Host-Parasite Relationships of Quill Mites (Syringophilidae) and Parrots (Psittaciformes)

Marciniak-Musial, Natalia; Skoracki, Maciej; Kosicki, Jakub Z.; Unsöld, Markus; Sikora, Bozena

doi:10.3390/d15010001

Open AccessArticle

Host-Parasite Relationships of Quill Mites (Syringophilidae) and Parrots (Psittaciformes)

¹

Department of Animal Morphology, Faculty of Biology, Adam Mickiewicz University in Poznan, Uniwersytetu Poznanskiego 6, 61-614 Poznan, Poland

²

Department of Avian Biology and Ecology, Faculty of Biology, Adam Mickiewicz University in Poznan, Uniwersytetu Poznanskiego 6, 61-614 Poznan, Poland

³

Zoologische Staatssammlung München, Sektion Ornithologie, Münchhausenstr. 21, 81247 Munich, Germany

^*

Authors to whom correspondence should be addressed.

Diversity 2023, 15(1), 1; https://doi.org/10.3390/d15010001

Submission received: 31 October 2022 / Revised: 15 December 2022 / Accepted: 15 December 2022 / Published: 20 December 2022

(This article belongs to the Special Issue Geographic Distribution and Diversity of Animal Parasitic Mites)

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Abstract

:

The family Syringophilidae (Acari: Prostigmata) includes obligatory ectoparasites, which occupy feather quills from various parts of avian plumage, where they feed and reproduce. Our study was concerned with the global fauna of syringophilid mites associated with Psittaciformes, as well as host-parasite specificity and evolution. We assumed that the system composed of quill mites and parrots represents a model group that can be used in a broader study of the relationships between parasites and hosts. In total, we examined 1524 host individuals of parrots belonging to 195 species, 73 genera, and 4 families (which constitute ca. 50% of global parrot fauna) from all zoogeographical regions where Psittaciformes occur. Among them, 89 individuals representing 81 species have been infested by quill mites belonging to 45 species and 8 genera. The prevalence of host infestations by syringophilid mites varied from 2.8% to 100% (95% confidence interval (CI Sterne method) = 0.1–100). We applied a bipartite analysis to determine the parasite-host interaction, network indices, and host specificity at the species and whole network levels. The Syringophilidae-Psittaciformes network was composed of 24 mite species and 47 host species. The bipartite network was characterized by a high network level specialization H2′ = 0.98, connectance C = 0.89, and high modularity Q = 0.90, with 23 modules, but low nestedness N = 0.0333. Moreover, we reconstructed the phylogeny of the quill mites on the generic level, and this analysis shows two distinct clades: Psittaciphilus (Peristerophila + Terratosyringophilus) (among Syringophilinae subfamily) and Lawrencipicobia (Pipicobia + Rafapicobia) (among Picobiinae). Finally, the distributions and host-parasite relationships in the system composed of syringophilid mites and parrots are discussed.

Keywords:

Acari; biodiversity; parrots; Psittaciformes; quill mites; Syringophilidae

1. Introduction

The study of parasitic organisms and their relationships to their hosts has, through the decades, enjoyed contributions from those who have studied parasites and parasitism from morphological, ecological, phylogenetical, physiological, and other standpoints [1]. Studying parasites in their own right is relatively simple, but the analyses of the interrelations between the parasite and its host requires a broad spectrum of biological disciplines [2]. As it increasingly happens in more sections of biological sciences, parasitologists are examining parasites and parasitism at all levels of organization, ranging from population and macro-ecological, to the micro-ecological levels [2].

The concept of the host-parasite relationship is an essential tenet in the study of parasitism because it provides the basis for understanding the manner in which the partners are tied to each other, both evolutionarily and ecologically [3,4]. As parasite-host relationships may constitute up to 75% of all species interactions in food webs [5], they are important at every level, up to entire ecosystems [6]. For this reason, precise indicators (including nestedness, specificity at the host and species level, connectance, and modularity) enhance the interpretation of the related communities [7,8].

Quill mites of the family Syringophilidae (Acariformes: Prostigmata: Cheyletoidea) are permanent and obligatory avian ectoparasites [9]. Syringophilid mites live, feed on, reproduce, and occupy various types of feathers of the avian plumage [9,10]. Their long and styletiform mobile digits of the chelicerae facilitate piercing the fibrous wall of the calamus and penetrating the interiors of quill feathers [10,11,12]. They are related to many orders of birds throughout the world. Based on their potential host species richness, Johnston and Kethley [13] noticed that all quill mite species permanently associated with birds could reach about 5000 species. Moreover, the distribution of quill mites includes all zoogeographical regions, which is correlated with their host distribution. Syringophilid mites are highly host-specific, and most known syringophilid species are mono- or oligoxenous parasites. To date, more than 400 species and 63 genera of quill mites have been described from about 670 bird species belonging to 27 orders of birds [14].

Although most of the work on the family deals with the morphology and systematics of these mites, recent studies focused on the non-taxonomical aspects, e.g., on anatomy [15,16,17,18], sexual selection [19], phylogeny [20,21,22], ecology [14,23,24,25,26,27]; and host-parasite relationships [22,28,29,30]. There are also an increasing number of papers with studies on trophic relationships in the host-parasite systems based on bipartite networks and some indices (e.g., nestedness, modularity, connectance). For quill mites, that research was conducted with the following host groups: passerines (Estrildidae [31], Nectariniidae [29]), cuckoos [28], and columbids [30,32]. The analysis of bipartite networks provides valuable information about the relationships between parasites and their hosts. In addition, they give a better understanding of their structure and impact on each other. Due to the syringophilid host- and habitat-specificity, they are a good model for the study of the ecological and evolutionary host-parasite relationships.

Parrots (Psittaciformes) are large and diverse bird order. This avian clade comprises about 390 living species belonging to four families: Strigopidae, Cacatuidae, Psittaculidae, and Psittacidae [33], which constitute three main lineages: Strigopoidea (New Zealand parrot), Psittacoidea (also called ‘true parrots’) and Cacatuoidea (cockatoos) [34]. The distribution of Psittaciformes is mainly related to the Southern Hemisphere, with ranges in Australasian, Oceanian, Oriental, Neotropical, and Afrotropical zoogeographical regions. They originated in Gondwana, with the Australasian region as the center of their radiation and distribution [35,36,37]. The most recent data indicate their closest affinity with passerines (Passeriformes), followed by falcons (Falconiformes). All three orders now form a single clade of Australaves [38,39] (belonging to the so-called Telluraves—core land birds [40]). The affinity between parrots and passerines is also confirmed by other studies on the evolution of modern Neoaves, which use different dating methods [38,41]. Parrots have the greatest diversity in South America and Australia. The superfamily Strigopoidea diverged from the other parrots around 82 mya when New Zealand broke off from Gondwana. In the Eocene, about 59 mya, Psittacoidea and Cacatoidea had a common ancestor. Finally, they diverged from each other at about 40.7 mya when Australia split off from western Antarctica and South America [42]. The families Psittaculidae and Psittacidae have been constituted into the superfamily clade of Psittacoidea [34,37]. Based on their complicated evolution history and poorly known relationship with mite parasites, parrots are a very interesting subject of examination regarding the infestation of quill mites.

In the present paper, we (1) summarized all taxonomic and locality records to create a worldwide distribution of quill mites associated with birds of the order Psittaciformes; (2) constructed a key to all species and genera of syringophilid mites parasitizing parrots; (3) described interactions and measured the specificity of quill mites and parrots at a global scale; (4) reconstructed the phylogeny of mites associated with parrots on a generic level, and finally (5) discussed the relationships between quill mite species and psittaciform birds.

2. Materials and Methods

2.1. Mite Material

In this study, we re-examined all syringophilid species described from birds of the order Psittaciformes. Mite material was examined mainly based on the syringophilid collection deposited in the Adam Mickiewicz University in Poznan, Department of Animal Morphology, Poznan, Poland. Other mite species were loaned from the collections deposited in different museums and institutions, i.e., Royal Museum for Central Africa, Tervuren, Belgium; Zoological Institute, Russian Academy of Science, St. Petersburg, Russia; Field Museum of Natural History, Chicago, IL, USA; National Autonomous University of Mexico (Universidad Nacional Autonoma de Mexico), Mexico City, Mexico.

2.2. Morphological Characters

The general morphological terminology for quill mites follows Skoracki [12] and Skoracki et al. [43]. The idiosomal setation follows Grandjean [44], as adapted for Prostigmata by Kethley [45]. The nomenclature of leg chaetotaxy follows that proposed by Grandjean [46]. All measurements are given in micrometers.

2.3. Prevalence

To describe the prevalence, we examined the bird collection (dry bird skins) housed in the Bavarian State Collection of Zoology, Munich, Germany, according to the methodology presented in Skoracki [12]. This bird collection was previously used as a donor of many mite species described and recorded in previous papers (e.g, Skoracki [12,47]; Skoracki et al. [43,48]; Skoracki & Hromada [49]; Marciniak et al. [50,51], Marciniak-Musial et al. [52]; Marciniak-Musiał & Sikora [53]). Descriptive statistics were computed using Quantitative Parasitology on the Web [54], with 95% confidence intervals (Sterne method).

2.4. Host Specificity

Terminology for the host specificity for particular mite species follows Caira et al. [55] and Skoracki et al. [43]. The division is based on host range and termed as: monoxenous species (parasite restricted to one host species), oligoxenous (more than one host, but restricted to one genus), mesostenoxenous (more than one genus of hosts, but restricted to one family), metastenoxenous (more than one family of hosts but restricted to one order), and polyxenous species (more than one order).

2.5. Host Scientific Names and Zoogeographical Regions

The common and scientific names of the birds follow Clements et al. [33]. Zoogeographic regions follow Holt et al. [56].

2.6. Bipartite Networks and Statistics

One way to represent the parasite-host interactions between quill mites and avian hosts is through the use of a ‘bipartite’ network. The ‘bipartite’ graph consists of rectangles representing compartment species, and the width is proportional to the sum of interactions involving that species. The number of interactions is shown by lines linking the species with different widths. To analyze patterns in the studied host-parasite-network, we used the ‘bipartite’ package available for R software [57]. The web was visualized by plot-web function. The number of quill mite species infesting each bird species was used as quantitative indices.

During our study, we prepared matrices where quill mite species are in the rows (parasites) and the bird species are (host) in the columns. Next, we calculated the following bipartite index: network specialization (H2′), nestedness (N), connectance (C), modularity (Q), and species specialization metrics (d′). Index of specialization at the species level (d′) measures interaction at the species level and refers to each quill mite species associated with parrots in the network [58]. Index of network specialization H2′ means the deviation of a species’ realized number of interactions and that expected from each species’ total number of interactions [59], with values ranging from 0 (implying low specialization) to 1 (suggesting high specialization). Nestedness describes how many interactions realized by specialists are a subset of those realized by generalists. The nestedness unit is the nestedness temperature T (0–100°). However, in this study, we used a binary system where metrics define as N = (100 − T)/100. It measures the departure from a perfectly nested interaction matrix [60]. In the range 0–1, value 1 implies maximum nestedness [61,62,63]. Connectance is understood as the proportion of possible links observed in the network, ranging from 0 to 1, where 0 suggests low connectance while approaching 1 means high connectance in the network [64]. Modularity is calculated as ‘likelihood’ implemented in computeModules in the bipartite library for R and has the same value meaning as Q (or M), given by Newman [65], Guimerà & Amaral [66], and is currently not supported by a library of QuanBiMo (Q) [67]. We evaluated 100 Q values (observed likelihood) [68] and compared them with 100 Q values coming from permutations for null models (null likelihood). Next, we also calculated the null.t.test (p < 0.05) to test a significant difference between the Q observed and Qnull values.

2.7. Mite Phylogeny

During the cladistic analysis, we examined relationships at the generic level, and OTUs (all operational units) were represented by taxonomic species, i.e., species related to parrots. Therefore, the character traits that appear as autapomorphies represent true synapomorphies for the genera. A total of nine OTUs representing all genera associated with psittaciform birds were included in our data matrix. Two species, i.e., a free living predator Cheyletus eruditus (Schrank, 1781) and quill-inhabiting predator Cheletopsis norneri (Poppe, 1888), both belonging to the sister family Cheyletidae, were used as the outgroups. In total, 56 unordered morphological characters were included in our data matrix (data matrix and morphological characters are supplemented (Figures S1 and S2). The data matrix was prepared in the NEXUS Data Editor 0.5.0 [69]. All characters were treated as unordered, and their states were polarized using outgroup comparison. The plesiomorphic state of each character was designated as ‘0′, apomorphic as ‘1′, and inapplicable as ‘-’. Reconstruction of phylogenetic relationships was performed with PAUP 4.0 [70]. The heuristic search option was used for maximum parsimony analysis. The delayed transformation option, which favors parallelism over reversal, was applied for a posteriori optimization of character states and tracing character changes in lineages.

2.8. Visualization of Host Phylogeny

A tree of the parrot species was constructed based on data and a consensus avian phylogenetic tool available from http://birdtree.org/ (accessed on 21 June 2022) [71], using the “Hackett All Species tree” with 1000 randomly generated trees. The most credible tree was then determined using the tool TreeAnnotator v1.8.2 in the software BEAST v1.8.2 Z [72]. The consensus tree was then graphically adjusted in FigTree v1.4.2 2 [73] (Andrew Rambaut, University of Edinburgh, UK; http://tree.bio.ed.ac.uk/software/figtree/ (accessed on 21 June 2022).

3. Results

3.1. The Species Richness of Syringophilid Mites Associated with Parrots

3.1.1. Subfamily Syringophilinae Lavoipierre, 1953

Mites of this subfamily occupy the quills of flight feathers, i.e., primaries, secondaries, rectrices, and wing and tail coverts. Mites of this subfamily differ from the Picobiinae ones by the presence of the rounded tibiotarsus of palps and fan-like proral setae of tarsuses I–IV.

The known Syringophilinae fauna from parrots comprises 28 species grouped in 5 genera, i.e., Megasyringophilus Fain, Bochkov & Mironov, 2000 (9 species), Neoaulobia Fain, Bochkov & Mironov, 2000 (11), Peristerophila Kethley, 1970 (3), Psittaciphilus Fain, Bochkov & Mironov, 2000 (2), and Terratosyringophilus Bochkov & Perez, 2002 (3). Syringophiline mites have been recorded on parrots belonging to all extant families, i.e., Cacatuidae, Psittacidae, Psittaculidae, and Strigopidae (Table 1).

Genus Megasyringophilus Fain, Bochkov & Mironov, 2000

This genus comprises large-sized syringophilids (total body length 950–1350), which are distinguished from the other genera by the combination of the following features in females: lateral hypostomal teeth are absent; the peritremes are M-shaped; the stylophore is rounded or slightly constricted posteriorly; the propodonotal shield is without pocket-like structures; the idiosoma and legs are with the full complement of smooth setae; legs I–IV are sub equal in thickness; the apodemes I are divergent, indistinctly fused to the apodemes II, and both apodemes are dissimilar in size and shape.

Currently, this genus comprises 11 species recorded in birds belonging to three orders; Accipitriformes, Psittaciformes, and Strigiformes [14], from the Afrotropical, Australian, Neotropical, Nearctic, Oriental, Oceanian, and Palearctic zoogeographical regions [47,74,75,76,77,78,79,80].

The Megasyringophilus fauna associated with parrots includes most of the described taxa of this genus and consists of nine species noted on representatives Cacatuidae, Psittaculidae, and Psittacidae.

Species included:

M. cacatua Glowska & Laniecka, 2013. Monoxenous parasite associated with Sulphur-crested Cockatoo Cacatua galerita (Latham) (Cacatuidae) from Australia [81].

M. cyanocephala Fain, Bochkov & Mironov, 2000. Oligoxenous species associated with psittaculid parrots of the genus Psittacula (Psittaculidae): Plum-headed Parakeet P. cyanocephala (Linnaeus), Alexandrine Parakeet P. eupatria (Linnaeus), and Rose-ringed Parakeet P. krameri (Scopoli) all host species from India [74,76].

M. dubinini Bochkov & Fain, 2003. Monoxenous parasite associated with Ornate Lorikeet Saudareos ornatus (Linnaeus) (Psittaculidae) from India [76].

M. eos Skoracki, 2005. Monoxenous parasite associated with Red Lory Eos bornea (Linnaeus) (Psittaculidae) from Indonesia [47].

M. geoffroyus Skoracki, 2005. Monoxenous parasite associated with Red-cheeked Parrot Geoffroyus geoffroyi (Bechstein) (Psittaculidae) from (Papua New Guinea) [47].

M. kethleyi Fain, Bochkov & Mironov, 2000. Mesostenoxenous parasite associated with parrots of the family Psittacidae: Jandaya Parakeet Aratinga jandaya (Gmelin) from Brazil, White-winged Parakeet Brotogeris versicolurus (St. Muller) from Brazil, and psittacid parrots of the genus Eupsittula: Orange-fronted Parakeet E. canicularis from Mexico, and Brown-throated Parakeet E. pertinax from Brazil [74,76,77].

M. platycercus Bochkov & Fain, 2003. Monoxenous parasite associated with Eastern Rosella Platycercus eximius (Shaw) (Psittaculidae) from Australia [76].

M. rhynchopsittae Bochkov & Perez, 2002. Monoxenous parasite associated with Thick-billed Parrot Rhynchopsitta pachyrhyncha (Swainson) (Psittacidae) from Mexico [75].

M. trichoglossus Fain, Bochkov & Mironov, 2000. Oligoxenous species associated with psittaculid parrots of the genus Trichoglossus (Psittaculidae): Olive-headed Lorikeet T. euteles (Temminck) from Indonesia, Scaly-breasted Lorikeet T. chlorolepidotus (Kuhl) from Australia, and unknown species Trichoglossus sp. from Papua New Guinea [47,74].

Genus Neoaulobia Fain, Bochkov & Mironov, 2000

The genus Neoaulobia comprises medium-sized syringophilids (total body length 430–730), exclusively associated with parrots. The females of the genus can be distinguished from other genera by the following combination of features: lateral hypostomal teeth are absent; the peritremes are M-shaped; the stylophore is slightly constricted posteriorly; the propodonotal shield is without pocket-like structures; the idiosoma is with the full complement of smooth setae; leg setae dTIII–IV or only dTIII are absent; legs I–IV are sub equal in thickness; the apodemes I are parallel and not fused to the apodemes II.

Currently, the Neoaulobia genus comprises 11 species recorded on members of the parrot families Cacatuidae, Psittaculidae, and Psittacidae in the Afrotropical, Australian, Oriental, Nearctic, and Neotropical regions [47,50,52,53,74,75,76,77,82].

Species included:

N. aratingae Fain, Bochkov & Mironov, 2000. Monoxenous parasite associated with Jandaya Parakeet Aratinga jandaya (Gmelin) (Psittacidae) from Brazil [74].

N. agapornis Fain, Bochkov & Mironov, 2000. Oligoxenous species associated with parrots of the genus Agapornis (Psittaculidae): Black-cheeked Lovebird A. nigrigenis Sclater from Zambia, Fischer’s Lovebird A. fischeri (Reichenow) from Tanzania, Yellow-collared Lovebird A. personatus Reichenow from Tanzania, Rosy-faced Lovebird A. roseicollis (Vieillot) from Namibia, Black-winged Lovebird A. taranta (Stanley) from Ethiopia [74,76].

N. cacatui Marciniak, Skoracki & Hromada, 2019. Mesostenoxenous parasite associated with cockatoos (Cacatuidae): Yellow-tailed Black-Cockatoo Calyptorhynchus funereus (Shaw) from Australia, and Palm Cockatoo Probosciger aterrimus (Gmelin) from Papua New Guinea [50].

N. krafti Skoracki, 2005. Monoxenous parasite associated with Long-billed Corella Cacatua tenuirostris (Kuhl) (Cacatuidae) from Australia [47].

N. unsoeldi Marciniak-Musial & Sikora 2002. Mesostenoxenous parasite associated with psittacid parrots: Turquoise-fronted Parrot Amazona aestiva (Linnaeus) from Paraguay, Red-and-green Macaw Ara chloropterus Gray from Costa Rica, and Burrowing Parakeet Cyanoliseus patagonus (Vieillot) from Argentina [53].

N. mexicana Bochkov & Perez, 2002. Oligoxenous species associated with psittacid parrots of the genus Eupsittula (Psittacidae): Orange-fronted Parakeet E. canicularis from Mexico, and Brown-throated Parakeet E. pertinax from Brazil [75,76].

N. mironovi Bochkov & Perez, 2002. Monoxenous parasite associated with Lilac-crowned Parrot Amazona finschi Sclater (Psittacidae) from Mexico [75,77].

N. pseudeos Marciniak-Musial, Hromada & Sikora, 2022. Monoxenous parasite associated with Dusky Lory Pseudeos fuscata (Blyth) (Psittaculidae) from Papua New Guinea [52].

N. psittaculae Fain, Bochkov & Mironov, 2000. Monoxenous parasite associated with Plum-headed Parakeet Psittacula cyanocephala (Linnaeus) (Psittaculidae) from India [74].

N. puylaerti (Skoracki & Dabert 1999). Metastenoxenous parasite associated with Philippine Hanging-Parrot Loriculus philippensis (St. Muller) (Psittaculidae) from Philippines, Yellow-throated Hanging-Parrot Loriculus pusillus Gray (Psittaculidae) from Indonesia, and Senegal Parrot Poicephalus senegalus (Linnaeus) (Psittacidae) from Togo [47,82].

N. skorackii Marciniak-Musial, Hromada & Sikora, 2022. Monoxenous parasite associated with Eastern Rosella Platycercus eximius (Shaw) (Psittaculidae) from Australia [52].

Genus Peristerophila Casto, 1980

The Peristerophila genus comprises medium- or large-sized syringophilids (total body length in homeomorphic form of females 535–750; in heteromorphic form of females 800–1000), distinguished from other genera by the following combination of features: lateral hypostomal teeth are absent; the peritremes are M-shaped; the stylophore is rounded posteriorly; the propodonotal shield is without pocket-like structures; the propodonotal setae vi are absent; leg setae dFII–IV and vsII are absent; legs I are thicker than II–IV; and the apodemes I are parallel and fused to the apodemes II. It is worth adding that in this genus, two forms of females (homeomorphic and heteromorphic) are present [83].

The genus comprises 15 species recorded on the broadest host spectrum among quill mite genera, and it consists of representatives of the following bird orders, Accipitriformes, Bucerotiformes, Columbiformes, Falconiformes, and Psittaciformes from the Holarctic, Afrotropical, Neotropical, Oriental, Oceanian, and Saharo-Arabian regions [12,51,83,84,85,86,87,88,89].

The fauna associated with parrots includes three species noted on representatives of the parrot families Psittaculidae, Psittacidae, and Strigopidae. Within these three mite species, two are exclusively related to parrots [51,75], but one—Peristerophila mucuya Casto, 1980—has psittaciform and columbiform hosts.

Species included:

P. forpi (Bochkov & Perez, 2002). Monoxenous parasite associated with Mexican Parrotlet Forpus cyanopygius (Souancé) (Psittacidae) from Mexico [75].

P. mucuya Casto, 1980. Polixenous parasite associated with hosts of the orders Psittaciformes and Columbiformes. The following parrot species are hosts for this quill mite: White-winged Parakeet Brotogeris versicolurus (St. Muller) (Psittacidae) from Brazil [53,76], Gray-hooded Parakeet Psilopsiagon aymara (d’Orbigny) (Psittacidae) from South America [76], and Coconut Lorikeet Trichoglossus haematodus (Linnaeus) (Psittaculidae) from Indonesia [76]. The columbiform hosts for this mite species are given in the recent paper of Kaszewska et al. [88].

P. nestoriae Marciniak, Skoracki & Hromada, 2019. Monoxenous parasite associated with New Zealand Kaka Nestor meridionalis (Gmelin) from New Zealand [51].

Genus Psittaciphilus Fain, Bochkov & Mironov, 2000

The genus Psittaciphilus comprises medium-sized syringophilids (total body length 600–800), distinguished from other genera by the following combination of features in females: lateral hypostomal teeth are absent; the peritremes are M-shaped; the stylophore is constricted posteriorly; the propodonotal shield is with pocket-like structures; the propodonotal setae vi are absent; leg setae dFII–IV and vsII are absent; legs I thicker than II–IV; the apodemes I are divergent and not fused to the apodemes II.

Currently, this genus comprises four species recorded on birds belonging to two orders, Columbiformes and Psittaciformes. All species have been recorded only in the Neotropical region [53,74,76,90].

The fauna associated with parrots includes two species noted on host representatives of the family Psittacidae.

Species included:

P. amazonae Fain, Bochkov & Mironov, 2000. Oligoxenous species associated with psittaculid parrots of the genus Amazona (Psittacidae): Turquoise-fronted Parrot A. aestiva (Linnaeus) from Brazil, Orange-winged Parrot A. amazonica (Linnaeus) from Colombia, Yellow-crowned Parrot A. ochrocephala Berlepsch from Brazil [74,76].

P. fritschi Fain, Bochkov & Mironov, 2000. Monoxenous parasite associated with unidentified parrot (Psittacidae) from South America [Amazonia] [74].

Genus Terratosyringophilus Bochkov & Perez, 2002

This genus comprises large-sized syringophilids (total body length 1370–1850) distinguished from other genera by the following combination of features: lateral hypostomal teeth are absent; the peritremes are M-shaped; the stylophore is rounded posteriorly; the propodonotal shield is without pocket-like structures; the propodonotal setae vi are absent; leg setae dFII and vsII are absent, dFIII–IV are present but replaced ventrally; legs I–II are thicker than III–IV; the apodemes I are parallel and fused to the apodemes II.

Terratosyringophilus includes five species recorded from birds of the orders Psittaciformes and Columbiformes. They were noted in the Nearctic, Neotropical, Oceanian, and Oriental regions [47,75,76,91,92]. Currently, three species of this genus have been recorded from parrots belonging to the families Psittaculidae and Psittacidae.

Species included:

T. loricinus Bochkov & Fain, 2003. Mesostenoxenous parasite associated with parrots of the family Psittaculidae: Chattering Lory Lorius garrulus (Linnaeus) from Indonesia [Halmahera Isl.], and Coconut Lorikeet Trichoglossus haematodus (Linnaeus) from Indonesia [Sumbawa Isl.] [76].

T. pioni Bochkov & Perez, 2002. Monoxenous parasite associated with White-crowned Parrot Pionus senilis (Spix) (Psittacidae) from Mexico [75].

T. reichholfi Skoracki & Sikora, 2008. Monoxenous parasite associated with Black-capped Lory Lorius lory (Linnaeus) (Psittaculidae) from Papua New Guinea [91].

3.1.2. Subfamily Picobiinae Johnston & Kethley, 1973

Mites of this subfamily differ from the Picobiinae by the presence of the truncated tibiotarsus of palps and rod-like proral setae of tarsuses I–IV. In addition, they exclusively occupy the quills of contour feathers, with one exception to this rule—Calamincola lobatus Casto, 1977—a representative of the enigmatic and monotypic genus found in the quills of wing feathers [93].

The Picobiinae fauna known from parrots comprises three genera and 17 species, i.e., Lawrencipicobia Skoracki & Hromada, 2013 (7 species), Pipicobia Glowska & Schmidt, 2014 (5), and Rafapicobia Skoracki, 2011 (5). Picobiinae mites have been recorded on parrots belonging to all extant families, i.e., Cacatuidae, Psittacidae, and Psittaculidae (Table 1).

The analysis of picobiinae relationships with the avian hosts in research provided by Skoracki et al. [22] shows that Picobiinae genera form two distinct monophyletic clades: Picobia-generic group and Neopicobia-generic-group. The clade Neopicobia-generic group comprises six genera, including all the below mentioned genera associated with parrots.

Genus Rafapicobia Skoracki, 2011

This genus comprises small-sized picobiines (total body length 450–650) distinguished from other genera by the following combination of features: the hypostomal apex tapering; the opisthonotal and genital lobes are absent; the pseudanal series is represented by two pairs of setae; the genital series with one pair of setae; apodemes I are without thorn-like protuberances; solenidia phi (φ) on tibiae I are absent.

Currently, 19 representatives of the genus Rafapicobia are associated with five bird orders: Coraciiformes, Gruiformes, Passeriformes, Piciformes, and Psittaciformes [14,94,95]. They have been recorded in the Afrotropical, Nearctic, Neotropical, Palaearctic, and Sino-Japanese regions [43,48,49,82,96,97,98,99]. Among them, five species are known to parasitize parrots from a single family, Psittacidae.

Species included:

R. brotogeris (Fain, Bochkov & Mironov, 2000). Mesostenoxenous parasite associated with psittacid parrots: Andean Parakeet Bolborhynchus orbygnesius (Souancé) from Peru, Yellow-chevroned Parakeet Brotogeris chiriri (Vieillot) from Paraguay, Cobalt-winged parakeet Brotogeris cyanoptera (Pelzeln) from Brazil, Orange-chinned Parakeet Brotogeris jugularis (St. Muller) from Panama, White-winged Parakeet Brotogeris versicolurus (St. Muller) from Brazil, Northern Red-shouldered Macaw Diopsittaca nobilis (Linnaeus) from Surinam, Peach-fronted Parakeet Eupsittula aurea (Gmelin) from Brazil, Brown-throated Parakeet Eupsittula pertinax (Linnaeus) from Surinam, Monk Parakeet Myiopsitta monachus (Boddaert) from Argentina, Pileated Parrot Pionopsitta pileata (Scopoli) from Paraguay, Mountain Parakeet Psilopsiagon aurifrons (Lesson) from Peru, Grey-hooded Parakeet Psilopsiagon aymara (d’Orbigny) from Bolivia, Scarlet-fronted Parakeet Psittacara wagleri (Gray) from Venezuela, Painted Parakeet Pyrrhura picta (St. Muller) from Guyana, Blue-crowned Parakeet Thectocercus acuticaudatus (Vieillot) from Argentina [43,53,74].

R. pyrrhura Marciniak-Musial & Sikora, 2022. Oligoxenous species associated with parrots of the genus Pyrrhura: Green-cheeked Parakeet P. molinae (Massena & Souance) from Bolivia, Maroon-bellied Parakeet P. frontalis (Vieillot), and Pearly Parakeet P. lepida (Wagler) both from Brazil [53].

R. trinidadi Marciniak-Musial & Sikora, 2022. Monoxenous parasite associated with Lilac-tailed Parrotlet Touit batavicus (Boddaert) from Trinidad and Tobago [53].

R. valdiviana Marciniak-Musial & Sikora, 2022. Mesostenoxenous parasite associated with: Austral Parakeet Enicognathus ferrugineus (St. Muller) from Chile, and Burrowing Parrot Cyanoliseus patagonus (Vieillot) from Argentina [53].

R. xanthopterygius Marciniak-Musial & Sikora, 2022. Monoxenous parasite associated with Blue-winged Forpus xanthopterygius (von Spix) from Brazil [53].

Genus Lawrencipicobia Skoracki & Hromada, 2013

The genus Lawrencipicobia comprises medium-sized picobiines (total body length 630–860), and differs from other genera by the combination of the following features: the hypostomal apex is flat; the opisthonotal and genital lobes are absent; the pseudanal setal series with two pairs; the genital series with one pair of setae; the apodemes I are with small thorn-like protuberances; solenidia phi (φ) on tibiae I are present.

Presently, this genus includes seven species exclusively associated with parrots and recorded from birds of the families Cacatuidae, Psittacidae, and Psittaculidae. They have been noted in the Afrotropical, Australian, and Oriental regions [50,52,53,100].

Species included:

L. ararauna Marciniak-Musial & Sikora, 2022. Monoxenous parasite associated with Black-headed Parrot Ara ararauna (Linnaeus) (Psittacidae) from [53].

L. arini Marciniak-Musial & Sikora, 2022. Mesostenoxenous parasite associated with psittacid parrots: White-bellied Parrot Pionites leucogaster (Kuhl) (Psittacidae) from Brazil, Black-headed Parrot Pionites melanocephalus (Linnaeus) (Psittacidae) from Surinam, and Maroon-bellied Parakeet Pyrrhura frontalis (Vieillot) (Psittacidae) from Paraguay [53].

L. calyptorhyncha Marciniak, Skoracki & Hromada, 2019. Monoxenous parasite associated with Glossy Black-Cockatoo Calyptorhynchus lathami (Temminck) (Cacatuidae) from Australia [50].

L. eclectus Marciniak-Musial, Hromada & Sikora 2022. Monoxenous parasite associated with Eclectus Parrot Eclectus roratus (St. Muller) (Psittaculidae) from Papua New Guinea [52].

L. poicephali (Skoracki & Dabert, 2002). Oligoxenous species associated with parrots of the genus Poicephalus (Psittacidae): Senegal Parrot P. senegalus versteri Finsch from Cameroon, Cape Parrot P. robustus (Gmelin) from DR Congo, Rwanda, Zambia, Red-fronted Parrot P. gulielmi (Jardine) from DR. Congo, Tanzania, Kenya, Cameroon, Red-bellied Parrot P. rufiventri (Rüppell) from Somalia, Meyer’s Parrot P. meyeri Cretzschmar from Zimbabwe, Rwanda, Kenya, Brown-necked Parrot P. fuscicollis Kuhl from Tanzania, Brown-headed Parrot P. cryptoxanthus (Peters) from Tanzania [100,101].

L. sulphurea Marciniak, Skoracki & Hromada, 2019. Monoxenous parasite associated with Yellow-crested Cockatoo Cacatua sulphurea (Gmelin) (Cacatuidae) from Indonesia [51].

L. touiti Marciniak-Musial & Sikora, 2022. Monoxenous parasite associated with Golden-tailed Parrotlet Touit surdus (Kuhl) (Psittacidae) from Brazil [53].

Genus Pipicobia Glowska and Schmidt, 2014

This genus comprises small-sized picobiines (total body length 430–690), distinguished from other genera by the following combination of features: the hypostomal apex is tapering; the opisthosomal and genital lobes are absent; each pseudanal and genital setal series is represented by one pair; apodemes I are with small thorn-like protuberances; solenidia phi (φ) on tibiae I are absent.

Members of this genus are known to parasitize birds of the orders Psittaciformes and Passeriformes and have been recorded in the Afrotropical, Australian, and Palearctic regions [47,102,103,104]. The Pipiobia fauna associated with parrots comprises five species recorded on birds from a single family Psittaculidae.

Species included:

P. cyclopsitta Marciniak-Musial, Hromada & Sikora, 2022. Monoxenous parasite associated with Double-Eyed Fig-Parrot Cyclopsitta diophthalma (Hombron & Jacquinot) Papua New Guinea [48,52]

P. fuscata Marciniak-Musial, Hromada & Sikora, 2022. Monoxenous parasite associated with Dusky Lory Pseudeos fuscata (Blyth) from Papua New Guinea [52].

P. tahitiana Marciniak-Musial, Hromada & Sikora, 2022. Monoxenous parasite associated with Blue Lorikeet Vini peruviana (St. Muller) from Tahiti [French Polynesia] [52].

P. malherbi Marciniak-Musial, Hromada & Sikora, 2022. Monoxenous parasite associated with Malherbe’s Parakeet Cyanoramphus malherbi Souance from New Zealand [52].

P. glossopsitta (Skoracki, Glowska & Sikora, 2008). Oligoxenous species associated with psittaculid parrots of the genus Parvipsitta (Psittaculidae): Purple-Crowned Lorikeet P. porphyrocephala (Dietrichsen), and Little Lorikeet P. pusilla (Shaw), both from Australia [48,52].

Table 1. Quill mite species of the family Syringophilidae parazitising birds of the order Psittaciformes with their distribution.

Quill Mite Species	Host Species	Host Family	Distribution	References
Subfamily Syringophilinae Lavoipierre, 1953
Genus Megasyringophilus Fain, Bochkov & Mironov, 2000
M. cacatua Glowska & Laniecka, 2013	Cacatua galerita (Latham)	Cacatuidae	Aust. (Australia)	[81]
M. cyanocephala Fain, Bochkov & Mironov, 2000	Psittacula cyanocephala (Linnaeus) *	Psittaculidae	Orie. (India)	[74]
	Psittacula eupatria (Linnaeus)	Psittaculidae	Orie. (India)	[76]
	Psittacula krameri (Scopoli)	Psittaculidae	Orie. (India)	[76]
M. dubinini Bochkov & Fain, 2003	Saudaeeos ornatus (Linnaeus)	Psittaculidae	Orie. (India)	[76]
M. eos Skoracki, 2005	Eos bornea (Linnaeus)	Psittaculidae	Orie. (Indonesia)	[47]
M. geoffroyus Skoracki, 2005	Geoffroyus geoffroyi (Bechstein)	Psittaculidae	Ocea. (Papua New Guinea)	[47]
M. kethleyi Fain, Bochkov & Mironov, 2000	Aratinga jandaya (Gmelin) *	Psittacidae	Neot. (Brazil)	[74]
	Brotogeris versicolurus (St. Muller)	Psittacidae	Neot. (Brazil)	[76]
	Eupsitulla canicularis (Linnaeus)	Psittacidae	Near. (Mexico)	[77]
	Eupsittula pertinax (Linnaeus)	Psittacidae	Neot. (Brazil)	[76]
M. platycercus Bochkov & Fain, 2003	Platycercus eximius (Shaw)	Psittaculidae	Austr. (Australia)	[74]
M. rhynchopsittae Bochkov & Perez, 2002	Rhynchopsitta pachyrhyncha (Swainson)	Psittacidae	Near. (Mexico)	[75]
M. trichoglossus Fain, Bochkov & Mironov, 2000	Trichoglossus sp.	Psittaculidae	Ocea. (Papua New Guinea)	[74]
	Trichoglossus chlorolepidotus (Kuhl)	Psittaculidae	Austr. (Australia)	[47]
	Trichoglossus euteles (Temminck)	Psittaculidae	Orie. (Indonesia)	[47]
Genus Neoaulobia Fain, Bochkov & Mironov, 2000
N. agapornis Fain, Bochkov & Mironov, 2000	Agapornis nigrigenis * Sclater	Psittaculidae	Afro. (Zambia)	[74]
	Agapornis fischeri (Reichenow)	Psittaculidae	Afro. (Tanzania)	[76]
	Agapornis personatus Reichenow	Psittaculidae	Afro. (Tanzania)	[76]
	Agapornis roseicollis (Vieillot)	Psittaculidae	Afro. (Namibia)	[76]
	Agapornis taranta (Stanley)	Psittaculidae	Afro. (Ethiopia)	[76]
N. aratingae Fain, Bochkov & Mironov, 2000	Aratinga jandaya (Gmelin)	Psittacidae	Neot. (Brazil)	[74]
N. cacatui Marciniak, Skoracki & Hromada, 2019	Calyptorhynchus funereus * (Shaw)	Cacatuidae	Austr. (Australia)	[50]
N. cacatui Marciniak, Skoracki & Hromada, 2019	Probosciger aterrimus (Gmelin)	Cacatuidae	Ocea. (Papua New Guinea)	[50]
N. krafti Skoracki, 2005	Cacatua tenuirostris (Kuhl)	Cacatuidae	Austr. (Australia)	[47]
N. mexicana Bochkov & Perez, 2002	Eupsittula canicularis * (Linnaeus)	Psittacidae	Near. (Mexico)	[75]
N. mexicana Bochkov & Perez, 2002	Eupsittula pertinax (Linnaeus)	Psittacidae	Neot. (Brazil)	[76]
N. mironovi Bochkov & Perez, 2002	Amazona finschi Sclater	Psittacidae	Near. (Mexico)	[75,77]
N. pseudeos Marciniak-Musial, Hromada & Sikora, 2022	Pseudeos fuscata (Blyth)	Psittaculidae	Ocea. (Papua New Guinea)	[52]
N. psittaculae Fain, Bochkov & Mironov, 2000	Psittacula cyanocephala (Linnaeus)	Psittaculidae	Orie. (India)	[74]
N. puylaerti (Skoracki & Dabert 1999)	Loriculus philippensis (St. Muller)	Psittaculidae	Orie. (Philippines)	[47]
	Loriculus pusillus Gray	Psittaculidae	Orie. (Indonesia)	[47]
	Poicephalus senegalus (Linnaeus)	Psittacidae	Afro. (Togo)	[82]
N. skorackii Marciniak-Musial, Hromada & Sikora, 2022	Platycercus eximius (Shaw)	Psittaculidae	Austr. (Australia)	[52]
N. unsoeldi Marciniak-Musial & Sikora 2002	Amazona aestiva (Linnaeus)	Psittacidae	Neot. (Paraguay)	[53]
	Ara chloropterus Gray	Psittacidae	Pana. (Costa Rica)	[53]
	Cyanoliseus patagonus * (Vieillot)	Psittacidae	Neot. (Argentina)	[53]
Genus Peristerophila Kethley, 1970
P. forpi (Bochkov & Perez, 2002)	Forpus cyanopygius (Souancé)	Psittacidae	Near. (Mexico)	[75]
P. mucuya Casto, 1980	Brotogeris versicolurus (St. Muller)	Psittacidae	Neot. (Brazil)	[53,76]
	Psilopsiagon aymara (d’Orbigny)	Psittacidae	Neot. (South America)	[76]
	Trichoglossus haematodus (Linnaeus)	Psittaculidae	Orie. (Indonesia: Sumbawa Isl.)	[76]
	Columbina minuta ** Linnaeus	Claravinae	Neot. (Paraguay)	[88]
	Columbina passerina ,* Linnaeus	Claravinae	Neot. (Colombia, Surinam); Near. (USA)	[84,89]
	Columbina squammata ** (Lesson)	Claravinae	Neot. (Brazil, Paraguay)	[76,88]
	Columbina talpacoti ** (Temminck)	Claravinae	Neot. (Brazil, Surinam, Trinidad and Tobago); Pala. (Monaco)	[88,89]
	Geophaps plumifera ** Gould	Claravinae	Aust. (Australia)	[76]
	Metriopelia ceciliae ** (Lesson)	Claravinae	Neot. (Peru)	[88]
	Metriopelia melanoptera ** (Molina)	Claravinae	Neot. (Argentina)	[88]
P. nestoriae Marciniak, Skoracki & Hromada, 2019	Nestor meridionalis (Gmelin)	Strigopidae	Austr. (New Zealand)	[51]
Genus Psittaciphilus Bochkov & Mironov, 2000
P. amazonae Fain, Bochkov & Mironov, 2000	Amazona aestiva (Linnaeus)	Psittacidae	Neot. (Brazil)	[76]
	Amazona amazonica * (Linnaeus)	Psittacidae	Neot. (Colombia)	[74]
	Amazona ochrocephala Berlepsch	Psittacidae	Neot. (Brazil)	[49]
P. fritschi Fain, Bochkov & Mironov, 2000	unidentified parrot	Psittacidae	Neot. (South America [Amazonia])	[70]
Genus Terratosyringophilus Bochkov & Perez, 2002
T. loricinus Bochkov & Fain, 2003	Lorius garrulus * (Linnaeus)	Psittaculidae	Orie. (Indonesia: Halmahera Isl.)	[72]
T. loricinus Bochkov & Fain, 2003	Trichoglossus haematodus (Linnaeus)	Psittaculidae	Orie. (Indonesia: Sumbawa Isl.)	[72]
T. pioni Bochkov & Perez, 2002	Pionus senilis (von Spix)	Psittacidae	Near. (Mexico)	[75]
T. reichholfi Skoracki & Sikora, 2008	Lorius lory (Linnaeus)	Psittaculidae	Ocea. (Papua New Guinea)	[91]
Subfamily Picobiinae Johnson & Kethley, 1973
Genus Lawrencipicobia Skoracki & Hromada, 2013
L. ararauna Marciniak-Musial & Sikora, 2022	Ara ararauna (Linnaeus)	Psittacidae	Neot. (Brazil)	[53]
L. arini Marciniak-Musial & Sikora, 2022	Pionites leucogaster * (Kuhl)	Psittacidae	Neot. (Brazil)	[53]
	Pionites melanocephalus (Linnaeus)	Psittacidae	Neot. (Surinam)	[53]
	Pyrrhura frontalis (Vieillot)	Psittacidae	Neot. (Paraguay)	[53]
L. calyptorhyncha Marciniak, Skoracki & Hromada, 2019	Calyptorhynchus lathami (Temminck)	Cacatuidae	Austr. (Australia)	[50]
L. eclectus Marciniak-Musial, Hromada & Sikora 2022	Eclectus roratus (St. Muller)	Psittaculidae	Ocea. (Papua New Guinea)	[52]
L. poicephali (Skoracki & Dabert, 2002)	Poicephalus senegalus versteri * Finsch	Psittacidae	Afro. (Cameroon)	[100]
	Poicephalus robustus (Gmelin)	Psittacidae	Afro. (DR Congo, Rwanda, Zambia)	[101]
	Poicephalus gulielmi (Jardine)	Psittacidae	Afro. (DR. Congo, Tanzania, Kenya, Cameroon)	[101]
	Poicephalus rufiventri (Rüppell)	Psittacidae	Afro. (Somalia)	[101]
	Poicephalus meyeri Cretzschmar	Psittacidae	Afro. (Zimbabwe, Rwanda, Kenya)	[101]
	Poicephalus fuscicollis Kuhl	Psittacidae	Afro. (Tanzania)	[101]
	Poicephalus cryptoxanthus (Peters)	Psittacidae	Afro. (Tanzania)	[101]
L. sulphurea Marciniak, Skoracki & Hromada, 2019	Cacatua sulphurea (Gmelin)	Cacatuidae	Orie. (Indonesia)	[50]
L. touiti Marciniak-Musial & Sikora, 2022	Touit surdus (Kuhl)	Psittacidae	Neot. (Brazil)	[53]
Genus Pipicobia Glowska & Schmidt, 2014
P. cyclopsitta Marciniak-Musial, Hromada & Sikora, 2022	Cyclopsitta diophthalma (Hombron & Jacquinot)	Psittaculidae	Ocea. (Papua New Guinea)	[52]
P. fuscata Marciniak-Musial, Hromada & Sikora, 2022	Pseudeos fuscata (Blyth)	Psittaculidae	Ocea. (Papua New Guinea)	[52]
P. glossopsitta (Skoracki, Glowska & Sikora, 2008)	Parvipsitta porphyrocephala * (Dietrichsen)	Psittaculidae	Austr. (Australia)	[48]
P. glossopsitta (Skoracki, Glowska & Sikora, 2008)	Parvipsitta pusilla (Shaw)	Psittaculidae	Austr. (Australia)	[52]
P. malherbi Marciniak-Musial, Hromada & Sikora, 2022	Cyanoramphus malherbi Souancé	Psittaculidae	Austr. (New Zealand)	[52]
P. tahitiana Marciniak-Musial, Hromada & Sikora, 2022	Vini peruviana (St. Muller)	Psittaculidae	Ocea. (Tahiti [French Polynesia])	[52]
Genus Rafapicobia Skoracki, 2011
R. brotogeris (Fain, Bochkov & Mironov, 2000)	Brotogeris cyanoptera * (Pelzeln)	Psittacidae	Neot. (Brazil)	[43,53,74]
	Brotogeris chiriri (Vieillot)	Psittacidae	Neot. (Paraguay)	[53]
	Brotogeris jugularis (St. Muller)	Psittacidae	Pana. (Panama)	[53]
	Brotogeris versicolurus (St. Muller)	Psittacidae	Neot. (Brazil)	[53]
	Bolborhynchus orbygnesius (Souancé)	Psittacidae	Neot. (Peru)	[53]
	Diopsittaca nobilis (Linnaeus)	Psittacidae	Neot. (Surinam)	[53]
	Eupsittula pertinax (Linnaeus)	Psittacidae	Neot. (Surinam)	[53]
	Eupsittula aurea (Gmelin)	Psittacidae	Neot. (Brazil)	[53]
	Myiopsitta monachus (Boddaert)	Psittacidae	Neot. (Argentina)	[53]
	Pionopsitta pileata (Scopoli)	Psittacidae	Neot. (Paraguay)	[53]
	Psilopsiagon aymara (d’Orbigny)	Psittacidae	Neot. (Bolivia)	[53]
	Psilopsiagon aurifrons (Lesson)	Psittacidae	Neot. (Peru)	[53]
	Psittacara wagleri (Gray)	Psittacidae	Neot. (Venezuela)	[53]
	Pyrrhura picta (St. Muller)	Psittacidae	Neot. (Guyana)	[43]
	Thectocercus acuticaudatus (Vieillot)	Psittacidae	Neot. (Argentina)	[53]
R. pyrrhura Marciniak-Musial & Sikora, 2022	Pyrrhura molinae * (Massena & Souancé)	Psittacidae	Neot. (Bolivia)	[53]
	Pyrrhura lepida (Wagler)	Psittacidae	Neot. (Brazil)	[53]
	Pyrrhura frontalis (Vieillot)	Psittacidae	Neot. (Brazil)	[53]
R. trinidadi Marciniak-Musial & Sikora, 2022	Touit batavicus (Boddaert)	Psittacidae	Neot. (Trinidad and Tobago)	[53]
R. valdiviana Marciniak-Musial & Sikora, 2022	Enicognathus ferrugineus * (St. Muller)	Psittacidae	Neot. (Chile)	[53]
R. valdiviana Marciniak-Musial & Sikora, 2022	Cyanoliseus patagonus (Vieillot)	Psittacidae	Neot. (Argentina)	[53]
R. xanthopterygius Marciniak-Musial & Sikora, 2022	Forpus xanthopterygius (von Spix)	Psittacidae	Neot. (Brazil)	[53]

Zoogeographical regions: Afro.—Afrotropical; Aust.—Australian, Near.—Nearctic, Neot.—Neotropical, Ocea.—Oceanian, Orie.—Oriental, Pala.—Palaearctic, Pana.—Panamanian, Sa-Arab.—Saharo-Arabian, Si-Jap.—Sino-Japanese (according to Holt et al. [52]). *—type host; **—host from order Columbiformes. Locality established based on the host distribution.

3.1.3. Key to the Syringophilid Subfamilies, Genera, and Species Associated with Parrots (the Morphological Terminology and Chaetotaxy follow Skoracki [12])

Tibiotarsus of palps rounded on distal margin. Prorals setae p’ and p” multiserrate, fan-like … subfamily Syringophilinae Lavoipierre, 1953 … 2
–
Tibiotarsus of palps truncate on distal margin. Prorals setae p’ and p” with two minute tines, rod-like … subfamily Picobiinae Johnston & Kethley, 1973 … 28
Propodonotal setae vi absent … 3
–
Propodonotal setae vi preset … 9
Setae dFIII-IV absent … 4
–
Setae dFIII-IV present, but placed ventrally … genus Terratosyringophilus Bochkov & Perez 2002 … 7
Setae ve and si situated at same transverse level. Pocket-like structures in anterior part of propodonotum present … genus Psittaciphilus Fain, Bochkov & Mironov, 2000 … 5
–
Setae ve situated anterior to si. Pocket-like structures in anterior part of propodonotum absent … genus Peristerophila Kethley, 1970 … 6
Lengths of setae ve and si 83–101 and 18–22, respectively … Ps. fritschi Fain, Bochkov & Mironov, 2000
–
Lengths of setae ve and si 110–123 and 30–47, respectively … Ps. amazonae Fain, Bochkov & Mironov, 2000
Propodonotal shield divided into 3 sclerites … Pe. mucuya Casto, 1980
–
Propodonotal shield entire … Pe. nestoriae Marciniak, Skoracki & Hromada, 2019
Setae si at least two times longer than ve … T. reicholfi Skoracki & Sikora, 2008
–
Setae si less than 1.3 times longer than ve … 8
Setae ve and si shorter than 200 … T. loricinus Bochkov & Fain, 2003
–
Setae ve and si longer than 340 … T. pioni Bochkov & Perez, 2002
Leg setae dTIII absent. Apodemes I parallel … Neoaulobia Fain, Bochkov & Mironov, 2000 … 10
–
Leg setae dTIII present. Apodemes I divergent … Megasyringophilus Fain, Bochkov & Mironov, 2000 … 20
Setae dTIV absent … 11
–
Setae dTIV present … 15
Setae ve distinctly longer than vi … 12
–
Setae vi and ve subequal in length … 13
Each lateral branch of peritremes with 7 chambers … N. pseudeos Marciniak-Musial, Hromada & Sikora, 2022
–
Each lateral branch of peritremes with 3 chambers … N. agapornis Fain, Bochkov & Mironov, 2000
Bases of setae d1 situated close to anterior margin of hysteronotal shield. Each medial branch of peritremes with 3–5 chambers. Length of setae vi 70–105 … N. mironovi Bochkov & Perez, 2002
–
Bases of setae d1 situated far from anterior margin of hysteronotal shield. Each medial branch of peritremes with 1–2 chambers. Length of setae vi 20–50 … 14
Lateral branch of peritremes with 5–6 chambers. Lengths of setae d1, e2 and f2 25–45, 40–57 and 50–65, respectively … N. mexicana Bochkov & Perez, 2002
–
Lateral branch of peritremes with 4 chambers. Lengths of setae d1, e2 and f2 74–105, 120–166 and 70–115, respectively … N. aratingae Fain, Bochkov & Mironov, 2000
Hysteronotal shield not fused to pygidial shield … 16
–
Hysteronotal shield fused to pygidial shield … 18
Lengths of stylophore 250–260. Bases of setae d1 situated distant from anterior margin of hysteronotal shield … N. krafti Skoracki, 2005
–
Lengths of stylophore 140–160. Bases of setae d1 are situated close to anterior margin of hysteronotal shield … 17
Each lateral branch of peritremes with 3 chambers. Stylophore and coxal fields punctate. Setae g2 36–52 long … N. cacatui Marciniak, Skoracki & Hromada, 2019
–
Each lateral branch of peritremes with 4 chambers. Stylophore and coxal fields apunctate. Setae g2 13–23 long … N. skorackii Marciniak-Musial, Hromada & Sikora, 2022
Each lateral branch of peritremes with 2–3 chambers. Bases of setae d1 situated distant from anterior margin of hysteronotal shield. Stylophore 125–136 long … N. unsoeldi Marciniak-Musial & Sikora, 2022
–
Each lateral branch of peritremes with 4 chambers. Bases of setae d1 situated close to anterior margin of hysteronotal shield. Stylophore 160–196 long … 19
Hysteronotal shield apunctate; bases of setae e2 situated near lateral margins of this shield … N. puylaerti (Skoracki & Dabert, 1999)
–
Hysteronotal shield punctate in posterior part; bases of setae e2 situated on this shield … N. psittaculae Fain, Bochkov & Mironov, 2000
Tarsal claws of legs III and IV without basal angles … 21
–
Tarsal claws of legs III and IV with basal angles … 24
Stylophore constricted posteriorly … 22
–
Stylophore rounded posteriorly … 23
Setae ve about 4 times longer than vi. Length of setae g1 115–130. Hysteronotal shield well sclerotized … M. geoffroyus Skoracki, 2005
–
Setae ve twice as long as vi. Length of setae g1 50. Hysteronotal shield weakly sclerotized or absent … M. cyanocephala Fain, Bochkov & Mironov, 2000
Length ratio of setae vi:ve 1:5. Setae g2 twice shorter than ag1. Hysteronotal shield present … M. cacatua Glowska & Laniecka, 2013
–
Length ratio of setae vi:ve 1:2.3. Setae g2 long, subequal to ag1. Hysteronotal shield absent … M. platycercus Bochkov & Fain, 2003
Hypostomal apex without median protuberances … M. dubinini Bochkov & Fain, 2003
–
Hypostomal apex with 1–3 pairs of median protuberances … 25
Setae tc′ and tc″ of the legs III–IV subequal in length … M. trichoglossus Fain, Bochkov & Mironov, 2000
–
Setae tc″ of the legs III–IV distinctly longer than tc′ of legs III–IV … 26
Hysteronotal shield absent … 27
–
Hysteronotal shield well-developed … M. rhynchopsittae Bochkov & Perez, 2002
Setae se situated posterior to level of setae c2. Bases of setae d1 situated equidistant between setae d2 and e2. Setae ag1 longer than g2 … M. eos Skoracki, 2005
–
Setae se situated anterior to level of setae c2. Bases of setae d1 situated closer to d2 than to e2. Setae ag1 and g2 subequal in length … M. kethleyi Fain, Bochkov & Mironov, 2000
Solenidion phi on tibia I present … Lawrencipicobia Skoracki & Hromada, 2013 … 29
–
Solenidion phi on tibia I absent … 35
Hysteronotal shield absent … 30
–
Hysteronotal shield present and reduced to two small sclerites surrounding bases of setae d1 … 32
Bases of setae c1 situated posterior to se. Two pairs of pseudanal setae (ps) present … L. poicephali (Skoracki & Dabert, 2002)
–
Bases of setae c1 and se situated at same transverse level. One pair of pseudanal setae (ps) present … 31
Agenital shield absent. Setae g1 setiform and 20 long … L. sulphurea Marciniak, Skoracki & Hromada, 2019
–
Agenital shield present as two narrow plates above bases of ag1. Setae g1 as microsetae and 10 long … L. calyptorhyncha Marciniak, Skoracki & Hromada, 2019
Posterior end of apodemes I without small thorn-like protuberances … L. eclectus Marciniak-Musial, Hromada & Sikora, 2022
–
Posterior end of apodemes I with small thorn-like protuberances … 33
Propodonotal shield without striae in middle part. Setae c1 and se situated at same transverse level. Coxal felds III–IV and alveoles surrounding bases of setae ag1 with minute punctuations … L. arini Marciniak-Musial & Sikora, 2022
–
Propodonotal shield with striae in middle part. Setae c1 situated posterior to se. Coxal felds III–IV and alveoles surrounding bases of setae ag1 apunctate … 34
Pygidal shield weakly sclerotized with indistinct margins. Setae ve situated slightly posterior to vi. Lengths of setae c1, d1 and ag3 184–217, 134–148 and 182–216, respectively … L. ararauna Marciniak-Musial & Sikora, 2022
–
Pygidal shield well sclerotized with clearly visible margins. Setae vi and ve situated at same transverse level. Lengths of setae c1, d1 and ag3 307, 186 and 261, respectively … L. touiti Marciniak-Musial & Sikora, 2022
Two pairs of pseudanal setae (ps1, ps2) present … Rafapicobia Skoracki, 2011 … 36
–
One pair of pseudanal setae (ps1) present … Pipicobia Glowska & Schmidt, 2014 … 40
Agenital plates absent … 37
–
Agenital plates as two longitudinal sclerites … 38
Bases of setae c1 and se situated at same transverse level. Length of setae ag2 and 4c 5 and 75, respectively … R. brotogeris (Fain, Bochkov & Mironov, 2000)
–
Bases of setae c1 situated anterior to se. Length of setae ag2 and 4c 18–23 and 120–154, respectively … R. valdiviana Marciniak-Musial & Sikora, 2022
Each medial branch of peritremes with 4–6 chambers. Setae f2 subequal or slightly (1.2–1.5 times) longer than f1 … 39
–
Each medial branch of peritremes with 6–7 chambers. Setae f2 about 2–3.5 times longer than f1 … R. trinidadi Marciniak-Musial & Sikora, 2022
Stylophore 111–118 long … R. xanthopterygius Marciniak-Musial & Sikora, 2022
–
Stylophore 136–143 long … R. pyrrhura Marciniak-Musial & Sikora, 2022
Agenital shield present as two longitudinal sclerites with ag1 situated on posterior margin of shield … P. cyclopsitta Marciniak-Musial, Hromada & Sikora, 2022
–
Agenital shield absent … 41
Anterior margin of pygidial shield reaching level of seate e2 … P. glossopsitta (Skoracki, Glowska & Sikora, 2008)
–
Anterior margin of pygidial shield not reaching level of seate e2 … 42
Length of setae ve 60–80 … 43
–
Length of setae ve 35–50 … P. fuscata Marciniak-Musial, Hromada & Sikora, 2022
Pygidial shield apunctate. Propodonotal shield weakly sclerotized, striae visible … P. malherbi Marciniak-Musial, Hromada & Sikora, 2022
–
Pygidial shield punctate. Propodonotal shield well developed and without striae … P. tahitiana Marciniak-Musial, Hromada & Sikora, 2022

3.2. Prevalence

In this study, we investigated a total of 1524 host individuals belonging to 195 species (50% of the global parrot fauna on the species level), 73 genera (76% of the global parrot fauna on the generic level), and four families of the order Psittaciformes (100% of the global parrot fauna on the family level). Among them, 89 individuals representing 46 species have been infested by quill mites belonging to the following genera: Megasyringophilus Fain, Bochkov & Mironov, 2000 (9 species), Neoaulobia Fain, Bochkov & Mironov, 2000 (11 species), Peristerophila Kethley, 1970 (3 species), Psittaciphilus Fain, Bochkov & Mironov, 2000 (2 species), Terratosyringophilus Bochkov & Perez, 2002 (3 species) (subfamily Syringophilinae), Lawrencipicobia Skoracki & Hromada, 2013 (7 species), Pipicobia Glowska & Schmidt, 2014 (5 species), and Rafapicobia Skoracki, 2011 (5 species) (subfamily Picobiinae) (Table 2 and Tables S1 and S3).

The index of prevalence (IP) of host species from Psittaciformes ranges from 2.8% to 100% (IP = 100 in 8 cases); the 95% confidence intervals (the Sterne method) varied from 0.1 to 100 (Table 2). We grouped host species into four classes according to the prevalence index:

Low IP 1–25%—Eupsitulla aurea, Forpus xanthopterygius, Amazona aestiva, Pyrrhura frontalis, Thectocercus acuticaudatus, Brotogeris versicolurus, Myiopsitta monachus, Pseudeos fuscata, Eclectus roratus, Diopsittaca nobilis, Psittacara wagleri, Brotogeris chiriri, Cyanoliseus patagonus, Enicognathus ferrugineus, Eupsitulla pertinax, Pionopsitta pileata, Parvipsitta porphyrocephala, Pionites melanocephalus, Touit batavicus, Pyrrhura molinae, Poicephalus cryptoxanthus, Poicephalus gulielmi, Pionites leucogaster, Poicephalus meyeri, Poicephalus robustus, Bolborhynchus orbygnesius, Nestor meridionalis, and Touit surdus.

Middle IP 26–50%—Poicephalus rufiventris, Brotogeris juglaris, Cacatua sulphurea, Calyptorhynchus funereus, Cyclopsitta diophthalma, Parvipsitta pusilla, Poicephalus fuscicollis, Amazona ochrocephala, Brotogeris cyanoptera, Platycercus eximius, and Psilopsiagon aymara.

High IP 51–75%—None.

Extremely high 76–100%—Ara ararauna, Ara chloropterus, Calyptorhynchus lathami, Cyanoramphus malherbi, Probosciger aterrimus, Psilopsiagon aurifrons, Pyrrhura lepida, and Vini peruviana.

In our material, 58 host species (257 individuals) were not infested by the syringophilid mites (excluded from Table 2), i.e.,

Cacatuidae: Callocephalon fimbriatum (Grant) [N = 1].

Psittaculidae: Agapornis fischeri Reichenow [N = 6], A. lilianae Shelley [N = 2], A. nigrigenis Sclater [N = 1], A. personatus Reichenow [N = 1], A. taranta Stanley [N = 4], A. pullarius (Linnaeus) [N = 3], Aprosmictus erythropterus (Gmelin) [N = 3], A. jonquillaceus (Vieillot) [N = 6], Barnardius zonarius (Shaw) [N = 3], Chalcopsitta atra (Scopoli) [N = 3], Ch. duivenbodei (Dubois) [N = 7], Charmosyna placentis (Temminck) [N = 2], Coracopsis nigra sibilans Milne-Edwards & Oustalet [N = 2], Coracopsis vasa comorensis (Peters) [N = 2], Cyanoramphus auriceps (Kuhl) [N = 1], Eos bornea (Linnaeus) [N = 2], Eos squamata (Boddaert) [N = 1], Forpus xanthops (Salvin) [N = 4], Geoffroyus geoffroyi (Bechstein) [N = 33], Geoffroyus heteroclitus Bonaparte [N = 1], Geoffroyus simplex (Meyer) [N = 1], Loriculus aurantiifrons Schlegel [N = 1], L. galgulus Linnaeus [N = 2], L. philippensis (Müller) [N = 2], L. pusillus Gray [N = 6], L. stigmatus (Müller) [N = 1], L. vernalis (Sparrman) [N = 2], Lorius domicella (Linnaeus) [N = 1], Lorius garrulous (Linnaeus) [N = 1], Lorius hypoinochrous Gray [N = 5], Lorius lory (Linnaeus) [N = 20], Glossopsitta concinna (Shaw) [N = 4], Melopsittacus undulates (Shaw) [N = 4], Micropsitta bruijnii (Salvadori) [N = 1], M. keiensis (Salvadori) [N = 3], M. pusio (Sclater) [N = 2], Polytelis anthopeplus Lear [N = 1], Prioniturus luconensis Steere [N = 2], P. mada Hartert [N = 1], P. platurus (Vieillot) [N = 3], Psittinus cyanurus Forster [N = 4], Psittaculirostris edwardsii (Oustalet) [N = 12], Psittacula alexandri (Linnaeus) [N = 7], P. cyanocephala (Linnaeus) [N = 8], P. eupatria (Linnaeus) [N = 1], P. himalayana (Lesson) [N = 1], P. longicauda (Boddaert) [N = 12], P. krameri (Scopoli) [N = 8], Psitteuteles versicolor (Lear) [N = 1], Psittrichas fulgidus (Lesson) [N = 5], Saudareos ornatus (Linnaeus) [N = 2], Tanygnathus magalorhynchos (Boddaert) [N = 3], T. sumatranus (Raffles) [N = 3], Trichoglossus haematodus (Linnaeus) [N = 32], Vini australis (Gmelin) [N = 2].

Strigopidae: Nestor notabilis Gould [N = 1], Strigops habroptila Gray [N = 1].

Table 2. Host species infested by quill mites with habitat and the index of prevalence (IP) and 95% confidence interval (CI, Sterne’s method).

Host Species		Exa.	Inf.	IP; CI	Mite Species	Habitat
Amazona aestiva	Turquoise-fronted Parrot	25	1	4 (0.2–19.6)	Ne. unsoeldi	covert
Amazona ochrocephala	Yellow-crowned Parrot	2	1	50 (2.5–97.5)	Ps. amazonae	covert
Ara ararauna	Chestnut-fronted Macaw	1	1	100 (5.0–100)	La. ararauna	contour
Ara chloropterus	Red-and-green Macaw	1	1	100 (5.0–100)	Ne. unsoeldi	covert
Bolborhynchus orbygnesius	Andean Parakeet	4	1	25 (1.3–75.1)	Ra. brotogeris	contour
Brotogeris chiriri	Yellow-chevroned Parakeet	20	2	10 (1.8–32.0)	Ra. brotogeris	contour
Brotogeris cyanoptera	Cobalt-winged Parakeet	2	1	50 (2.5–97.5)	Ra. brotogeris	contour
Brootgeris juglaris	Orange-chinned Parakeet	7	2	28.6 (5.3–65.9)	Ra. brotogeris	contour
Brotogeris versicolurus	White-winged Parakeet	42	2	4.8 (0.9–16.3)	Ra. brotogeris	contour
Brotogeris versicolurus	White-winged Parakeet	42	2	4.8 (0.9–16.3)	Pe. mucucya	covert
Cacatua sulphurea	Yellow-crested Cockatoo	3	1	33.3 (1.7–86.5)	La. sulphurea	contour
Calyptorhynchus funereus	Yellow-tailed Black-Cockatoo	3	1	33.3 (1.7–86.5)	Ne. cacatui	covert
Calyptorhynchus lathami	Glossy Black-Cockatoo	1	1	100 (5.0–100)	La. calyptorhychus	contour
Cyanoliseus patagonus	Burrowing Parakeet	9	1	11.1 (0.6–44.4)	Ra. valdiviana	contour
Cyanoliseus patagonus	Burrowing Parakeet	9	1	11.1 (0.6–44.4)	Ne. unsoeldi	covert
Cyanoramphus malherbi	Malherbe’s Parakeet	1	1	100 (5.0–100)	Pi. malherbi	contour
Cyclopsitta diophthalma	Double-eyed Fig-Parrot	3	1	33.3 (1.7–86.5)	Pi. cyclopsitta	contour
Diopsittaca nobilis	Red-shouldered Macaw	11	1	9.1 (0.5–40.5)	Ra. brotogeris	contour
Eclectus roratus	Eclectus Parrot	26	2	7.7 (1.4–24.6)	La. eclectus	contour
Enicognathus ferrugineus	Austral Parakeet	9	1	11.1 (0.6–44.4)	Ra. valdiviana	contour
Eupsitulla aurea	Peach-fronted Parakeet	36	1	2.8 (0.1–14.8)	Ra. brotogeris	contour
Eupsitulla pertinax	Brown-throated Parakeet	18	2	11.1 (2.0–33.0)	Ra. brotogeris	contour
Forpus xanthopterygius	Blue-winged Parrotlet	33	1	3 (0.2–16.1)	Ra. xanthopterygius	contour
Parvipsitta porphyrocephala	Purple-crowned Lorikeet	4	1	12.5 (1.3–75.1)	Pi. glossopsitta	contour
Parvipsitta pusilla	Little Lorikeet	3	1	33.3 (1.7–86.5)	Pi. glossopsitta	contour
Myiopsitta monachus	Monk Parakeet	18	1	5.6 (0.3–27.1)	Ra. brotogeris	contour
Nestor meridionalis	New Zealand Kaka	4	1	25 (1.3–75.1)	Pe. nestoriae	contour
Pionites leucogaster	White-bellied Parrot	5	1	20 (1.0–65.7)	La. arini	contour
Pionites melanocephalus	Black-headed Parrot	8	1	12.5 (0.6–5.0)	La. arini	contour
Pionopsitta pileata	Pileated Parrot	9	1	11. 1 (0.6–44.4)	Ra. brotogeris	contour
Platycercus eximius	Eastern Rosella	2	1	50 (2.5–97.5)	Ne. skoracki	covert
Poicephalus cryptoxanthus	Brown-headed Parrot	11	2	18.2 (3.3–50.0)	La. poicephali	contour
Poicephalus flavifrons	Yellow-fronted Parrot	1	0	-	La. poicephali	contour
Poicephalus fuscicollis	Brown-necked Parrot	9	3	33.3 (9.8–67.7)	La. poicephali	contour
Poicephalus gulielmi	Red-fronted Parrot	38	7	18.4 (8.8–34.0)	La. poicephali	contour
Poicephalus meyeri	Meyer’s Parrot	48	11	22.9 (12.9–37.4)	La. poicephali	contour
Poicephalus robustus	Cape Parrot	30	7	23.3 (11.2–41.6)	La. poicephali	contour
Poicephalus rueppellii	Rüppell’s Parrot	1	0	-	La. poicephali	contour
Poicephalus rufiventris	Red-bellied Parrot	11	3	27.3 (7.9–59.6)	La. poicephali	contour
Poicephalus senegalus	Senegal Parrot	11	0	-	La. poicephali	contour
Probosciger aterrimus	Palm Cockatoo -	1	1	100 (5.0–100)	Ne. cacatui	covert
Pseudeos fuscata	Dusky Lory	16	1	6.2 (0.3–30.5)	Pi. fuscata	contour
Pseudeos fuscata	Dusky Lory	16	1	6.2 (0.3–30.5)	Ne. pseudeos	covert
Psilopsiagon aurifrons	Mountain Parakeet	1	1	100 (5.0–100)	Ra. brotogeris	contour
Psilopsiagon aymara	Gray-hooded Parakeet	2	1	50 (2.5–97.5)	Ra. brotogeris	contour
Psittacara wagleri	Scarlet-fronted Parakeet	11	1	9.1 (0.5–40.5)	Ra. brotogeris	contour
Pyrrhura lepida	Pearly Conure	1	1	100 (5.0–100)	Ra. pyrrhura	contour
Pyrrhura molinae	Green cheeked Parakeet	6	1	16.7 (0.9–58.9)	Ra. pyrrhura	contour
Pyrrhura frontalis	Maroon-bellied Parakeet	50	2	4 (0.7–13.7)	Ra. pyrrhura	contour
Pyrrhura frontalis	Maroon-bellied Parakeet	50	2	4 (0.7–13.7)	La. arini	contour
Thectocercus acuticaudatus	Blue-crowned Parakeet	24	1	4.2 (0.2–20.4)	Ra. brotogeris	contour
Touit surdus	Golden-tailed Parrotlet	4	1	25 (1.3–75.1)	La. touiti	contour
Touit batavicus	Lilac-tailed Parrotlet	8	1	12.5 (0.6–50)	Ra. trinidadi	contour
Vini peruviana	Blue Lorikeet	1	1	100 (5.0–100)	Pi. tahitiana	contour

Exa.—number of individual host species examined during study; Inf.—number of host individuals infested by quill mites; IP—prevalence index given in (%); CI—confidence interval (Sterne method); ”-“ —unknown prevalence for infested hosts.

3.3. Host-Specificity of the Quill Mites

Based on the analyzed mite material (see Table 1), we classified all syringophilids associated with parrots into the following host specificity groups:

Monoxenous parasites (28 species): Subfamily Syringophilinae: Megasyringophilus cacatua, Me. dubinini, Me. eos, Me. geoffroyus, Me. platycercus, Me. rhynchopsittae, Neoaulobia aratingae, Ne. krafti, Ne. mironovi, Ne. pseudeos, Ne. psittaculae, Ne. skorackii, Peristerophila forpi, Pe. nestoriae, Psittaciphilus fritschi, Terratosyringophilus pioni, Te. reichholfi. Subfamily Picobiinae: Lawrencipicobia ararauna, La. calyptorhyncha, La. eclectus, La. sulphurea, La. touiti, Pipicobia cyclopsitta, Pi. fuscata, Pi. tahitiana, Pi. malherbi, Rafapicobia trinidadi, Ra. xanthopterygius.

Oligoxenous parasites (8 species): Subfamily Syringophilinae: Megasyringophilus cyanocephala, Me. trichoglossus, Neoaulobia agapornis, Ne. mexicana, Psittaciphilus amazonae. Subfamily Picobiinae: Pipicobia glossopsitta, Rafapicobia pyrrhura, Lawrencipicobia poicephali.

Mesostenoxenous parasites (6 species): Subfamily Syringophilinae: Megasyringophilus kethleyi, Neoaulobia cacatui, Ne. unsoeldi, Terratosyringophilus loricinus. Subfamily Picobiinae: Lawrencipicobia arini, Rafapicobia valdiviana.

Metastenoxenous parasites (2 species): Subfamily Syringophilinae: Neoaulobia puylaerti. Subfamily Picobiinae: Rafapicobia brotogeris.

Polyxenous parasites (1 species): Subfamily Syringophilinae: Peristerophila mucuya.

3.4. Bipartite Network Analysis

Fifty one quill mite-parrot associations were observed between 24 species of quill mites and 47 species of parrots (Figure 1). The Syringophilidae–Psittaciformes antagonistic bipartite network had a high value of connectance (C = 0.89). The specialization is high (H2′ = 0.98), but with a low degree of nestedness (N = 0.033). The comparison between H2′ and null model values showed significant differences (mean for null model = 0.078; t = −8.970, p < 0.0001). The specialization on the species-level (d′) is ranged between 0.84–1 (see Table 3 and Table 4).

The prevalence, understood as the strength of the interaction between both sides, is illustrated in the graph as the thickness of the interaction between parasites and hosts. To make it easier to read the bipartite graph, each type of the quill mites genus is marked with a different color: Neoaulobia—pink, Peristerophila—green, Psittaciphilus—purple, Lawrencipicobia—yellow, Pipicobia—blue, and Rafapicobia—red (see Figure 1).

Ectoparasitic specialization (d′) to their hosts was placed into two categories:

d′ = 0.80–0.99 for 8 quill mite species: Peristerophila mucuya (0.84), Neoaulobia pseudeos (0.84), Pipicobia fuscata (0.84), Rafapicobia valdiviana (0.91), Neoaulobia unsoeldi (0.97), Lawrencipicobia arini (0.98), Rafapicobia pyrrhura (0.99), Rafapicobia brotogeris (0.99).

d′ = 1 for 16 quill mites species: Lawrencipicobia ararauna, Lawrencipicobia calyptorhyncha, Lawrencipicobia eclectus, Lawrencipicobia poicephali, Lawrencipicobia sulphurea, Lawrencipicobia touiti, Neoaulobia cacatui, Neoaulobia skorackii, Peristerophila nestoriae, Pipicobia cyclopsitta, Pipicobia glossopsitta, Pipicobia malherbi, Pipicobia tahitiana, Psittaciphilus amazonae, Rafapicobia trinidadi, Rafapicobia xanthopterygius.

The highest value is observed for sixteen quill mites species from six genera (see above: d′ = 1), whereas for three of eight quill mites species with the lowest value d′ = 0.84 (Peristerophila mucuya, Neoaulobia pseudeos, Pipicobia fuscata).

W registered high modularity (likelihood = 0.90), presenting 23 modules sorted into three types of modules: (A) single-host (one quill mite species associated with one host species), (B) multi-host (one quill mite species connected with more the one host species), and (C) multi-parasites (more than one quill mite species associated with one host species) (Figure 2).

Single-host module: (module number: 4) parasite: Neoaulobia skorackii—[host: Platycercus eximius], (5) Peristerophila mucuya—[Brotogeris versiculorus], (6) Peristerophila nestoriae—[Nestor meridionalis], (7) Psittaciphilus amazonae—[Amazona ochrocephala], (8) Lawrencipicobia ararauna—[Ara ararauna], (10) Lawrencipicobia calyptorhyncha—[Calyptorhynchus lathami], (11) Lawrencipicobia eclectus—[Eclectus roratus], (13) Lawrencipicobia sulphurea—[Cacatua sulphurea], (14) Lawrencipicobia touiti—[Touit surdus], (15) Pipicobia cyclopsitta—[Cyclopsitta diophthalma], (16) Pipicobia tahitiana—[Vini peruviana], (17) Pipicobia malherbi—[Cyanoramphus malherbi], (21) Rafapicobia trinidadi—[Touit batavicus], (23) Rafapicobia xanthopterygius—[Forpus xanthopterygius].
Multi-host module: (1) parasite Neoaulobia cacatui—[hosts: Calyptorhynchus funereus, Probosciger aterrimus], (2) Neoaulobia unsoeldi—[Amazona aestiva, Ara chloropterus], (9) Lawrencipicobia arini—[Pionites leucogaster, Pi. melanocephalus, Pyrrhura frontalis], (12) Lawrencipicobia poicephali—[Poicephalus senegalus, Po. robustus, Po. gulielmi, Po. rufiventris, Po. meyeri, Po. fuscicollis, Po. cryptoxanthus], (18) Pipicobia glossopsitta—[Parvipsitta porphyrocephala, Pa. pusilla], (19) Rafapicobia brotogeris—[Brotogeris cyanoptera, Br. chiriri, Br. jugularis, Br. versicolurus, Bolborhynchus orbygnesius, Diopsittaca nobilis, Eupsittula pertinax, Eu. aurea, Myiopsitta monachus, Pionopsitta pileata, Psilopsiagon aymara, Ps. aurifrons, Psittacara wagleri, Pyrhurra picta, Thectocercus acuticaudatus], (20) Rafapicobia pyrrhura—[Pyrrhura molinae, Py. lepida, Py. frontalis], (22) Rafapicobia valdiviana—[Enicognathus ferrugineus, Cyanoliseus patagonus].
Multi-parasite module: (3) parasites: Neoaulobia pseudeos, Pipicobia fuscata—[host: Pseudeos fuscata].

3.5. Co-Infestation of the Quill Mites

The analysis of the host spectrum and preferred habitat showed three various patterns of co-infestation (Table 5):

“Syr + Pic”—quill mite species belonging to the different Syringophilidae subfamilies and inhabiting the same host species but different habitats, i.e., members of Syringophilinae in quills of flight feathers and members of Picobiinae in quills of contour feathers.

Host: Cyanoliseus patagonus parasitized by Neoaulobia unsoeldi (subfamily: Syringophilidae; habitat: wing coverts) and by Rafapicobia valdiviana (subfamily: Picobiinae; habitat: contours);

Host: Poicephalus senegalus parasitized by Neoaulobia puylaerti (Syr; wing cov.) + Lawrencipicobia poicephali (Pic; con.);

Host: Pseudeos fuscata parasitized by Neoaulobia pseudeos (Syr; wing cov.) + Pipicobia fuscata (Pic; con.);

Host: Psilopsiagon aymara parasitized by Peristerophila mucuya (Syr; wing cov.) + Rafapicobia brotogeris (Pic; con.).

B.: “Syr + Syr + Pic”—another, more extensive above mentioned variant of co-infestation was observed when one host species was infested by two species of the subfamily Syringophilinae occupying flight feathers, but restricted to coverts or secondaries, and by the species of Picobiinae found in quills of contour feathers.

Host: Brotogeris versicolurus parasitized by Megasyringophilus kethleyi (Syr; sec.) + Peristerophila mucuya (Syr; wing cov.) + Rafapicobia brotogeris (Pic; con.);

Host: Eupsitulla pertinax parasitized by Megasyringophilus kethleyi (Syr; sec.) + Neoaulobia mexicana (Syr; wing cov.) + Rafapicobia brotogeris (Pic; con.).

C.: “Syr + Syr”—this configuration only includes representatives of the subfamily Syringophilinae which were found in the different habitats of the flight feathers on the same host species.

Host: Amazona aestiva parasitized by Neoaulobia unsoeldi (Syr; wing cov.) + Psittaciphilus amazonae (Syr; tail cov.);

Host: Aratinga yandaya parasitized by Megasyringophilus kethleyi (Syr; sec.) + Neoaulobia aratinga (Syr; wing cov.);

Host: Eupsitulla canicularis parasitized by Megasyringophilus kethleyi (Syr; sec.) + Neoaulobia mexicana (Syr; wing cov.);

Host: Platycercus eximius parasitized by Megasyringophilus platycercus (Syr; sec.) + Neoaulobia skorackii (Syr; wing cov.).

D.: “Pic + Pic”—this configuration includes different quill mites species belonging to the subfamily Picobiinae, and inhabiting the same niche on the same host species.

Host: Pyrrhura frontalis parasitized by Lawrencipicobia arini (Pic; con.) + Rafapicobia pyrrhura (Pic; con.).

Table 5. Host species infested by two or more syringophilid species with the notation of the habitat preference.

Hosts	Quill Mites	Subfamily	Habitat
Amazona aestiva	Neoaulobia unsoeldi	S	w.cov.
Amazona aestiva	Psittaciphilus amazonae	S	t.cov.
Aratinga yandaya	Megasyringophilus kethleyi	S	sec.
Aratinga yandaya	Neoaulobia aratinga	S	w.cov.
Brotogeris versiculorus	Megasyringophilus kethleyi	S	sec.
	Peristerophila mucuya	S	w.cov.
	Rafapicobia brotogeris	P	con.
Cyanoliseus patagonus	Neoaulobia unsoeldi	S	w.cov.
Cyanoliseus patagonus	Rafapicobia valdiviana	P	con.
Eupsitulla canicularis	Megasyringophilus kethleyi	S	sec.
Eupsitulla canicularis	Neoaulobia mexicana	S	w.cov.
Eupsitulla pertinax	Megasyringophilus kethleyi	S	sec.
	Neoaulobia mexicana	S	w.cov.
	Rafapicobia brotogeris	P	con.
Platycercus eximius	Megasyringophilus platycercus	S	sec.
Platycercus eximius	Neoaulobia skorackii	S	w.cov.
Poicephalus senegalus	Neoaulobia puylaerti	S	w.cov.
Poicephalus senegalus	Lawrencipicobia poicephali	P	con.
Pseudeos fuscata	Neoaulobia pseudeos	S	w.cov.
Pseudeos fuscata	Pipicobia fuscata	P	con.
Psilopsiagon aymara	Peristerophila mucuya	S	w.cov.
Psilopsiagon aymara	Rafapicobia brotogeris	P	con.
Psittacula cyanocehala	Megasyringophilus cyanocephala	S	sec.
Psittacula cyanocehala	Neoaulobia psittaculae	S	w.cov.
Pyhrrura frontalis	Lawrencipicobia arini	P	con.
Pyhrrura frontalis	Rafapicobia pyrhurra	P	con.

P—Picobiinae; S—Syringophilinae; con.—contour feathers; w.cov.—wing coverts; t.cov.—tail coverts; sec.—secondaries.

3.6. Zoological Distribution of Quill Mites Species Associated with Parrots

Data presented in Table 1, indicate that syringophilid mites associated with parrots are present in the following zoogeographical regions: Neotropical, Nearctic, Panamanian, Afrotropical, Oriental, Australasian, and Oceanian (Table 6).

In the particular regions, we noted the following genera with the number of quill mites species:

Neotropical: Megasyringophilus (4), Neoaulobia (3), Peristerophila (1), Psittaciphilus (2), Terratosyringophilus (1), Lawrencipicobia (3), Rafapicobia (5);
Nearctic: Megasyringophilus (2), Neoaulobia (2), Peristerophila (1), Terratosyringophilus (1);
Panamanian: Neoaulobia (1), Rafapicobia (1);
Afrotropical: Neoaulobia (2), Lawrencipicobia (1);
Oriental: Megasyringophilus (4), Neoaulobia (2), Peristerophila (1); Terratosyringophilus (1), Lawrencipicobia (1);
Oceanian: Megasyringophilus (2), Neoaulobia (2), Terratosyringophilus (1), Lawrencipicobia (1), Pipicobia (3);
Australasian: Megasyringophilus (3), Neoaulobia (3), Peristerophila (1), Lawrencipicobia (1), Pipicobia (2).

Among all 45 quill mites species associated with parrots, 37 of them were noted only from one zoogeographical region:

Nearctic: Megasyringophilus rhynchopsittae, Neoaulobia mironovi, Peristerophila forpi, Terratosyringophilus pioni;
Neotropical: Neoaulobia aratingae, Psittaciphilus amazonae, Ps. fritschi, Lawrencipicobia ararauna, La. arini, La. touiti, Rafapicobia pyrrhura, Ra. trinidadi, Ra. valdiviana, Ra. xanthopterygius;
Afrotropical: Neoaulobia agapronis, Lawrencipicobia poicephali;
Australasian: Megasyringophilus cacatua, Me. platycercus, Neoaulobia krafti, Ne. skorackii, Peristerophila nestoriae, Lawrencipicobia calyptorhyncha, Pipicobia malherbi, Pi. glossopsitta;
Oriental: Megasyringophilus cynaocephala, Me. dubinini, Me. eos, Neoaulobia psittaculae, Terratosyringophilus loricinus, Lawrencipicobia sulphurea;
Oceanian: Megasyringophilus geoffroyus, Neoaulobia pseudeos, Terratosyringophilus reichlofi, Lawrencipicobia eclectus, Pipicobia cyclopsitta, Pi. fuscata, Pi. tahitiana.

Eight quill mite species were recorded from more than one zoogeographical region:

Oriental + Afrtotropical: Neoaulobia puylaerti;
Neotropical + Panamanian: Neoaulobia unsoeldi, Rafapicobia brotogeris;
Neotropical + Nearctic: Megasyringophilus kethleyi, Neoaulobia mexicana;
Neotropical + Oriental: Peristerophila mucuya;
Oceanian + Australasian: Neoaulobia cacatui;
Oriental + Oceanian + Australasian: Megasyringophilus trichoglossus.

3.7. Phylogenetic Relationship of the Genera Associated with Parrots

The analysis under equal weights resulted in one most parsimonious tree (MPT) shown in Figure 3. Number of characters—56 (Figures S1 and S2), number of parsimony informative characters—46, tree length (L) = 69, consistency index (CI) = 0.841, retention index (RI) = 0.861, rescaled consistency index (RC) = 0.724, homoplasy index (HI) = 0.259.

4. Discussion

4.1. Species Richness and Phylogenetic Relationship of Quill Mites Associated with Psittaciformes Birds

Despite intensive taxonomic research provided on quill mites in recent years, our knowledge of the extent ofSyringophilidae biodiversity is still far from satisfactory. Currently, more than 400 species and 63 genera of these mites have been described from about 670 bird species belonging to 27 orders of birds [14]. However, these numbers show that the actual species richness of syringophilids is only a small part of their taxonomical diversity because the broad spectrum of the avian hosts is still largely unexplored. In addition, most taxonomic studies were conducted on mite species collected from randomly selected (or found) birds and, with few exceptions, did not focus on detailed studies of the syringophilid fauna associated with particular groups of birds. These exceptions are, for example, research on quill mite fauna associated with birds of the genus Estrilda [31], family Nectariniidae [29], Cuculidae [28], Cacatuidae [50], Psittaculidae [52], Psittacidae [53], or recently studied avian order Columbiformes [30].

The fauna of quill mites related to parrots comprises 45 species belonging to five genera, Megasyringophilus, Neoaulobia, Psittaciphilus, Peristerophila, and Terratosyringophilus representing the subfamily Syringophilinae and three genera, Lawrencipicobia, Pipicobia, and Rafapicobia, representing subfamily Picobiinae (see Table 1; Figure 3, Figure 4 and Figure 5).

The genera Megasyringophilus and Neoaulobia comprise large and medium-sized syringophilids occupying quills of wing feathers and represent basal lineages to all remaining syringophilid genera involved in the analysis (Figure 3). These genera are common on all parrot families except the family Strigopidae, suggesting that these genera were already present in a common ancestor before the split of the main phylogenetic lines of parrots, i.e., Psittacoidea and Cacatoidea in the Eocene (about 59 mya). It is worth noting that the absence of Neoaulobia and Megasyringophilus on the small group (only four species) of New Zealand parrots (Strigopidae) can be a result of the too-small sample of examined birds of this family. In the present study, we examined only four specimens of Nestor meridionalis (see Table 2), and we cannot exclude that future research on quill mites associated with strigopids bring records of these mite genera also on birds of the family Strigopidae.

In contrast to Neoaulobia, which host distribution is restricted exclusively to Psittaciformes, the representatives of Megasyringophilus, except parrots, were also recorded on raptor birds, i.e., Megasyringophilus dalmas Skoracki & Unsoeld, 2016 collected from a representative of owls, Megascops choliba (Strigidae) from Venezuela and M. aquilus Skoracki et al., 2010 from accipitrids (Accipitridae) of the genera Aquila, Accipiter, Buteo, Clanga, and Hieraaetus [78,80] (Figure 4). The presence of this genus on phylogenetically not closely related avian orders, Psittaciformes, Strigiformes, and Accipitriformes, is probably an example of the horizontal transfers (host switch) between prey and predator. In the literature, there are two similar examples of the exchange of quill mite fauna between predator and prey, i.e., the mite species Syringophilopsis kirgizorum Bochkov et al. found on finches of the genus Carduelis (Passeriformes: Fringillidae) but also found on the Tawny Owl Strix aluco Linnaeus (Strigidae) [105], and the mite Peristerophila columbae Casto known from the domestic pigeon Columba livia, but also recorded on the Red-tailed Hawk Buteo jamaicensis (Accipitriformes: Accipitridae) [106].

The following three syringophiline genera associated with parrots form phylogenetically closely related lineages Psittaciphilus + (Peristerophila + Terratosyringophilus) (Figure 3). This monophyletic clade is also known as Psittaciphilus-generic-group assigned by Bochkov & Perez [75]. The species of these genera are found inside the quills of wing coverts (Peristerophila, Terratosyringophilus) or tail coverts (Psittaciphilus). The genera Terratosyringophilus (five species) and Psittaciphilus (four species), except parrots, share their species also with pigeons and doves (Columbiformes). In contrast, Peristerophila (currently comprising 14 species) is associated, excepting parrots and columbiform birds, also with raptors Accipitriformes and Falconiformes, and the other two non-passerine avian orders, i.e., Bucerotiformes, and Coraciiformes (Figure 4). The presence of representatives of Terratosyringophilus and Psittaciphilus on parrots and pigeons is problematic, because recent molecular studies indicate that these two avian clades are phylogenetically not closely related; Psittaciformes belongs to the clade Australaves, whereas Columbiformes to distant Columbaves [38,39,107]. Similarly, a broad host spectrum of Peristerophila, represented by not related avian orders, suggests factors other than co-evolutionary processes.

The Psittaciformes-related picobiine genera Lawrenicipicobia, Pipicobia, and Rafapicobia, belong to the monophyletic Neopicobia-generic-group in the subfamily Picobiinae [22]. Among representatives of this clade, the genus Lawrencipicobia, the sister clade to the other two genera, is exclusively associated with parrots and is present on all parrot families except Strigopidae (Figure 5). On the other hand, the genus Pipicobia infests only old world parrots (Psittaculidae), but is also recorded on passerines (Passeriformes) which are phylogenetically closely related to Psittaciformes (both orders belong to the Australaves clade) [38]. The Rafapicobia species associated with parrots are limited only to the Neotropical psittacines, but this genus is also known from closely related passerines (Passeriformes). Additionally, Rafapicobia was also noted on hosts from the orders Coraciiformes and Piciformes, which belong to the sister clade Coraciimorphae [38,98]. The host spectrum comprising four closely related avian orders (Psittaciformes + Passeriformes + Piciformes + Coraciiformes—all of them belong to the Telluraves, core landbirds [40]) suggests co-evolutionary events, but surprisingly, this genus was recently also recorded on several hosts of the distant order Gruiformes [98] which indicates that also horizontal transfers took place in this parasite-host system. In conclusion, the quill mites-parrots system is a composition of the co-evolutionary processes that undoubtedly take place, e.g., in genera exclusively associated with parrots—Neoaulobia, Lawrencipicobia, as well as horizontal transmission to unrelated hosts clades, e.g., genera Megasyringophilus, Rafapicobia.

4.2. Species Richness and Phylogenetic Relationship of Quill Mites Associated with Psittaciformes Birds

Although the quill mite fauna includes genera found on unrelated host groups (see above), at the species level, most syringophilid species are restricted to one host species (monoxenous parasites; 63%). The species associated with phylogenetically closely related host species belonging to the same genus (oligoxenous parasites; 18%) or family (mesostenoxenous parasites; 17%) are a minority. The marginal part of the syringophilid fauna associated with parrots are the species infesting more or less but not closely related host species (metastenoxenous parasites; 1% or polixenous parasites; 1%) (Table 7). The proportion of monoxenous quill mite species in relation to the rest is not unique to the fauna associated with parrots. A similar ratio is typical for all other genera of the family Syringophilidae, which is evidence of a long-term and close relationship with their hosts [12,30,36]. Additionally, except for horizontal transmission, we cannot exclude that Neoaulobia puylaerti and Peristerophila mucuya, which are metastenoxenous and polixenous parasites, respectively, are, in fact, represented by cryptic species. Although we do not yet have evidence of this, future molecular research will clear up the doubts on this topic.

4.3. Quill Mites and Their Habitat-Specificity

Feathers and their various types are interesting examples of a living environment for many parasitic and commensal species that can coexist in such a habitat. J.B. Kethley was the first to give (but without exact examples) a short note that “adaptations restrict mites to specific conditions so that some genera are limited to specific feather tracts” and, consequently, one host species can by parasitized by three or even four different genera occupying different habitats (types of feathers) [9]. Later on, Schmäschke et al. [108] observed the co-infestation of two species, Syringophilopsis turdi and Syringophiloidus sp., on Fieldfare Turdus pilaris (Passeriformes: Turdidae), as well as Syringophilopsis kirgizorum and Syringophiloidus sp. found on European greenfinch Chloris chloris (Passeriformes: Fringillidae). In the paper of Skoracki et al. [109], the authors showed not only different patterns of observed co-infestation, but they noted also the niches occupied by quill mites, e.g., Syringophilipsis kirgizorum (primaries) + Torotrogla gaudi (secondaries) on Chaffinch Fringilla coelebs (Fringillidae); Syringophiloidus presentlis (secondaries) + Picobia sturni and Aulonastus buczekae (contour feathers) on Common Starling Sturnus vulgaris (Sturnidae).

Until recently, the multi-infestations by quill mites have been observed only in passeriform birds. However, interesting results on habitat specificity were also obtained by Kaszewska-Gilas et al., who observed several cases of the multi-infestation on columbiform birds [30]. The authors distinguish two patterns of the multi-infestations, i.e., “Syr-Pic pattern”, where the quill mites belonging to two subfamilies Syringophilinae and Picobiinae occupy the same host species or individual; and “Syr-Syr pattern”, where the quill mites belong to the same subfamily, Syringophilinae and are present on the same host species.

In our study, we found 12 examples of multi-infestation in three different patterns: Syr-Pic, Syr-Syr, and, for the first time, Pic-Pic, where both components belong to the same subfamily, Picobiinae, and are recorded from the same host species or individual.

In the first Syr-Pic configuration, members of Syringophilinae inhabit mainly quills of secondaries, wing or tail coverts, and rectrices (Table 2 and Table 5), while representatives of Picobiinae exclusively inhabit contour feathers. However, within the Syr-Pic group, we distinguished two variants. The first one is when one host species is infested by two quill mite species that occupy different types of feathers, e.g., Neoaulobia unsoeldi (covert) + Rafapicobia valdiviana (contour) on Burrowing Parrot Cyanoliseus patagonus; Neoaulobia puylaerti (covert) + Lawrencipicobia poicephali (contour) on Senegal Parrot Poicephalus senegalus; Neoaulobia pseudeos (covert) + Pipicobia fuscata (contour) on Dusky Lory Pseudeos fuscata; Peristerophila mucuya (covert) + Rafapicobia brotogeris (contour) on Grey-hooded Parakeet Psilopsiagon aymara. The second one is more diverse, and comprises two different species of the subfamily Syringophilinae and a representative of the subfamily Picobiinae on the same host. This configuration was observed, e.g., Megasyringophilus kethleyi (secondary) + Peristerophila mucuya (covert) + Rafapicobia brotogeris (contour) from White-winged Parakeet Brotogeris versicolurus; Megasyringophilus kethleyi (secondary) + Neoaulobia mexicana (covert) + Rafapicobia brotogeris (contour) from Brown-throated Parakeet Eupsitulla pertinax.

For Syr-Syr pattern, in all four observed cases, representatives of the subfamily infested the same host, but also with the restriction to the different types of feathers, e.g., Neoaulobia unsoeldi (wing covert) + Psittaciphilus amazonae (tail covert) on Turquoise-fronted Amazon Amazona aestiva.

For Pic-Pic pattern, we found only one case, when two quill mites species, Lawrencipicobia arini and Rafapicobia pyrrhura, infested the same host species and occupied the same type of habitat—quills of contour feathers.

Generally, various species of quill mites avoid occurrence in the same niche, because niche separation is one of the parts of natural selection. Thanks to this, the competing species try using different hosts or microhabitats [110]. This happens because the competition for the same resources, understood as occupying the same niche and using the same resources, ends when one competitor displaces the other and, thus, leads to his extinction [111,112,113]. The phenomenon of separation of the niche is common and well-documented among many ectoparasitic mites, but these relationships remain poorly studied among Syringophilidae. Our results confirm that the family Syringophilidae is characterized by a high degree of specificity to occupy a niche as it was previously postulated [9,30,108,109,114]. Kethley & Johnston [115], Casto [11], Grossi & Proctor [25], Skoracki et al. [27] postulated that the habitat specificity is also a result of the preference of quill mites to the specific parameters of the quills—their volume and quill-wall thickness. It should also be noted, however, habitat represented by contour feathers comprises more or less morphologically uniform feathers; the particular sectors of the contour plumage do not have to be infected by syringophilids with the same frequency, and, in fact, mites choose a specific place on the host body, e.g., the feathers on the belly are more often infested than the feathers on the neck or back.

4.4. Prevalence

The prevalence index (IP) provides information about the strength of the relationship between a given host species and the parasite. A crucial role in determining the prevalence of infested hosts in the environment is the number of examined bird individuals and the number of examined feathers [25,27]. The previous studies on the distribution of the quill mites on their hosts showed that the highest values of prevalence are for birds kept in crowded conditions, e.g., 75% for domestic hens Gallus gallus domesticus (N = 1500) [116] and 82% (N = 492) for house sparrows Passer domesticus [117]. When analyzing farm birds or highly gregarious hosts, these high prevalence values are understandable. However, the prevalence for wild and non-social birds is much lower and rarely exceeds 45%, e.g., 7.3% for the rock ptarmigans Lagopus muta (N = 1209) [24]; 7.3% for the boreal owls Aegolius funereus (N = 55) [27]; 3.5% for the great grey shrike Lanius excubitor (N = 508) [118]; 42.9% for the ovenbirds Seiurus aurocapilla (N = 21) [25].

The only analysis of the infestation of parrots was carried out by Jardim et al. [119]. Their research was mainly concerned with parrots held captive in Brazil. During this study, authors examined 30 species of New World parrots and syringophilid mites were found on three of them, i.e., Aratinga aurea (IP = 9.1%; N = 11), Brotogeris chirri (IP = 7.7%; N = 13), and Pionopsitta pilleata (IP = 20%; N = 5).

In our study, most of the host species belong to the first group, for which the prevalence is low and not exceeds 25%, e.g., 2.8% for Eupsitulla aurea (N=36), 3% for Forpus xanthopterygius (N = 33), 4% for Amazona aestiva (N = 25), 4% for Pyrrhura frontalis (N = 50), 4.8% Brotogeris versicolurus (N = 42) (see Table 2). To this group also belong parrots with evident higher prevalence, e.g., birds of the genus Poicephalus—18.4% for P. gulielmi (N = 38); 22.9% for P. meyeri (N = 48), or 23.3% for P. robustus (N = 30). The second group of hosts, where IP is medium (26–50%), includes 11 host species, whereas none of them belong to the group of hosts with high IP (51–75%). However, in our material there are parrots with IP = 100% (eight species), but these results are affected by the small sample size of study specimens.

The studies on the infestation of the host populations were provided on bird material originated from various sources: (i) from the ornithological collection (dry bird skins, frozen or alcohol preserved specimens) deposited in the museum or other scientific institutions [26,27,29,30,31,114,120]; (ii) from birds examined during fieldworks [24,109,113,114], and (iii) from birds kept in the zoological gardens [119] or farms [23,116,121,122]. Considering that not every feather on the host is infected (see [25,27]), it is important that the analyzed host sample, apart from the sufficiently large number of tested specimens, also includes the largest possible number of examined feathers, or all, if we want to know the border of the habitat. Of course, the second condition is impossible to realize during research on museum and live bird material. In estimating the prevalence, the age and sex of the tested hosts and the sampling season are also important. We are aware that our results are estimates that show, at least approximately, the degree of the infestation of the host population. However, this does not change the fact that it is worthwhile to investigate further the strength of the relationships mentioned in the prevalence index and simultaneously continue research toward the study of habitat specificity.

4.5. Analyses of the Bipartite Network of Quill Mite–Parrots Communities

The bipartite network and some indices, such as nestedness, connectance, etc., are part of an ecological approach which provides interesting information about biological systems, i.e., host-parasite relationships for communities of quill mites and birds. Networks are good tools for illustrating and describing the interactions inside of various types of communities, their relationships, and ecological connections [7]. Although for many years this type of research has mainly focused on mutualistic relationships at the plant-animal level, such as pollinators, seed spreading, and others [57,123,124,125], we can use this type of analysis to study parasite-host relationships. The bipartite analyses are read as a graph that illustrates links between two trophic levels, but, above all, quantify indices such as host specificity in parasites and provide a topological description [8,123].

Until now, analyses at the level of host-parasite were conducted for relationships among quill mites and sunbirds (Passeriformes: Nectariniidae) [29], estrildids (Passeriformes: Estrildidae) [31], and pigeons and doves (Columbiformes: Columbidae) [30,32].

Our investigation was intended to determine binary indices such as: network specialization (H2′), nestedness (N), modularity (Q), species specialization metrics (d’ index), and connectance (C). Each of these indices provides the following information: the number of interactions, the level of sharing partners, the degree of compartmentalization of the networks, and network-level specialization [58,126,127].

The indicators used in our research (i.e., nestedness, modularity, and connectance) allow a better understanding of the relationships occurring between species in the network, which are correlated and depend on each other, which has been shown in previous studies provided by Fortuna et al. [63], Pavlopoulos et al. [62] and Olesen et al. [128].

Connectance illustrates a relationship between parasitic species and individual hosts. A high index means non-random infestation and a stable community. This has been proven, e.g., by Devictor’s analyses concerned with the conservation and protection of biodiversity demonstrate that high C-value is characteristic for more stable communities, while low C-value can be an indicator of an ecological threat [129]. Moreover, when the network loses or gains generalists, the value of the connectance may decrease [129,130]. A high value of the connectance indicator was observed in many other networks, i.e., food webs, plant–herbivores–parasitoids in the forest or plant–pollinator [131,132,133].

Nestedness is one of the most important indicators, and values higher and closer to 1 means that the structure of the studied network is non-random, more diverse, and complex [61]. Nestedness interacts with modularity [128], and their correlation depends on network connectance [63]. On the other hand, a trend towards the ecological network to divided into modules is known as modularity [63]. Delmas et al. [134] indicate that the modules should be stable, thanks to which the organisms within them have a limited ability to spread beyond their structure. Modularity interacts with nestedness [128] and their correlation depends on network connectance [63]. Moreover, Fortuna et al. showed that the complex dependence between nestedness and modularity has clear potential to temper or augment the different connotation of the two patterns [63].

Our results confirm that there is a high specialization between syringophilid mites and parrots, on both the network- and the species-level. Our network pattern is characterized by a high values of: connectance (C = 0.89), H2′ (H2′ = 0.98), and modularity (Q = 0.90) with 23 modules. Specialization on the species-level (d′) is also high and ranged between 0.84–1. By contrast to these, the value of nestedness index is low (N = 0.033).

The connectance, modularity, and network specialization results were similar to those obtained by Kaszewska-Gilas et al. [30] in a study of syringophilids and doves and pigeons as well as ectoparasitic flies of the family Streblidae (Hippoboscoidea) and bat hosts from the tropical dry forest [125]. The values of examined features have the following qualities for:

Network specialization (H2′) = 0.98 (in our study), (H2′) = 0.93 (in quill mites-columbid birds network [30]), and (H2′) = (in Hippoboscoidea-bats network [125]);
Conncetance (C) = 0.89 (in our study), (C) = 0.90 (in quill mites-columbid birds network [30]), and (C) = 0.30 (in Hippoboscoidea-bats network [125]);
Modularity (Q) = 0.90 (in our study), (Q) = 0.83 (quill mites-columbid birds network [30]), (Q) = 0.7 (in Hippoboscoidea-bats network [125]);
Nestedness (N) = 0.033 (in our study), (N) = 0.908 (in quill mites-columbid birds network [30]), but in the study of Duran et al. the nesttednes has not been examined [125].

The high similarity C-index of the ecological network of quill mites and columbids and psittacids, as opposed to flies-bats value (C)=0.30, can be related to sampled and net-work size—the syringophilds and their bird hosts were more numerous. In the quill mites–parrots and quill mites–doves networks, the proportion of specialized species is comparably high, and much higher than in the bat–fly network. As in the case of Kaszewska-Gilas et al. [30] and their networks of quill mites-doves with a high C-index value, we also hypothesize that the higher the index of C-value is observed, the hosts-parasites systems are older and more stable.

Our network has a high value of modularity (Q = 0.90) and consists of 23 modules. Within these modules there were three types of elements: single-host, multi-host, multi-parasite modules. The most common adjustment is single-host item. Thus, a strong interaction with the host species was observed for 14 single-host modules. The next seven modules were multi-host; among them module number “19” has the highest number of hosts. Only one of them was a multi-parasite module (see module number “3” with Neoaulobia pseudeos and Pipicobia fuscata related to Pseudeos fuscata). This multi-parasite community contains two species from the genera: Neoualobia (Syringophilinae) and Pipicobia (Picobiinae), which interact with one host species. Although Neoaulobia and Pipicobia are not the sister caldes and represent two subfamilies of Syringophilidae, their coexistence on one host species—the Dusky lory Pseudeos fuscata from the Australian region, which was a center of diversity and diversification of parrots during the Gondwanaland rifting [35,36,37], could be a result of the phylogenetic relationship between particular quill mites and their hosts.

According to research of Bascompte et al., a higher nestedness index determines the complexity of the network [63], which was confirmed in the quill mites-columbid birds relationships (N = 0.908) [30], our study shows that nestedness index between Syringophilidae and parrots is very low (N) = 0.033.

Although nestedness and modularity are correlated, Fortuna et al. also observed that the most highly connected communities inclined to demonstrate only one of these two properties [63]. This trend seems to be observed in our study. The bipartite network associated with Syrongophilidae and Psittaciformes favored modularity, with a high value in contrast to a very low amount of nestedness.

5. Conclusions

Before we began the current research, the number of fauna from Syringophilidae associated with parrots was 26 species. We examined the feathers of 1524 parrot specimens belonging to 195 species and our analysis was concerned with 50% of all known species of parrots distributed in the Australian, Afrotropical, Neotropical, Oriental and Oceanian regions. After completing the study and analyzing all available acarological material, this fauna contained 45 species of quill mites belonging to 8 syringophilid genera, infesting 81 parrot species. A full key to the identification of all currently known species and genera of quill mites occurring on parrots are also a part of this publication.

Mites of the subfamily Syringophilinae are found on parrots of the families: Strigopidae, Cacatuiae, Psittaculidae, and Psittacidae. In contrast, species of the subfamily Picobiinae infested representatives of the families Cacatuidae, Psittaculidae, and Psittacidae. They still have not been seen from the from Strigopidae family. Parrot-associated Syringophilidae mites, similar to the whole family, are highly host-specific. They are mainly monoxenous (63%) and mesostenoxenous (18%) parasites, as well as mesostenoxenous (15%), metastenoxenous (2%) and polixenous (2%) parasites. The analysis of the host spectrum and preferred habitat showed three various patterns of co-infestation. The prevalence of host infestations by syringophilid mites varied from 2.8% to 100% (95% confidence interval (CI Sterne method) = 0.1–100).

The zoogeographical distribution of quill mites coincides with the distribution of their hosts, and suggest a high level of endemism both of individual parrot and syringophilid species. The greatest species richness of Syringophilidae is found in the Austrolasian (center of biodiversity of the families: Cacatuidae and Psittaculidae) and Neotropical (center of biodiversity of the family Psittacidae) regions.

The Syringophilidae-Psittaciformes bipartite network was composed of 24 mite species and 47 host species. The bipartite network was characterized by a high network level specialization H2′ = 0.98, connectance C = 0.89, and high modularity Q = 0.90, with 23 modules, but low nestedness N = 0.0333.

The analysis of phylogeny of the quill mites on the generic level shows two distinct clades: Psittaciphilus (Peristerophila + Terratosyringophilus) (among Syringophilinae subfamily) and Lawrencipicobia (Pipicobia + Rafapicobia) (among Picobiinae).

Our results are interesting and certainly give deeper insight into the relationship between Syringophilidae mites and parrots. As syringophilid mites form a sizable part of the parasite world, the results of the described research will significantly contribute to the basic knowledge of parasitology, biogeography, phylogeny, and evolution of parasites and their hosts. In the future, these results may also be used by epidemiologists and bird conservation organizations in their research. Someday, perhaps they will help ornithologists to finalize the family tree of birds.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/d15010001/s1, Figure S1: Characters; Figure S2: A data matrix; Table S1: The degree of Syringophilidae examination for each Psittaciformes family.

Author Contributions

Conceptualization, N.M.-M.; methodology, N.M.-M., M.S., J.Z.K., M.U. and B.S.; investigation, N.M.-M., M.S., J.Z.K., M.U. and B.S.; data curation, N.M.-M.; formal analysis, N.M.-M., M.S., J.Z.K. and B.S.; writing—original draft preparation, N.M.-M.; writing—review and editing, N.M.-M., M.S. and B.S.; supervision, N.M.-M., M.S. and B.S.; project administration, N.M.-M.; funding acquisition, N.M.-M. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by POWR.03.02.00-00-I006/17 and by Dean of Faculty Biology, Adam Mickiewicz University.

Institutional Review Board Statement

Not applicable.

Data Availability Statement

Data is available upon request from the corresponding authors.

Acknowledgments

We thank Stefan Friedrich and Roland Melzer (SNSB-ZSM—Arthropoda Varia) for their help during our studies in the Bavarian State Collection of Zoology. We also thank anonymous reviewers for their critical review of the manuscript.

Conflicts of Interest

The authors declare no conflict of interest. The funders had no role in the design of the study; in the collection, analyses, or in the decision to publish the results.

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Figure 1. Bipartite network graph of interactions between quill mite species (left) and their parrot hosts (right).

Figure 2. Modules of the quill mites–parrot communities. Modules 1–23, generated for quill mites species and parrots. The intensity of the colors of the squares indicates the strength of the interaction between particular parasite species (vertical axis) and their host species (horizontal axis).

Figure 3. Phylogenetic tree of the syringophilid genera associated with parrots.

Figure 4. Host association of the species in the particular genera of the subfamily Syringophilinae recorded from parrots.

Figure 5. Host association of the species in the particular genera of the subfamily Picobiinae recorded from parrots.

Table 3. Host specificity of quill mite species of the subfamily Syringophilinae with the value of d’ index.

Specificity	d′	Quill Mites	Hosts Spectrum
Monoxenous	-	Megasyringophilus cacatua	Cacatua galerita
	-	Megasyringophilus dubinini	Trichoglossus ornatus
	-	Megasyringophilus eos	Eos bornea
	-	Megasyringophilus geoffroyus	Geoffroyus geoffroyi
	-	Megasyringophilus platycercus	Platycercus eximius
	-	Megasyringophilus rhynchopsittae	Rhynchopsitta pachyrhyncha
	-	Neoaulobia aratingae	Aratinga jandaya
	-	Neoaulobia krafti	Cacatua tenuirostris
	-	Neoaulobia mironovi	Amazona finschi
	0.84	Neoaulobia pseudeos	Pseudeos fuscata
	-	Neoaulobia psittaculae	Psittacula cyanocephala
	1	Neoaulobia skorackii	Platycercus eximius
	-	Peristerophila forpi	Forpus cyanopygius
	1	Peristerophila nestoriae	Nestor meridionalis
	-	Psittaciphilus fritschi	unidentified parrot
	-	Terratosyringophilus pioni	Pionus senilis
	-	Terratosyringophilus reichholfi	Lorius lory
Oligoxenous	-	Megasyringophilus cyanocephala	Psittacula cyanocephala
	-		Psittacula eupatria
	-		Psittacula krameri
	-	Megasyringophilus trichoglossus	Trichoglossus sp.
	-		Trichoglossus euteles
	-		Trichoglossus chlorolepidotus
	-	Neoaulobia agapornis	Agapornis nigrigenis
	-		Agapornis fischeri
	-		Agapornis personatus
	-		Agapornis roseicollis
	-		Agapornis taranta
	-	Neoaulobia mexicana	Eupsittula canicularis
	-	Neoaulobia mexicana	Eupsittula pertinax
	-	Psittaciphilus amazonae	Amazona aestiva
	-		Amazona amazonica
	1		Amazona ochrocephala
Mesostenoxenous	-	Megasyringophilus kethleyi	Aratinga jandaya
	-		Brotogeris versicolurus
	-		Eupsitulla canicularis
	-		Eupsittula pertinax
	1	Neoaulobia cacatui	Calyptorhynchus funereus
	1	Neoaulobia cacatui	Probosciger aterrimus
	0.97	Neoaulobia unsoeldi	Amazona aestiva
			Ara chloropterus
			Cyanoliseus patagonus
	-	Terratosyringophilus loricinus	Lorius garrulous
	-	Terratosyringophilus loricinus	Trichoglossus haematodus
Polixenous	-	Neoaulobia puylaerti	Loriculus philippensis
	-		Loriculus pusillus
	-		Poicephalus senegalus
	0.84	Peristerophila mucuya	Brotogeris versicolurus
	-		Psilopsiagon aymara
	-		Trichoglossus haematodus
	-		Columbina minuta *
	-		Columbina passerine *
	-		Columbina squammata *
	-		Columbina talpacoti *
	-		Metriopelia ceciliae *
	-		Metriopelia melanoptera
	-		Streptopelia decaocto *

d′—index measured specialization at species level; *—hosts species belonging to order Columbiformes.

Table 4. Host specificity of quill mite species the subfamily Picobiinae with the value of d′ index.

Specificity	d′	Quill Mites	Hosts Spectrum
Monoxenous	1	Lawrencipicobia ararauna	Ara ararauna
	1	Lawrencipicobia calyptorhyncha	Calyptorhynchus lathami
	1	Lawrencipicobia eclectus	Eclectus roratus
	1	Lawrencipicobia sulphurea	Cacatua sulphurea
	1	Lawrencipicobia touiti	Touit surdus
	1	Pipicobia cyclopsitta	Cyclopsitta diophthalma
	0.84	Pipicobia fuscata	Pseudeos fuscata
	1	Pipicobia tahitiana	Vini peruviana
	1	Pipicobia malherbi	Cyanoramphus malherbi
	1	Rafapicobia trinidadi	Touit batavicus
	1	Rafapicobia xanthopterygius	Forpus xanthopterygius
Oligoxenous	1	Pipicobia glossopsitta	Parvipsitta porphyrocephala
	1	Pipicobia glossopsitta	Parvipsitta pusilla
	0.99	Rafapicobia pyrrhura	Pyrrhura molinae
			Pyrrhura lepida
			Pyrrhura frontalis
	1	Lawrencipicobia poicephali	Poicephalus senegalus versteri
			Poicephalus robustus
			Poicephalus gulielmi
			Poicephalus rufiventri
			Poicephalus meyeri
			Poicephalus fuscicollis
			Poicephalus cryptoxanthus
Mesostenoxenous	0.98	Lawrencipicobia arini	Pionites leucogaster
			Pionites melanocephalus
			Pyrrhura frontalis
	0.91	Rafapicobia valdiviana	Enicognathus ferrugineus
	0.91	Rafapicobia valdiviana	Cyanoliseus patagonus
	0.99	Rafapicobia brotogeris	Brotogeris cyanoptera
			Brotogeris chiriri
			Brotogeris jugularis
			Brotogeris versicolurus
			Bolborhynchus orbygnesius
			Diopsittaca nobilis
			Eupsittula pertinax
			Eupsittula aurea
			Myiopsitta monachus
			Pionopsitta pileata
			Psilopsiagon aymara
			Psilopsiagon aurifrons
			Psittacara wagleri
			Pyrhurra picta
			Thectocercus acuticaudatus

d′—index measured specialization on species level.

Table 6. Distribution of syringophilids associated with parrots in the zoogeographical regions.

Zoogeographical Region
Quill Mites Species	Neot.	Near.	Pana.	Afro.	Orie.	Ocean.	Austra.
Me. cacatua
Me. cyanocephala
Me. dubinini
Me. eos
Me. geoffroyus
Me. kethleyi
Me. platycercus
Me. rhynchopsittae
Me. trichoglossus
Ne. aratingae
Ne. agapornis
Ne. cacatui
Ne. krafti
Ne. unsoeldi
Ne. mexicana
Ne. mironovi
Ne. pseudeos
Ne. psittaculae
Ne. puylaerti
Ne. skorackii
Pe. forpi
Pe. mucuya
Pe. nestoriae
Ps. amazonae
Ps. fritschi
Te. loricinus
Te. pioni
Te. reichholfi
La. araraunae
La. arini
La. calyptorhyncha
La. eclectus
La. poicephali
La. sulphurea
La. touiti
Pi. cyclopsitta
Pi. fuscata
Pi. tahitiana
Pi. malherbi
Pi. glossopsitta
Ra. brotogeris
Ra. pyrrhura
Ra. trinidadi
Ra. valdiviana
Ra. xanthopterygius

Zoogeographical regions: Afro.—Afrotropical, Aust.—Australasian, Near.—Nearctic, Neot.—Neotropical, Ocea.—Oceanian, Orie.—Oriental, Pala.—Palaearctic, Pana.—Panamanian, Sa-Arab.—Saharo-Arabian, Si-Jap.—Sino-Japanese (according to Holt et al. [56]). Filling with black color - confirms the presence of a given species of quill mite in a given area.

Table 7. Host specificity of quill mites associated with parrots.

Genus and Number of Species	Monoxenous Parasites	Oligoxenous Parasites	Mesostenoxenous Parasites	Metastenoxenous Parasites	Polixenous Parasites
Megasyringophilus (9)	6	2	1	-	-
Neoaulobia (11)	6	2	2	1	-
Peristerophila (3)	2	-	-	-	1
Terratosyringophilus (3)	2	-	1	-	-
Psittaciphilus (2)	1	1	-	-	-
Lawrencipicobia (7)	5	1	1	-	-
Pipicobia (5)	4	1	-	-	-
Rafapicobia (5)	2	1	2	-	-
Total (45)	28 (63%)	8 (18%)	7 (15%)	1 (2%)	1 (2%)

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Marciniak-Musial, N.; Skoracki, M.; Kosicki, J.Z.; Unsöld, M.; Sikora, B. Host-Parasite Relationships of Quill Mites (Syringophilidae) and Parrots (Psittaciformes). Diversity 2023, 15, 1. https://doi.org/10.3390/d15010001

AMA Style

Marciniak-Musial N, Skoracki M, Kosicki JZ, Unsöld M, Sikora B. Host-Parasite Relationships of Quill Mites (Syringophilidae) and Parrots (Psittaciformes). Diversity. 2023; 15(1):1. https://doi.org/10.3390/d15010001

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Marciniak-Musial, Natalia, Maciej Skoracki, Jakub Z. Kosicki, Markus Unsöld, and Bozena Sikora. 2023. "Host-Parasite Relationships of Quill Mites (Syringophilidae) and Parrots (Psittaciformes)" Diversity 15, no. 1: 1. https://doi.org/10.3390/d15010001

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Host-Parasite Relationships of Quill Mites (Syringophilidae) and Parrots (Psittaciformes)

Abstract

1. Introduction

2. Materials and Methods

2.1. Mite Material

2.2. Morphological Characters

2.3. Prevalence

2.4. Host Specificity

2.5. Host Scientific Names and Zoogeographical Regions

2.6. Bipartite Networks and Statistics

2.7. Mite Phylogeny

2.8. Visualization of Host Phylogeny

3. Results

3.1. The Species Richness of Syringophilid Mites Associated with Parrots

3.1.1. Subfamily Syringophilinae Lavoipierre, 1953

Genus Megasyringophilus Fain, Bochkov & Mironov, 2000

Genus Neoaulobia Fain, Bochkov & Mironov, 2000

Genus Peristerophila Casto, 1980

Genus Psittaciphilus Fain, Bochkov & Mironov, 2000

Genus Terratosyringophilus Bochkov & Perez, 2002

3.1.2. Subfamily Picobiinae Johnston & Kethley, 1973

Genus Rafapicobia Skoracki, 2011

Genus Lawrencipicobia Skoracki & Hromada, 2013

Genus Pipicobia Glowska and Schmidt, 2014

3.1.3. Key to the Syringophilid Subfamilies, Genera, and Species Associated with Parrots (the Morphological Terminology and Chaetotaxy follow Skoracki [12])

3.2. Prevalence

3.3. Host-Specificity of the Quill Mites

3.4. Bipartite Network Analysis

3.5. Co-Infestation of the Quill Mites

3.6. Zoological Distribution of Quill Mites Species Associated with Parrots

3.7. Phylogenetic Relationship of the Genera Associated with Parrots

4. Discussion

4.1. Species Richness and Phylogenetic Relationship of Quill Mites Associated with Psittaciformes Birds

4.2. Species Richness and Phylogenetic Relationship of Quill Mites Associated with Psittaciformes Birds

4.3. Quill Mites and Their Habitat-Specificity

4.4. Prevalence

4.5. Analyses of the Bipartite Network of Quill Mite–Parrots Communities

5. Conclusions

Supplementary Materials

Author Contributions

Funding

Institutional Review Board Statement

Data Availability Statement

Acknowledgments

Conflicts of Interest

References

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