Feather mites (Acariformes: Analgoidea) associated with the hairy woodpecker Leuconotopicus villosus (Piciformes: Picidae) in Panama

A BSTRACT — Two new feather mite species of the superfamily Analgoidea are described from the hairy woodpecker Leuconotopicus villosus (Linnaeus, 1766) (Piciformes: Picidae) in Panama: Pterotrogus panamensis n. sp. (Pteronyssidae) and Trouessartia hernandesi n. sp. (Trouessartiidae). Pterotrogus panamensis belongs to the simplex species group and most clearly differs from the other species of this group in having the pregenital sclerite paired in males, and the hysteronotal shields strongly narrowed posteriorly in females. Trouessartia hernandesi is close to T. picumni Hernandes, 2014, the only previously known species of this genus from woodpeckers, and differs from the latter by having the following features: in both sexes, setae d1 and d2 are present and genual setae cG I, cG II and mG I are spiculiform; in males, epimerites IVa are long, bow-shaped and extend to the base of the genital apparatus; in females, the external copulatory tube is long and spiculiform.


INTRODUCTION
Feather mites are a vast group of astigmatan mites (Acari: Astigmata) that are highly specialized ectoparasites and commensals permanently living on birds.These mites currently include over 2500 species arranged, according to the most widely accepted concept, in two superfamilies, Analgoidea and Pterolichoidea.Feather mites are known from all presently recognized orders of birds; most live in various microhabitats of the plumage of their hosts, although representatives of some families live on the skin and even in the nasal cavities (Gaud and Atyeo 1996;Dabert and Mironov 1999;Proctor 2003;OConnor 2009).
In the present paper, which we intend to be the first of a series of papers on feather mites of Panama, we describe two new species from the hairy woodpecker Leuconotopicus villosus (Linnaeus) (Piciformes: Picidae).

MATERIALS AND METHODS
The material used in the present work was collected during our parasitological survey in Las Nubes station in the south-eastern part of La Amistad International Park (Chiriquí Province, Panama) in April of 2016.This field site has an elevation of 2500 -2800 m and is predominantly covered with a cloud forest.Birds were captured with mist-nets, identified, and checked for the presence of ectosymbionts.Feather mites were taken from live birds under stereomicroscope with a preparation needle or fine forceps and placed in tubes with 96% ethanol.After processing, captured birds were released back to the wild.In the laboratory, feather mites were mounted on slides in Hoyer's medium according to the standard technique for small acariform mites (Krantz and Walter 2009).Investigation of mite specimens and drawings were made using a Leica DM 2500 light microscope equipped with differential interference contrast (DIC) and a camera lucida.
The descriptions of new species and techniques for measuring morphological structures follows the modern formats elaborated for corresponding taxonomic groups of mites (Mironov 2005;Mironov and Wauthy 2005;Hernandes 2012Hernandes , 2014;;Mironov and González-Acuña 2013).General morphological terms and leg and idiosomal chaetotaxy follow Gaud and Atyeo (1996); idiosomal chaetotaxy also follows these authors with minor corrections for coxal setation by Norton (1998).All measurements are in micrometers (µm).
The taxonomic system and scientific names of birds follow Gill and Donsker (2017).Abbreviations used in collection numbers and type material depositories are as follows: BMOC and UMMZ -Museum of Zoology of the University of Michigan, Ann Arbor, USA; ZISP -Zoological Institute of the Russian Academy of Sciences, Saint-Petersburg, Russia.
The feather mite genus Pterotrogus Gaud (in: Faccini and Atyeo 1981) was originally established for the species Pterotrogus simplex (Haller, 1882) from Melanerpes erythrocephalus (Linnaeus) (Piciformes, Picidae).This genus is one of 12 pteronyssid genera restricted in their host associations to birds of the order Piciformes (Mironov 2003).To date, the genus Pterotrogus has included 17 species; all of them are associated with woodpeckers of the New World (Mironov 2005;Mironov et al. 2005;Hernandes 2012).Phylogenetic analysis of relationships within this genus, based on morphological characters, and a key to species were provided by Mironov (2005).All presently known species are arranged in four species groups: iron, lanceolatus, sinusoidus, and simplex.Representatives of this genus inhabit the ventral side of vanes of wing feathers (primaries, secondaries and tertiaries), where they are located in corridors.
Epimerites I, II with narrow sclerotized areas.Inner ends of epimerites IIIa shaped as an oblique L. Setae 3a and 4b approximately at the same transverse level.Genital arch 15 (15 -16) long, 10 (10 -11) wide, aedeagus about one third the length of arch.Epiandrum present, minute.Pregenital sclerites present, represented by a pair of small longitudinal sclerites.Coxal setae 4a approximately at level of genital arch apex.Genital shield and adanal shields absent.Diameter of anal discs 13 (11 -13).
Epimerites I, II as in the male.Epimerites III, IV with small triangular sclerotized areas.Epigynum shaped as long arch, with tips extending beyond level of setae g, without lateral extensions, 60 -65 long, 70 -78 wide; sclerotized folds of oviporus ex-FIGURE 3: Pterotrogus panamensis n. sp., details: A-E -male, F, G -female.A, B -leg I and II of male, respectively, C -genu, tibia and tarsus III of male, D -tibia and tarsus IV of male, E -male opisthosoma, dorsal view, F, G -tibia and tarsus III and IV of female.Abbreviations: vm -ventral membrane of tarsus I.
Differential diagnosis -The new species, Pterotrogus panamensis n. sp., belongs to the simplex species group (Mironov 2005) in having, in both sexes, simple filiform setae on the posterior margin of the body (f2, h2, h3, ps1, and ps2) and by the absence of dorsal crests on segments of legs I, II.Among seven previously known species of this group (Mironov 2005;Hernandes 2012), the new species is most similar to P. colapti Mironov, 2005 from Colaptes punctigula guttatus (von Spix) (Piciformes: Picidae) in having setae c3 lanceolate and setae e1 situated between levels of setae d2 and e2 in both sexes, and rounded incisions around bases of setae se in males.Pterotrogus panamensis n. sp.differs from this species by the following features: in males, a pair of small pregenital sclerites are present anterior to the genital arch, bases of setae h2 and h3 are slightly flattened and enlarged; in females, the posterior end of the hysteronotal shield is strongly narrowed (about 1/3 the width of the main body of the shield) and heavily sclerotized.In males of P. colapti and other species of the simplex group, the pregenital sclerites are absent or represented by a single median band (P.veniliornis Mironov, 2005), setae h2 and h3 are simple whip-like; in females, the posterior end of the hysteronotal shield is widely rounded and without strong sclerotization.
Etymology -The specific epithet is derived from the country name where this species was found.
The genus Trouessartia is distributed worldwide.Its representatives are predominately associated with passerines and have been recorded from members of 28 families as classified by Gill and Donsker (2017).Among the species living on passerines, almost all are associated with oscines, and only five species have so far been recorded from suboscines of the families Tyrannidae and Rhinocryptidae in South America.Three single records of Trouessaria species on non-passerines hosts of the orders Charadriiformes, Coraciiformes, and Psittaciformes were considered as the result of accidental contaminations, since they have never been recollected from the same hosts (Orwig 1968;Santana 1976;Gaud and Atyeo 1996).The only species reliably known from non-passerine hosts is recently described Trouessartia picumni Hernandes, 2014 from the tawny piculet Picumnus fulvescens (Stager) (Piciformes: Picidae) in Brazil (Hernandes 2014).Within the plumage of their hosts, mites of the genus Trouessartia are mainly located on the wing feathers (secondaries, tertiaries, and greater upper coverts) and the rectrices (Mironov and González-Acuña 2013).
A new Trouessartia species described below is the first record of this genus in Panama.
Differential diagnosis -The new species, Trouessartia hernandesi n. sp., is close to T. picumni Hernandes, 2014 from Picumnus fulvescens (Stager) (Piciformes, Picidae).These two species constitute a distinct species group, which we refer here the picumni group, characterized by the following common features: in both sexes, the prodorsal shield is fused with anterior ends of scapular shields, and the hysteronotal shield is fused with anterior ends of the humeral shields, trochanteral setae sRIII are long filiform; in females, setae ps1 are situated closer to setae h2 than to h3.Trouessartia hernandesi differs from T. picumni by the following features: in both sexes, setae d1 and d2 are present, the lateral margins of the hysteronotal shield lack any incisions, genual setae cGI, cGII and mGI are spiculiform; in males, epimerites IVa are long, bow-shaped and extend to the base of the genital apparatus; in females, the external copulatory tube is long spiculiform.In both sexes of T. picumni, setae d1 and d2 are absent, the lateral margins of the hysteronotal shields have a notch-like incision at level of trochanters III, setae cGI, cGII and mGI are filiform; in males, epimerites IVa are short and barely extend to the level of setae g; in females, the external copulatory tube is absent, the copulatory opening is in the anterior end of the terminal cleft.
Etymology -The species is named after Dr. Fabio A. Hernandes (Universidade Estadual Paulista, Rio Claro, São Paulo, Brazil), a prominent Brazilian expert on feather mites.

DISCUSSION
The hairy woodpecker, Leuconotopicus villosus (Linnaeus), has a very broad distribution throughout North and Central America (del Hoyo et al. 2002).The most southern part of its range extends to western Panama, where this bird is represented by a subspecies L. v. extimus (Bangs) (Gill and Donsker 2017).The feather mite fauna of the hairy woodpecker has been previously explored in Canada (Mironov & Galloway 2006;Galloway et al. 2014), with four species reported: Neopteronyssus pici (Scopoli, 1763), Pteronyssus brevipes (Berlese, 1884), P. picoides Černý & Schumilo, 1973 (Pteronyssidae), and Picalgoides picimajoris (Buchholz, 1869) (Psoroptoididae).All these mite species are rather common on woodpeckers of the genera Dendrocopos Koch, Leuconotopicus Malherbe and Picoides Lacépède in northern Eurasia and North America (Mironov 1989(Mironov , 2003(Mironov , 2004;;Mironov and Galloway 2006).Although several individuals of L. villosus were examined in Canada over the course of that study, none of the new mite species described herein was found.Similarly, none of the four species occurring on L. villosus in Canada have been found in Panama.
The most reasonable explanation of this discordance in the feather mite faunas is that the mites associated with the hairy woodpecker in Panama, Pterotrogus panamensis and Trouessartia hernandesi, might be of a secondary origin on this host.In other words, the ancestors of these mite species may have been transferred from unrelated and presently unknown host species.The mite genus Pterotrogus is widely distributed on New World woodpeckers, particularly the species-rich genera Campephilus Gray, Colaptes Vigors and Veniliornis Bonaparte in Central and South America.A few species of Pterotrogus species are also known from single host species from the genera Dryocopus Boie, Leuconotopicus, and Melanerpes Swainson in North America (Mironov 2005;Mironov et al. 2005;Hernandes 2012).We suggest that the ancestor of P. panamensis has shifted from a woodpecker species of the gen-era Colaptes or Veniliornis harboring species of the simplex group (Mironov 2005).
The genus Trouessartia, currently including over 110 species and the richest genus within the family, is associated almost exclusively with passerines (Santana 1976;Mironov and González-Acuña 2013;Hernandes andValim 2015, Mironov andPalma 2016).Trouessartia picumni Hernandes, 2014, described from piculets of the genus Picumnus Temminck (Picidae: Picumninae) in Brazil, is the only species previously known to be associated with piciform hosts (Hernandes 2014).Since T. hernandesi and T. picumni are closely related species, but associated with woodpeckers from very distant phylogenetic lineages (different subfamilies), we suggest that the ancestors of both mite species have been transferred from probably related passerine hosts.