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

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.


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 , 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 (1990Oniki ( , 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. (2004Valim et al. ( , 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.
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.

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

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).
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.

Figure 1 .
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.