI.1944, A.M. Olalla col. 1♀ (#7147) ex M. cayennensis (#58046), Rio Tapajós (03°40′S, 55°30′W), Fordlândia, Pará, Brazil, 10.XI.1964, A.M. Olalla col.

Colpocephalum harpiprioni Price & Beer, 1965 : 118 ( Fig. 1C )

Distribution: Argentina, Brazil (present study).

Distribution in Brazil: MT (present study).

Host:Theristicus caerulescens (Vieillot, 1817) (type host) (Threskiornithidae).

Material examined: 1♂4♀ (#7155-56) ex Theristicus caerulescens (#79231), Fazenda Descalvados (16°42′35″S, 57°44′55″W), Cáceres, Mato Grosso, Brazil, 04.IX.2007, L.F. Silveira col. 2♂ (#7157-58) ex T. caerulescens (#98503), Vila Bela da Santíssima Trindade (14°59′15.4″S, 59°55′10.6″W), Mato Grosso, Brazil, 17.II.2014, L.F. Silveira col.

Colpocephalum infuscati Price & Emerson, 1967 : 877 ( Fig. 1D )

Distribution: Argentina, Brazil, Colombia.

Distribution in Brazil: BA, PA (present study), CE (Price & Emerson, 1967), RS (Valim et al., 2009).

Host:Phimosus infuscatus (Lichtenstein, 1823) (type host) (Threskiornithidae).

Material examined: 1♂ (#7164) ex Phimosus infuscatus nudifrons (#40753), Rio Preto (11°21′S, 43°52′W), Santa Rita de Cássia, Bahia, Brazil, 28.III.1958, E. Dente col. 1♂2♀1N (#7162-63) ex P. i. nudifrons (#97035), Barra das Princesas, Fazenda Fartura (09°47′S, 50°12′W), Santana do Araguaia, Pará, Brazil, 15.VIII.2013, L.F. Silveira col. 1♂, 1N (#7160-61) ex P. i. nudifrons (#83734), Fazenda Fartura (09°42′S, 50°24′W), Santana do Araguaia, Pará, Brazil, 03.IX.2009, L.F. Silveira col.

Colpocephalum leptopygos Nitzsch [in Giebel], 1874 : 273 ( Fig. 1E )

Distribution: Argentina, Brazil, Russia, USA.

Distribution in Brazil: SC (Eichler, 1954), SP (present study).

Hosts:Plegadis chihi (Vieillot, 1817), P. falcinellus (Linnaeus, 1766) (type host), P. ridgwayi (Allen, 1876) (Threskiornithidae).

Material examined: 1♀ (#7159) ex Plegadis chihi (#9792), Rio Pinheiros (23°32′S, 46°44′W), São Paulo, São Paulo, Brazil, III.1906, J. Florencio col.

Colpocephalum trispinum Piaget, 1885 : 122 ( Fig. 1F )

Distribution: Brazil (present study), Chile, Ecuador.

Distribution in Brazil: SC, MS (present study).

Hosts:Theristicus caudatus (Boddaert, 1783) (type host), T. melanopis (Gmelin, 1789) (Threskiornithidae).

Material examined: 4♂1♀ (#7151-52) ex Theristicus caudatus (#18247), Salobra (20°10′S, 56°31′W, 125 amsl), Miranda, Mato Grosso do Sul, Brazil, 21.VII.1939, Exp. [MZUSP] Mato Grosso col. 2♂ (#7153-54) same data, except ex T. caudatus (#18246). 2♂6♀ (#2892-95) ex T. caudatus, Escola de Veterinária, Blumenau, Santa Catarina, Brazil, 2001, J.C. Souza Jr col.

Dicteisia Bedford, 1939

Species of this genus are found exclusively on the screamers (Anhimidae) and currently comprise 5 valid species (Price et al., 2003). For a detailed taxonomic review of the genus see Price (1968).

Dicteisia abdominalis Carriker & Díaz-Ungría, 1961 : 38 ( Fig. 2A )

Figure 2
Habitus in most dorsal view: A = Dicteisia abdominalis male; B = Dicteisia keleri male; C = Dicteisia palamedae male; D = Plegadiphilus mamillatus female; E = Plegadiphilus plegadis male; F = Plegadiphilus riograndensis female. All photos are in same scale.

Distribution: Brazil, Colombia, Ecuador, Paraguay, Venezuela.

Distribution in Brazil: no further data (Price, 1968), “Amazonia” (present study).

Host:Anhima cornuta (Linnaeus, 1766) (type host) (Anhimidae).

Material examined: 3♂1♀1N (#7175-79) ex Anhima cornuta (#73171), Amazonia, V.1967, no further data.

Dicteisia keleri Price, 1968 : 448 ( Fig. 2B )

Distribution: Argentina, Brazil, Paraguay.

Distribution in Brazil: MT (Price, 1968; present study), MS (Price, 1968).

Hosts:Anhima cornuta (Linnaeus, 1766), Chauna torquata (Oken, 1816) (type host) (Anhimidae).

Material examined: 1♂ (#7173) ex Chauna torquata (#98649), Rio Guaporé (15°03′01.18″S, 59°05′32.07″W), Vila Bela da Santísima Trindade, Mato Grosso, Brazil, 26.II.2014, L.F. Silveira col.

Dicteisia palamedea Eichler, 1954 : 43 ( Fig. 2C )

Distribution: Brazil, Colombia, Ecuador, Paraguay, Peru.

Distribution in Brazil: no further data (Price, 1968), “Amazonia” (present study).

Host:Anhima cornuta (Linnaeus, 1766) (type host) (Anhimidae).

Material examined: 11♂5♀3N (#7186-7200) ex Anhima cornuta (#73171), Amazonia, V.1967, no further data. 3♂2♀1N (#7180-85) ex A. cornuta (#24540), Amazonia, 1937, A.M. Olalla col.

Plegadiphilus Bedford, 1939

Species of this genus are found exclusively on ibises (Threskiornithidae) and currently comprise 8 valid species (Price et al., 2003; Valim et al., 2009). For a limited discussion of the genus see Tuff (1965), Emerson & Price (1969), and Ledger (1971).

Plegadiphilus mamillatus ( Piaget, 1885 : 114) ( Fig. 2D )

Distribution: Bolivia, Brazil (present study), Colombia.

Distribution in Brazil: MS (present study).

Host:Theristicus caudatus (Boddaert, 1783) (type host) (Threskiornithidae).

Material examined: 1♀ (#7165) ex Theristicus caudatus (#18247), Salobra (20°10′S, 56°31′W, 125 amsl), Miranda, Mato Grosso do Sul, Brazil, 21.VII.1939, Exp. [MZUSP] Mato Grosso col.

Plegadiphilus plegadis ( Dubinin, 1938 : 178) ( Fig. 2E )

Distribution: Argentina, Brazil (present study), Russia, USA.

Distribution in Brazil: SP (present study).

Hosts:Plegadis chihi (Vieillot, 1817), P. falcinellus (Linnaeus, 1766) (type host) (Threskiornithidae).

Material examined: 2♂1N (#7168-70) ex P. chihi (#9792), Rio Pinheiros (23°32′S, 46°44′W), São Paulo, Brazil, III.1906, J. Florencio col. 1♂1N (#7166-67) ex P. chihi (#9792), Iguape (24°43′S, 47°33′W, msl), São Paulo, Brazil, 20.V.1904, R. Krone col.

Plegadiphilus riograndensis Valim [in **Valim et al.], 2009 : 253 (** Fig. 2F )

Distribution: Brazil.

Distribution in Brazil: RS (Valim et al., 2009), PA (present study).

Host:Phimosus infuscatus (Lichtenstein, 1823) (type host) (Threskiornithidae).

Material examined: 1♀1N (#7171-72) ex Phimosus infuscatus nudifrons (#83734), Fazenda Fartura (09°42′S, 50°24′W), Santana do Araguaia, Pará, Brazil, 03.IX.2009, L.F. Silveira col.

Suborder ISCHNOCERA Kellogg, 1896 Family PHILOPTERIDAE Burmeister, 1838 (sensu lato)

Ardeicola Clay, 1936

This genus has a worldwide distribution, and it is found exclusively on Ciconiiformes. Currently the genus comprises 68 described species (Price et al., 2003). For a limited discussion of the genus and identification of Brazilian species see Pessôa & Guimarães (1935a), Carriker (1960), Hajela (1966), Tuff (1967), and Hajela & Tandan (1968).

Ardeicola meinertzhageni Hajela, 1966 : 551 ( Fig. 3A )

Figure 3
Habitus in most dorsal view: A = Ardeicola meinertzhageni male; B = Ardeicola praegracilis female; C = Ardeicola rhaphidius male; D = Ardeicola theristicus male. All photos are in same scale.

Distribution: Brazil (present study), Paraguay.

Distribution in Brazil: GO, MT, MS (present study).

Host:Theristicus caerulescens (Vieillot, 1817) (type host) (Threskiornithidae).

Material examined: 6♂1♀1N (#7234-37) ex Theristicus caerulescens (#30657), Rio Aricá, Fazenda Aricá (Expedição ao Alto Tapajós) (17°57′S, 55°56′W), Aruanã, Goiás, Brazil, 21.VI.1944, O. Pinto col. 1♂1N (#7238) ex T. caerulescens (#79231), Fazenda Descalvados (16°42′35″S, 57°44′55″W), Cáceres, Mato Grosso, Brazil, 04.IX.2007, L.F. Silveira col. 1♂1N (#7239-40) ex T. caerulescens (#98085), Aquidauana, Mato Grosso do Sul, Brazil, 15.VII.1973, G. Baudet col. 1♂1N (#7241-42) ex T. caerulescens (#98503), Vila Bela da Santíssima Trindade (14°59′15.4″S, 59°55′10.6″W), Mato Grosso, Brazil, 17.II.2014, L.F. Silveira col.

Ardeicola praegracilis Carriker, 1960 : 321 ( Fig. 3B )

Distribution: Argentina, Brazil, Colombia.

Distribution in Brazil: RS (Valim et al., 2009), BA, PA (present study).

Hosts:Phimosus infuscatus (Lichtenstein, 1823), P. i. berlepschi Hellmayr, 1903 (type host) (Threskiornithidae).

Material examined: 1♂1♀2N (#7248-51) ex Phimosus infuscatus nudifrons (#83734), Fazenda Fartura (09°42′S, 50°24′W), Santana do Araguaia, Pará, Brazil, 03.IX.2009, L.F. Silveira col. 1♂1♀ (#7252-53) ex P. i. nudifrons (#40753), Rio Preto (11°21′S, 43°52′W), Santa Rita de Cássia, Bahia, Brazil, 28.III.1958, E. Dente col.

Ardeicola rhaphidius (Nitzsch [in Giebel], 1866 : 384) ( Fig. 3C )

Distribution: Argentina, Brazil, Peru, USA.

Distribution in Brazil: SC (Eichler, 1943; Tuff, 1967), SP (present study).

Hosts:Plegadis chihi (Vieillot, 1817), P. falcinellus (Linnaeus, 1766) (type host) (Threskiornithidae).

Material examined: 1♂ (#7243) ex P. chihi (#9792), Rio Pinheiros (23°32′S, 46°44′W), São Paulo, Brazil, III.1906, J. Florencio col. 1♂ (#7244) ex P. chihi (#2152), Iguape (24°43′S, 47°33′W, msl), São Paulo, Brazil, 20.V.1904, R. Krone col. 1♀2N (#7245-47) ex P. chihi (#1934), same locality, 30.IV.1901, same collector.

Ardeicola theristicus ( Pessôa & Guimarães, 1935a : 311) ( Fig. 3D )

Distribution: Brazil.

Distribution in Brazil: MS (Pessôa & Guimarães, 1935a; present study).

Host:Theristicus caudatus (Boddaert, 1783) (type host) (Threskiornithidae).

Material examined: 5♂5♀9N (#7218-27) ex Theristicus caudatus (#18247), Salobra (20°10′S, 56°31′W, 125 amsl), Miranda, Mato Grosso do Sul, Brazil, 21.VII.1939, Exp. [MZUSP] Mato Grosso col. 4♂2♀7N (#7228-33) same data, except ex T. caudatus (#18246).

Bothriometopus Taschenberg, 1882

Species of this genus are found exclusively on the screamers (Anhimidae) and currently comprise 2 described species (Price et al., 2003). For a detailed morphological and ecological discussion of the genus see Cicchino & Mey (2007).

Bothriometopus macrocnemis ( Burmeister, 1838 : 433) ( Fig. 4A )

Figure 4
Habitus in most dorsal view: A = Bothriometopus macrocnemis female; B = Ibidoecus heterogenitalis male; C = Ibidoecus iberoamericanus female; D = Ibidoecus phimosus female (note a fusion of tergopleurites IV+V on left and V+VI on right side of specimen as result of a teratology); E = Rallicola funebris female. All photos are in same scale.

Distribution: Bolivia, Brazil, Venezuela.

Distribution in Brazil: PR (Cicchino & Mey, 2007), RS (Valim et al., 2009), MS, MT, PA, “Amazonia” (present study).

Hosts:Anhima cornuta (Linnaeus, 1766) (type host), Chauna chavaria (Linnaeus, 1766), C. torquata (Oken, 1816) (Anhimidae).

Material examined: 1♀1N (#7201-02) ex Chauna torquata (#98649), Rio Guaporé (15°31′18″S, 59°5′32.07″W), Vila Bela da Santísima Trindade, Mato Grosso, Brazil, 26.II.2014, L.F. Silveira col. 2N (#7207-08) ex C. torquata (#10104), Corumbá (19°01′S, 57°39′W), Mato Grosso do Sul, Brazil, IX.1917, E. Garbe col. 1♀4N (#7203-06) ex Anhima cornuta (#73171), Amazonia, V.1967, no further data. 6N (#7209-11) ex A. cornuta (#24540), Amazonia, 1937, A.M. Olalla col. 1♂ (#7642) ex A. cornuta (#97226), Fazenda Fartura (09°50′S, 50°29′W), Santana do Araguaia, Pará, Brazil, VIII.2013, M.P. Valim and L.F. Silveira cols.

Ibidoecus Cummings, 1916

This genus is distributed across the world but is found exclusively on the ibises (Threskiornithidae). It currently comprises 23 valid species (Price et al., 2003). For a review about the Neotropical species see Carriker (1947).

Ibidoecus heterogenitalis Carriker, 1947 : 128 ( Fig. 4B )

Distribution: Bolivia, Brazil (present study)

Distribution in Brazil: SC (present study).

Host:Theristicus caudatus (Boddaert, 1783) (type host).

Material examined: 1♂ (#2891) ex Theristicus caudatus, Escola de Veterinária, Blumenau, Santa Catarina, Brazil, 2001, J.C. Souza Jr col.

Ibidoecus iberoamericanus Eichler, 1943 : 5 ( Fig. 4C )

Distribution: Argentina, Brazil, Colombia.

Distribution in Brazil: PA (Eichler, 1943), MG, SP (present study).

Host:Platalea ajaja Linnaeus, 1758 (type host) (Threskiornithidae).

Material examined: 1♀2N (#7212-14) ex Platalea ajaja (#2406), Iguape (24°43′S, 47°33′W, msl), São Paulo, Brazil, 10.VII.1893, R. Krone col. 1N (#72115) ex P. ajaja (#14955), Tabatinguara (25°01′S, 47°57′W), Cananéia, São Paulo, Brazil, 20.IX.1934, C. Camargo col. 1♂1♀1N (#66-67) ex P. ajaja, Tabatinguara (25°01′S, 47°57′W), Cananéia, São Paulo, Brazil, no date, C. Worontzow col. 1♀ (#1501) ex P. ajaja, Pirapora, Minas Gerais, Brazil, 1913, E. Garbe col.

Ibidoecus phimosus Carriker, 1947 : 124 ( Fig. 4D )

Distribution: Argentina, Brazil, Colombia.

Distribution in Brazil: BA (present study), RS (Valim et al., 2009).

Hosts:Phimosus infuscatus (Lichtenstein, 1823), P. i. berlepschi Hellmayr, 1903 (type host) (Threskiornithidae).

Material examined: 1♀1N (#7216-17) ex Phimosus infuscatus nudifrons (#40753), Rio Preto (11°21′S, 43°52′W), Santa Rita de Cássia, Bahia, Brazil, 28.III.1958, E. Dente col.

Rallicola Johnston & Harrison, 1911

Species of this polyphyletic genus (Valim & Weckstein, 2012) occur worldwide and are commonly found on six bird orders (Apterygiformes, Charadriiformes, Cuculiformes, Gruiformes, Passeriformes, and Piciformes, sensuCBRO, 2021). Currently, the genus comprises 96 valid species (Price et al., 2003). For identification of the species parasitic on the limpkin see Pessôa & Guimarães (1935b) and Emerson (1955).

Rallicola funebris (Nitzsch [in Giebel], 1866 : 371) ( Fig. 4E )

Distribution: Argentina, Brazil, Bolivia, Colombia, USA.

Distribution in Brazil: MS (Pessôa & Guimarães, 1935b), SP (present study).

Host:Aramus guarauna (Linnaeus, 1766) (type host) (Aramidae).

Material examined: 4♀ (#6366-67) ex Aramus guarauna (#93041), Itanhaém (24°11′S, 46°47′W, 3 amsl), São Paulo, Brazil, 17.IX.2011, CETAS São Vicente Team col. 2♀ (#6365) ex A. guarauna (#91605), Vila Monteiro Lobato (23°27′25″S, 46°30′06″W), Guarulhos, São Paulo, Brazil, 12.IV.2010, Zoo Guarulhos col.

DISCUSSION

Scientific collections have proved to be a great source for new discoveries and an inexhaustible source for morphological, molecular, and biogeographic data (Funk, 2018; de Vivo et al., 2014). The material deposited at museums represents an endless source of knowledge about biodiversity, so the specimens must be treated as unique and irreplaceable. The revision of scientific material brings not only new data and even new species, but also has a terrific potential to discover new or historical localities (Serrano-Villavicencio & Silveira, 2019).

Mey (2002) attests that studies using bird skins have not been established by museums to later examine the specimens for the occurrence of ectoparasites. Nevertheless, it is worth noting that the material obtained through this method serves as an invaluable and efficient resource, considering the scarcity and challenges associated with acquiring bird specimens. It helps to elucidate our current knowledge about the occurrence and distribution of chewing lice that parasitize birds worldwide. Chewing lice typically exhibit a strong preference for specific hosts, and the significance of bird collections extends beyond ornithology. These collections play a crucial role in exploring the the relationship between hosts and their parasites, as well biogeography, and co-evolution (e.g.,Sweet et al., 2016, Catanach et al., 2019). The technique of shaking out skins (ruffling), remains as an effective way of studying the diversity of these host-specific insects. It is a simple and cheap method, requiring a plastic bag, a curved point needle, and a white surface (e.g., paper sheet) to collect the parasites. However, we cannot dismiss a disadvantage of this method using museum specimens, which is possible feather loss that can damage the specimens and erroneous records due to contamination (Clayton & Drown, 2001; Mey, 2002).

Here we report twenty-one chewing lice species from two separate families, Menoponidae (Amblycera) and Philopteridae (Ischnocera), found on nine bird species: Anhima cornuta, Chauna torquata (Anhimidae), Plegadis chihi, Mesembrinibis cayennensis, Phimosus infuscatus nudifrons, Theristicus caerulescens, T. caudatus, Platalea ajaja (Threskiornithidae), and Aramus guarauna (Aramidae). All species of chewing lice were recorded from their regular hosts (Price et al., 2003), except for the subspecies Phimosus infuscatus nudifrons, which is recorded for the first time harboring four chewing lice species that were previously only recorded on either P. infuscatus ssp. or P. i. berlepschi. Many novel geographical records were made.

Seven species are reported for the first time in Brazil: Colpocephalum ajajae, C. harpiprioni, C. trispinum, Plegadiphilus mamillatus, P. plegadis (Amblycera, Menoponidae), Ibidoecus heterogenitalis, Ardeicola meinertzhageni (Ischnocera, Philopteridae). Another ten species were recorded from new localities in Brazil: Colpocephalum infuscati (Price & Emerson, 1967; Valim et al., 2009), C. leptopygos (Eichler, 1954), Plegadiphilus riograndensis (Valim et al., 2009) (Menoponidae), Ardeicola praegracilis (Valim et al., 2009), A. rhaphidius (Eichler, 1943; Tuff, 1967), Bothriometopus macrocnemis (Cicchino & Mey, 2007; Valim et al., 2009), Ibidoecus iberoamericanus (Eichler, 1943), I. phimosus (Valim et al., 2009), and Rallicola funebris (Pessôa & Guimarães, 1935b). This is also the first time that more precise locality information is given for Colpocephalum cayennensis; previously recorded only as ‘Brazil’ (Price & Emerson, 1967). Herein this species is recorded from Pará and Goiás states.

Faunal inventory studies provide access to a diversity of a determined locality or biome in a certain time and space (Silveira et al., 2010). This study provided new information about chewing lice diversity and abundance in four Brazilian biomes, Amazon, Atlantic Forest, Cerrado, and Pantanal. It also sheds a light on the importance of museum collections, previously pointed out by Oniki (2002) and Mey (2002), as a methodological way to reduce the gap between the bird fauna in Brazil, with almost two thousand bird species recorded (CBRO, 2021), and the 438 bird lice species records in Brazil (Valim & Kuabara, 2022). After the present report, this number will reach exactly 445 species of bird lice recorded so far in Brazil.

ACKNOWLEDGMENTS:

We thanks B. Ehlers (UPS) and Dr. W.L. de Moraes Neto (Fartura Agropecuária) for their support in field and laboratory work. Specimens were collected under Brazilian permit no. 10013-1, following the regulations provided by Brazil’s National Council for the Control of Animal Experimentation (CONCEA).

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FUNDING INFORMATION:
This study was supported by FAPESP - São Paulo Research Foundation, Brazil (MPV: 2011/11420-5 and 2012/06951-4; KMDK: 2013/08685-2; LFS: 2017/23548-2), and CNPq - National Council for Scientific and Technological Development, Brazil (LFS: 302291/2016 and 308337/2019-0).
Published with the financial support of the "Programa de Apoio às Publicações Científicas da Universidade de São Paulo"

Edited by

Edited by:
Carlos José Einicker Lamas

Publication Dates

Publication in this collection
24 July 2023
Date of issue
2023

History

Received
10 Sept 2022
Accepted
28 Apr 2023
Published
05 July 2023

This is an open-access article distributed under the terms of the Creative Commons Attribution License

[1] Arzua, M. & Valim, M.P. 2010. Bases para o estudo qualitativo e quantitativo de ectoparasitos em aves. In: Von Matter, S.; de Queiroz Piacentini, V.; Straube, F.C.; Cândido Jr, J.F. & Accordi, I.A. Ornitologia e conservação: ciência aplicada, técnicas de pesquisa e levantamento. Rio de Janeiro, Editora Technical Books. p. 347-366.

[2] Bedford, G.A.H. 1939. Notes on Menoponidae (Mallophaga) with descriptions of new genera and species. Onderstepoort Journal Veterinary Science and Animal Industry, 12(1): 121-152.

[3] Burmeister, H.C.C. 1838. Mallophaga Nitzsch. In: Burmeister, H.C.C. Handbuch der Entomologie. Berlin, Enslin. p. 418-443.

[4] Carriker Jr., M.A. 1947. Neotropical Mallophaga miscellany. No. 2. The genus Ibidoecus Cummings. Boletín de Entomología Venezolana, 6(2-4): 111-136.

[5] Carriker Jr., M.A. 1960. New species of Ardeicola (Mallophaga) from Colombian hosts. Novedades Colombianas, 1(5): 317-329.

[6] Carriker, M.A. Jr. & Díaz-Ungría, C. 1961. New and little known Mallophaga from Venezuelan birds (Part I). Novedades Cientificas. Serie zoológica: contribuiciones ocasionales del Museo de Historia Natural La Salle, 28: 1-60.

[7] Catanach, T.A.; Johnson, K.P.; Marks, B.D.; Moyle, R.G.; Valim, M.P. & Weckstein, J.D. 2019. Two lineages of kingfisher feather lice exhibit different degrees of cospeciation with their hosts. Parasitology, 146(8): 1-13. https://doi.org/10.1017/S0031182019000453
» https://doi.org/10.1017/S0031182019000453

[8] Cicchino, A.C. & Mey, E. 2007. On morphology, taxonomy, ecology, and distribution of Bothriometopus Taschenberg (Phthiraptera, Ischnocera, Philopteridae sensu lato). Rudolstädter Naturhistorische Schriften, 14: 43-60.

[9] Clay, T. 1936. Two new genera of Mallophaga. Proceedings of the Zoological Society of London, 105(3): 615-618. https://doi.org/10.1111/j.1096-3642.1935.tb01684.x
» https://doi.org/10.1111/j.1096-3642.1935.tb01684.x

[10] Clayton, D.H. & Drown, D.M. 2001. Critical evaluation of five methods for quantifying chewing lice (Insecta: Phthiraptera). Journal of Parasitology, 87(6): 1291-1300. https://doi.org/10.1645/0022-3395(2001)087[1291:CEOFMF]2.0.CO;2
» https://doi.org/10.1645/0022-3395(2001)087[1291:CEOFMF]2.0.CO;2

[11] Comitê Brasileiro de Registros Ornitológicos (CBRO). 2021. Listas das aves do Brasil. Available: Available: http://www.cbro.org.br Access: 02/07/2022.
» http://www.cbro.org.br

[12] Cummings, B.F. 1916. Studies on the Anoplura and Mallophaga, being a report upon a collection from the mammals and birds in the Society’s Gardens - Part II. Proceedings of the Zoological Society of London , 1915: 643-693.

[13] Dubinin, W.B. 1938. Ismenenija parasitofauny karavajki (Plegadis falcinellus) vysyvajemyje vosrostom i migracjej chosiaina. Trudy Astrachanskogo Gosudarstvennogo Zapovednika, 2: 114-212. [in Russian]

[14] Eichler, W. 1943. Notulae Mallophagologicae VI. Über acht meist neue Federlingsarten aus Südamerika. Memórias e Estudos do Museu Zoologico da Universidade de Coimbra, 140: 1-7.

[15] Eichler, W. 1954. Peruanische Mallophagen. In: Titischack, E. Beiträge zur Fauna Perus, nach der ausbeute der hamburg sudperu-expedition. Jena, G. Fisher. v. 4, p. 28-62.

[16] Emerson, K.C. 1955. A review of the genus Rallicola (Philopteridae, Mallophaga) found on Aramidae, Psophiidae and Rallidae. Annals of the Entomological Society of America, 48(4): 284-299. https://doi.org/10.1093/aesa/48.4.284
» https://doi.org/10.1093/aesa/48.4.284

[17] Emerson, K.C. & Price, R.D. 1969. A new species of Plegadiphilus (Mallophaga: Menoponidae) from the Cayenne Ibis. The Florida Entomologist, 52(3): 161-163. https://doi.org/10.2307/3493851
» https://doi.org/10.2307/3493851

[18] Ewing, H.E. 1930. Two new generic names and three new species of Mallophaga. Proceedings of the Biological Society of Washington, 43: 125-128.

[19] Freitas, M.F.L.; Botelho, M.C.N.; Leite, A.S.; Magalhães, V.S.; Sobrinho, A.E.; Oliveira, R.A.; Oliveira, M.H.C.C. & Oliveira, J.B. 2002. Ectoparasitos de aves silvestres mantidas em cativeiro no estado de Pernambuco, Brasil. Entomologia y Vectores, 9(1): 25-33.

[20] Funk, V.A. 2018. Collections-based science in the 21^st Century. Journal of Systematics and Evolution, 56(3): 175-193. https://doi.org/10.1111/jse.12315
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Host Order	Host Family	Host Species	Host common name (in English/Portuguese)	Number of host skins examined	Number of host skins with lice	Louse species	Number of lice collected
Host Order	Host Family	Host Species	Host common name (in English/Portuguese)	Number of host skins examined	Number of host skins with lice	Louse species	Males	Females	Nymphs
Anseriformes	Anhimidae	Anhima cornuta (Linnaeus, 1766)	Horned Screamer/Anhuma	2	2	Dicteisia abdominalis (Menoponidae)	3	1	1
						Dicteisia palamedea (Menoponidae)	11	5	3
						Bothriometopus macrocnemis (Philopteridae)	1	1	10
		Chauna torquata (Oken, 1816)	Southern Screamer/Tachã	3	2	Dicteisia keleri (Menoponidae)	1	0	0
		Chauna torquata (Oken, 1816)	Southern Screamer/Tachã	3	2	Bothriometopus macrocnemis* (Philopteridae)	0	1	3
Pelecaniformes	Threskiornithidae	Cercibis oxycerca (Spix, 1825)	Sharp-tailed Ibis/Trombeteiro	0	0	-	-	-	-
		Eudocimus ruber (Linnaeus, 1758)	Scarlet Ibis/Guará	6	0	-	-	-	-
		Mesembrinibis cayennensis (Gmelin, 1789)	Green Ibis/Coró-coró	3	2	Colpocephalum cayennensis*** (Menoponidae)	1	2	0
		Phimosus infuscatus nudifrons (Spix, 1825)	Whispering Ibis/Tapicuru	4	4	Colpocephalum infuscati* (Menoponidae)	3	2	1
						Plegadiphilus riograndensis* (Menoponidae)	0	1	1
						Ardeicola praegracilis* (Philopteridae)	2	2	2
						Ibidoecus phimosus* (Philopteridae)	0	1	1
		Platalea ajaja Linnaeus, 1758	Roseate Spoonbill/Colhereiro	6	1	Colpocephalum ajajae** (Menoponidae)	1	1	1
		Platalea ajaja Linnaeus, 1758	Roseate Spoonbill/Colhereiro			Ibidoecus iberoamericanus* (Philopteridae)	1	3	4
		Plegadis chihi (Vieillot, 1817)	White-faced Ibis/Caraúna	5	3	Colpocephalum leptopygos* (Menoponidae)	0	1	0
						Plegadiphilus plegadis** (Menoponidae)	3	0	2
						Ardeicola rhaphidius* (Philopteridae)	2	1	2
		Theristicus caerulescens (Vieillot, 1817)	Plumbeous Ibis/Curicaca-real	5	3	Colpocephalum harpiprioni** (Menoponidae)	3	4	0
		Theristicus caerulescens (Vieillot, 1817)	Plumbeous Ibis/Curicaca-real			Ardeicola meinertzhageni** (Philopteridae)	9	1	4
		Theristicus caudatus (Boddaert, 1783)	Buff-necked Ibis/Curicaca	7	2	Colpocephalum trispinum** (Menoponidae)	8	7	0
						Plegadiphilus mamillatus** (Menoponidae)	0	1	0
						Ardeicola theristicus (Philopteridae)	9	7	16
						Ibidoecus heterogenitalis** (Philopteridae)	1	0	0
Gruiformes	Aramidae	Aramus guarauna (Linnaeus, 1766)	Limpkin/Carão	4	2	Rallicola funebris* (Philopteridae)	0	6	0

New records of chewing lice (Insecta: Phthiraptera) parasites of Brazilian Anhimidae, Threskiornithidae, and Aramidae (Aves)

Abstract

INTRODUCTION

MATERIAL AND METHODS

RESULTS

Order PHTHIRAPTERA Haeckel, 1896 Suborder AMBLYCERA Kellogg, 1896 Family MENOPONIDAE Mjöberg, 1910

Colpocephalum Nitzsch, 1818

Colpocephalum ajajae Ewing, 1930 : 126 ( Fig. 1A )

Colpocephalum cayennensis Price & Emerson, 1967 : 875 ( Fig. 1B )

Colpocephalum harpiprioni Price & Beer, 1965 : 118 ( Fig. 1C )

Colpocephalum infuscati Price & Emerson, 1967 : 877 ( Fig. 1D )

Colpocephalum leptopygos Nitzsch [in Giebel], 1874 : 273 ( Fig. 1E )

Colpocephalum trispinum Piaget, 1885 : 122 ( Fig. 1F )

Dicteisia Bedford, 1939

Dicteisia abdominalis Carriker & Díaz-Ungría, 1961 : 38 ( Fig. 2A )

Dicteisia keleri Price, 1968 : 448 ( Fig. 2B )

Dicteisia palamedea Eichler, 1954 : 43 ( Fig. 2C )

Plegadiphilus Bedford, 1939

Plegadiphilus mamillatus ( Piaget, 1885 : 114) ( Fig. 2D )

Plegadiphilus plegadis ( Dubinin, 1938 : 178) ( Fig. 2E )

Plegadiphilus riograndensis Valim [in Valim et al.], 2009 : 253 ( Fig. 2F )

Suborder ISCHNOCERA Kellogg, 1896 Family PHILOPTERIDAE Burmeister, 1838 (sensu lato)

Ardeicola Clay, 1936

Ardeicola meinertzhageni Hajela, 1966 : 551 ( Fig. 3A )

Ardeicola praegracilis Carriker, 1960 : 321 ( Fig. 3B )

Ardeicola rhaphidius (Nitzsch [in Giebel], 1866 : 384) ( Fig. 3C )

Ardeicola theristicus ( Pessôa & Guimarães, 1935a : 311) ( Fig. 3D )

Bothriometopus Taschenberg, 1882

Bothriometopus macrocnemis ( Burmeister, 1838 : 433) ( Fig. 4A )

Ibidoecus Cummings, 1916

Ibidoecus heterogenitalis Carriker, 1947 : 128 ( Fig. 4B )

Ibidoecus iberoamericanus Eichler, 1943 : 5 ( Fig. 4C )

Ibidoecus phimosus Carriker, 1947 : 124 ( Fig. 4D )

Rallicola Johnston & Harrison, 1911

Rallicola funebris (Nitzsch [in Giebel], 1866 : 371) ( Fig. 4E )

DISCUSSION

ACKNOWLEDGMENTS:

REFERENCES

Edited by

Publication Dates

History

Plegadiphilus riograndensis Valim [in **Valim et al.], 2009 : 253 (** Fig. 2F )