Next Article in Journal
Genomic and Pathological Characterization of Acute Hepatopancreatic Necrosis Disease (AHPND)-Associated Natural Mutant Vibrio parahaemolyticus Isolated from Penaeus vannamei Cultured in Korea
Previous Article in Journal
Comparing the Performance of Automatic Milking Systems through Dynamic Testing Also Helps to Identify Potential Risk Factors for Mastitis
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Animals
Volume 14
Issue 19
10.3390/ani14192790
animals-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Article

Corvisyringophilus, a New Genus in the Family Syringophilidae (Acariformes: Prostigmata) and Its Phylogenetic Position among Primitive Genera †

by
Maciej Skoracki
1,*,
Ólafur K. Nielsen
2 and
Bozena Sikora
1,*
1
Department of Animal Morphology, Faculty of Biology, Adam Mickiewicz University, Uniwersytetu Poznańskiego 6, 61-614 Poznań, Poland
2
Icelandic Institute of Natural History, Urriðaholtsstræti 6-8, IS-210 Garðabær, Iceland
*
Authors to whom correspondence should be addressed.
†
urn:lsid:zoobank.org:act:D8277935-119A-4996-A22C-EEA6A123CB92; urn:lsid:zoobank.org:act:304D74F8-514F-4AD0-89FA-F12836EA9F28.
Animals 2024, 14(19), 2790; https://doi.org/10.3390/ani14192790
Submission received: 5 September 2024 / Revised: 23 September 2024 / Accepted: 24 September 2024 / Published: 26 September 2024
(This article belongs to the Section Ecology and Conservation)
Browse Figures
Versions Notes

Abstract

:

Simple Summary

The Syringophilidae family is one of the most diverse groups of prostigmatic mites (Acari: Prostigmata) parasitising birds. In this paper, we describe a new genus and species, Corvisyringophilus krummi, which parasitises the Common Raven (Corvus corax) in Iceland. This new genus belongs to a group of primitive genera that retain a complete set of idiosomal and leg setae. Our phylogenetic analysis suggests that Corvisyringophilus is morphologically closely related to the genera Blaszakia Skoracki & Sikora, 2008 and Charadriphilus Bochkov & Mironov, 1998, which are associated with birds of different and phylogenetically unrelated orders: Musophagiformes and Charadriiformes, respectively. This research highlights the importance of examining the genus Corvus in order to better understand the specialised host–parasite relationships. Furthermore, the study emphasises the significance of using museum collections to study parasitic interactions.

Abstract

Syringophilidae is one of the most species-rich families in the superfamily Cheyletoidea, comprising approximately 420 species across 62 genera and two subfamilies. In this paper, we propose a new genus, Corvisyringophilus, and a new species, C. krummi gen. n. et sp. n., found in the wing covert quills of the Common Raven, Corvus corax Linnaeus, in Iceland. Corvisyringophilus is placed among the primitive genera of syringophilid mites, which possess the full complement of idiosomal and leg setae. Phylogenetic analysis based on morphological characters suggests that this genus forms a sister clade to Blaszakia Skoracki & Sikora, 2008, and Charadriphilus Bochkov & Mironov, 1998, which inhabit birds of the orders Musophagiformes and Charadriiformes, respectively. The study proposes that the current distribution patterns of quill mites, based on their morphological characteristics, may result from multiple host switching followed by co-speciation events, highlighting the complex evolutionary dynamics within this family.

1. Introduction

The Syringophilidae is one of the most species-rich families in the superfamily Cheyletoidea (Acariformes: Prostigmata), and currently comprises approximately 420 species arranged in 62 genera and two subfamilies, Picobiinae Johnston & Kethley, 1973 and Syringophilinae Lavoipierre, 1953 [1,2,3,4,5,6]. Syringophilid species have been recorded from 25 neognathous bird orders (Neognathae) and 1 paleognathous order, Tinamiformes (Paleognathae) [7]. These obligatory ectoparasites inhabit quill feathers and exhibit high specificity to both their hosts and habitats. Consequently, individual species infest a limited range of hosts and specific types of feathers [3,4,8].
Among quill mite genera, there are highly speciose taxa, such as Picobia Haller, 1878, which comprises 44 species; Syringophiloidus Kethley, 1970, with 47 species; and Syringophilopsis Kethley, 1970, with 49 species. There are also monotypic genera, such as Trypetoptila Kethley, 1970, Tanopicobia Skoracki et al., 2020, and Calamincola Casto, 1978. Most genera are associated with specific avian orders; for example, Gunabopicobia Skoracki & Hromada, 2013, is associated exclusively with Columbiformes; Aulobia Kethley, 1970, is associated with Passeriformes; and Bubophilus Philips & Norton, 1978, is associated with Strigiformes [3,4]. However, some genera are distributed across a broad range of host orders, which are not always phylogenetically closely related. For instance, Peristerophila Kethley, 1970, is associated with Accipitriformes, Bucerotiformes, Columbiformes, Coraciiformes, Falconiformes, and Psittaciformes; Picobia is recorded on Bucerotiformes, Passeriformes, and Piciformes; and Rafapicobia Skoracki, 2011, is noted on Coraciiformes, Gruiformes, Passeriformes, Piciformes, and Psittaciformes [3,4,5].
Compared to Cheyletidae Leach, 1815, their sister family, the Syringophilidae, has relatively uniform morphology. The main criterion for distinguishing the genera is the presence or absence of setae on the legs and idiosoma [9,10,11]. However, seta characters are crucial for the phylogenetic reconstruction of the whole Eleutherengones group [12]. Among syringophilids, some genera retain a full complement of setae, while others lose certain setae [3]. The absence of idiosomal setae is notable on the propodonotum, such as setae vi in genera like Aulonastus Kethley, 1970, Neoaulonastus Skoracki, 2004, and Peristerophila; or on the opisthosoma, such as aggenital setae ag2 in Kethleyana Kivganov, 1995, Mironovia Chirov & Kravtsova, 1995, and Picisyringophilus Skoracki & OConnor, 2010; pseudanal setae ps2 in Betasyringophiloidus Skoracki, 2011, or Krantziaulonastus Skoracki, 2011, and genital setae g2 in Procellariisyringophilus Schmidt & Skoracki, 2007. The absence of leg setae is more varied and can include the loss of setae on different podomers and pairs of legs, such as the absence of tarsus setae vsI in Paraniglarobia Skoracki, 2011, or Philoxanthornea Kethley, 1970, vsII in Cuculisyringophilus Skoracki, 2008, or Niglarobia Kethley, 1970; femoral setae dFII in Fritschisyringophilus Bochkov et al., 2004, or Meitingsunes Skoracki & Glowska, 2010, dFIII–IV in Peristerophila, or Psittaciphilus Fain et al., 2000; genu setae dGII in Syringophiloidus, or Galliphilopsis Skoracki & Sikora, 2004, l’GIV in Neosyringophilopsis Skoracki & Sikora, 2005, or Apodisyringiana Skoracki, 2005; tibial setae dTIII–IV in Galliphilopsis, or Neoaulonastus, and trochanter setae l’RI–II in Aulonastus, or Picobia. In syringophilid genera, species are primarily distinguished by quantitative characteristics such as the length of the stylophore or setae, with a few exceptions, and this is the main reason why the genera are not divided into subgenera.
In the present paper, we propose a new genus, Corvisyringophilus, for a new species, C. krummi gen. n. et sp. n., collected from the feather quills of the Common Raven Corvus corax Linnaeus in Iceland, and determine the placement of this new genus among other primitive genera of syringophilid mites, which retain a full complement of setae. It should also be noted that this is the fourth species of quill mite recorded on bird hosts in Iceland, the other three being Mironovia lagopus Bochkov & Skirnisson, 2011, from the Rock Ptarmigan Lagopus muta (Montin) (Galliformes: Phasianidae); Syringophilus bipectinatus Heller, 1880, from the Red Junglefowl (domestic type) Gallus gallus domesticus (Linnaeus); and Stibarokris nielseni Skoracki et al., 2022, from the Manx Shearwater Puffinus puffinus (Brünnich) [13,14,15,16].

2. Materials and Methods

2.1. Mites Collection and Description

Mite material was collected from the dry skin of the Common Raven Corvus corax housed in the ornithological collection at the Icelandic Institute of Natural History, Reykjavík, Iceland (IINH). Mites were removed from the quills of small wing coverts using sharp tweezers. Initially, mite specimens were softened and cleared in Nesbitt’s solution at 40 °C for about two days and then mounted in Hoyer’s medium [17]. Identification of mite specimens and drawing preparations were carried out with a ZEISS Axioscope2™ light microscope, equipped with differential interference contrast (DIC) optics and a camera lucida (Carl-Zeiss AG, Oberkochen, Germany). In the description, all measurements are given in micrometres, with ranges for paratypes in parentheses following data for a holotype. The general syringophilid morphological terms follow Kethley [2] and Skoracki [4]. The nomenclature for leg setation is that of Grandjean [18]; the idiosomal setation follows Grandjean [19], as adapted for Prostigmata by Kethley [20].
Specimen depositories and reference numbers are cited using the following abbreviations: AMU—Adam Mickiewicz University, Department of Animal Morphology, Poznan, Poland; IINH—Icelandic Institute of Natural History, Reykjavík, Iceland.

2.2. Phylogenetic Analysis

To determine the placement of the new genus, we used the data matrix recently published by Skoracki et al. [7]. The species used in the analyses represent the most primitive genera of the family Syringophilidae, specifically the 19 genera that possess a full complement of setae on the idiosoma and legs. Because the monophyly of the family Syringophilidae has been tested with numerous outgroups and always received high support [9,10,21,22], only two outgroups were used in the analyses, both belonging to the sister family Cheyletidae—the quill-inhabiting predator Cheletopsis norneri (Poppe) and the free-living predator Cheyletus eruditus (Schrank). In the cladistic analysis, only qualitative characteristics from external morphology were used, focusing on features such as the presence or absence of specific structures and the form of particular morphological features. A total of 32 operational taxonomic units (OTUs) and 50 informative characters were included in the maximum parsimony-based cladistic analysis (Supplementary Tables S1 and S2). All characters in the data matrix were treated as unordered, with their states polarised through outgroup comparison. Phylogenetic relationships were reconstructed using PAUP 4.0 [23], employing a heuristic search for the maximum parsimony analysis. The delayed transformation (DELTRAN) option was applied to favour parallelism over reversal, optimising character states and tracing changes across lineages a posteriori. All characters were analysed without weighting.

3. Results

3.1. Systematic

Family: Syringophilidae Lavoipierre, 1953.
Subfamily: Syringophilinae Lavoipierre, 1953.

3.1.1. Description

Genus Corvisyringophilus gen. n

Diagnosis. Female. Small-sized syringophilids. Gnathosoma. The hypostomal apex is rounded and without protuberances. Two pairs of large hypostomal lips are present. Lateral hypostomal teeth are absent. The peritremes are M-shaped with clearly visible chambers in each branch. The anterior tip of each movable cheliceral digit is edentate. The stylophore is rounded posteriorly. Idiosoma. The propodonotum bears six pairs of propodonotal setae arranged in the pattern 2–1–1–2; bases of setae se are situated on the propodonotal shield and posterior to c1. Setae d1 are situated closer to d2 than to e2. The hysteronotal shield is present. The aggenital setal series consists of three pairs of setae. Each pseudanal and genital series has two pairs of setae. All idiosomal setae are smooth and whip-like. Legs. Legs I are thicker than II. Antaxial and paraxial members of the claw pair are subequal in size and shape and without a basal angle. Apodemes I are parallel and not fused to apodemes II. Legs contain the full complement of setae.
Male. Features the same as in the female, except hypostomal lips, which are small-sized; stylophore is constricted posteriorly; six pairs of propodonotal setae are arranged in the pattern 2–1–1–1–1; bases of setae se are situated out of the propodonotal shield and anterior to c1; apodemes I are strongly divergent and not fused to apodemes II.

Habitat

Quills of secondary wing coverts.

Type Species

Corvisyringophilus krummi sp. n.

Remarks

Phylogenetic and morphological analyses indicate that Corvisyringophilus gen. n. is the most similar to two genera, i.e., Blaszakia Skoracki & Sikora, 2008, associated with birds of the family Musophagidae (Musophagiformesthe) [24] and Charadriphilus Bochkov & Chistyakov, 2001 associated with birds of the orders Charadriiformes and Gruiformes [25]. In females of these three genera, the lateral hypostomal teeth are absent; the distal tip of the movable cheliceral digits are edentate; the peritremes are M-shaped; bases of setae se are situated on the propodonotal shield and posterior to setal bases c1; the hysteronotal shield is present and fused to the pygidial shield, its anterior margin reach bases of setae d2; the aggenital series contains three pairs of setae; each pseudanal and genital series contains two pairs of setae, each; apodemes I and II are not fused; the idiosoma and legs contain the full complement of setae. The differences between Corvisyringophilus and those mentioned above, which are closely related genera, are presented in Table 1.

Etymology

The name “Corvisyringophilus” is derived from the generic name of the host—Corvus—and the type genus of the syringophilid family—Syringophilus.

Corvisyringophilus krummi sp. n. (Figure 1 and Figure 2)

Description. Female, holotype. The total body length of the holotype is 655 (650–665 in seven paratypes). Gnathosoma. The infracapitulum is punctate in the anterior part. The hypostomal apex is without protuberances, but two pairs of finger-like hypostomal lips are present. The stylophore is rounded posteriorly and 165 (150–170) long. The exposed portion of the stylophore is apunctate and 125 (115–135) long. Each branch of the peritremes has two chambers, and each lateral branch has six chambers. Idiosoma. The propodonotal shield is entire, with concave anterior and posterior margins, punctate near lateral margins, bearing bases of all propodonotal setae except c2. Setae vi, ve, and si are short; the length ratio of setae vi:ve:si is 1:1–1.3:1–2. The bases of setae c1 are situated anterior to the level of setal bases se. Setae c1 and se are subequal in length. The apunctate hysteronotal shield is not fused to the pygidial shield; the anterior margin reaches the level of setae d2, the posterior margin tapers, and the bases of setae d1 are situated on the lateral margins of this shield. The length ratio of setae d2:d1:e2 is 1.2–1.3:1:1–1.2. The pygidial shield is apunctate and with an indiscernible anterior margin. Bases of setae f2 are situated distinctly anterior to the level of setal bases f1. Setae f2 are about six times longer than f1; setae h2 are about twice as long as f2. Setae ag1 and ag3 are subequal in length, and both pairs of these setae are about twice as long as ag2. The genital plate is present, bearing setae ag2 and ag3 bases on its lateral margins. Both pairs of pseudanal setae ps1 and ps2 are subequal in length. Both pairs of genital setae g1 and g2 are subequal in length, and both pairs are 1.7–2 times longer than pseudanal setae. Coxal fields I and II are sparsely punctate; III and IV are densely punctate. The cuticular striations of the idiosoma are as shown in Figure 1A,B. Legs. Fan-like setae p′ and p″ of tarsi III and IV have six to eight tines. Setae tc″III–IV are about twice as long as tc’III–IV. Setae l’RIII and l’RIV are subequal in length. The lengths of the setae are as follows: vi 20 (20–30), ve 20 (20–25), si 30 (30–40), se 185 (180–200), c1 205 (175–195), c2 185 (180–190), d1 145 (140–155), d2 180 (180–185), e2 180 (160–180), f1 30 (25–30), f2 185 (175–185), h1 30 (25–30), h2 (350–370), ag1 120 (110–125), ag2 60 (60–70), ag3 125 (125–130), ps1 and ps2 15 (15–20), g1 and g2 30 (25–30), tc’III–IV 30 (30–35), tc″III–IV 60 (55–60), l’RIII–IV 30 (30–35).
Male. The total body length is 480–490 in four paratypes. Gnathosoma. The infracapitulum is sparsely punctate in the anterior part. The hypostomal apex is without protuberances. The stylophore is slightly constricted posteriorly and is 150–155 long. The exposed portion of the stylophore is apunctate and 120–125. Each branch of the peritremes has two chambers, each lateral branch has eight or nine chambers. Idiosoma. The propodonotal shield is entire, with a concave anterior margin, covered with minute punctuations in the anterior part, bearing bases of setae vi, ve, si, and c1. Setae vi, ve, and si are short and subequal in length. The bases of setae c1 are situated slightly posterior to the level of setal bases se. The hysteronotal shield is fused to the pygidial shield, apunctate; the anterior margin reaches above the level of setae d2, and bases of setae d1, f2, and h2 are situated on this shield. Setae d2 are about twice as long as d1 and e2. Setae h2 are about four times longer than f2. All coxal fields are sparsely punctate. The cuticular striations of the idiosoma are as shown in Figure 2A,B. Legs. Fan-like setae p′ and p″ of tarsi III and IV have six or seven tines. Setae tc″III–IV are about twice as long as tc’III–IV. The lengths of the setae are as follows: vi 20–25, ve 20–30, si 20–30, se 130–140, c1 is variable in lengths: 65 or 100–130, c2 110–145, d1 15–20, d2 30–40, e2 15–20, f2 25–35, h2 230, agenital setae are variable in lengths: ag1 30–90, ag2 40–70, ag3 50–90, tc’III–IV 20–25, tc″III–IV 40, l’RIII 40, l’RIV 25, 3b and 4b 25, 3c and 4c 75.
Animals 14 02790 g001
Figure 1. Corvisyringophilus krummi gen. n. et sp. n. Female. (A) Dorsal view; (B) ventral view; (C) hypostomal apex in dorsal view; (D) peritremes; (E) fan-like seta p’III. Scale bars (A,B) = 50 µm, (C–E) = 20 µm.
Figure 1. Corvisyringophilus krummi gen. n. et sp. n. Female. (A) Dorsal view; (B) ventral view; (C) hypostomal apex in dorsal view; (D) peritremes; (E) fan-like seta p’III. Scale bars (A,B) = 50 µm, (C–E) = 20 µm.
Animals 14 02790 g001
Animals 14 02790 g002
Figure 2. Corvisyringophilus krummi gen. n. et sp. n. Male. (A) Dorsal view; (B) ventral view; (C) peritremes; (D) fan-like seta p’III. Scale bars (A,B) = 50 µm, (C,D) = 20 µm.
Figure 2. Corvisyringophilus krummi gen. n. et sp. n. Male. (A) Dorsal view; (B) ventral view; (C) peritremes; (D) fan-like seta p’III. Scale bars (A,B) = 50 µm, (C,D) = 20 µm.
Animals 14 02790 g002

Type Material

Female holotype and paratypes: seven females and four males collected from the quill of the wing covert of the Common Raven Corvus corax Linnaeus (Passeriformes: Corvidae) (host reg. no. IINH-RM 10049, male); Iceland: Borgarhofn, South District, East Skaftafell County (Borgarhöfn, Suðursveit, A.-Skaft.) 64°11′32.1″ N 15°48′33.1″ W, 5 October 1989, bird coll. S. Valtýsson, mites removed by M. Skoracki.

Type Material Deposition

The holotype and most paratypes (reg. no. MS 24-0903-001) are deposited in the AMU except three female paratypes and one male paratype in the IINH.

Etymology

The species name “krummi” is derived from the Icelandic word “krummi,” the nickname of the “raven” that is affectionally used by Icelanders when referring to this bird species. This name was chosen to honour the Common Raven, Corvus corax, the bird species with which this mite is associated. The use of “krummi” reflects both the common name of the bird in Icelandic culture and the genus Corvus, which signifies the host genus of the new species.

3.1.2. Parsimony Analysis

Three equally parsimonious trees were produced by the initial analysis, with all characters treated as unordered and unweighted (tree length 129, consistency index (CI) for phylogenetically informative characters—0.45, retention index (RI)—0.69, rescaled consistency index (RC)—0.31. The strict consensus of these trees is shown in Figure 3 and Figure 4. The differences between these trees lie solely in the positioning of the genus Trypetoptila relative to the genera Torotrogla, Syringophilopsis, and Crotophagisyringophilus.

4. Discussion

Crown birds (Neornithes), comprising approximately 11,000 species, are divided into two distinct monophyletic groups: Palaeognathae, which includes tinamous and ratites, and Neognathae, which encompasses all other avian species [26,27]. Within the Neognathae, the Galloanserae (which consists of Galliformes and Anseriformes) is identified as the sister group to the remaining birds, collectively referred to as Neoaves [28,29,30,31]. Syringophilid mites, from the subfamilies Syringophilinae and Picobiinae, have been found in 27 out of the 44 recognised orders of extant neognathous and palaeognathous birds [5,7].
Syringophilid mites from the most primitive genera, which possess a complete set of idiosomal and leg setae, are distributed across all three major clades of birds: Palaeognathae, Galloanserae, and Neoaves. The presence of syringophilids on these two primary bird clades led Skoracki et al. [32] to suggest that syringophilids likely formed relationships with the ancestors of birds, feathered theropod dinosaurs like Archaeopteryx or Aurornis [33,34,35,36]. However, recent cladistic analyses indicate that mite genera associated with the earliest divergent clades of extant birds, Tinamiformes (Palaeognathae) and Galloanserae (Anseriformes and Galliformes), are mosaically distributed within the core of the tree (see Figure 4). This contradiction between the presumed syringophilid parasitism of the common bird ancestor and the observed phylogenetic pattern could be explained by multiple host switching (secondary infestation) from Neoaves to palaeognathous and galloanserae birds, followed by subsequent co-speciation [7]. The genus Corvisyringophilus, proposed herein, belongs to a clade that includes the genera Kalamotrypetes Casto, 1980 and Colinophilus Kethley, 1973, found on birds of the order Galliformes [37,38]. It represents a sister clade to the closely related genera Blaszakia, which inhabits birds of the order Musophagiformes [24], and Charadriphilus found on birds of the orders Charadriiformes and Gruiformes [25,39,40,41] (Figure 3 and Figure 4). Phylogenetic analyses of birds do not indicate a close relationship between Passeriformes and either Musophagiformes or Charadriiformes and Gruiformes [30,31,42]. In this case, we are likely observing the host switching between birds belonging to unrelated orders, followed by subsequent speciation.
The genus Corvisyringophilus is one of the several syringophilid genera inhabiting passeriform birds. The order Passeriformes represents the largest and most diverse group of birds, comprising approximately 6,200 species, which constitutes about 60% of all extant avian species. [43]. Notably, this order also harbours the greatest number of syringophilid mite species. To date, 17 genera (out of 65, or 26%) and 241 species (out of 425, or 57%) of syringophilid mites have been documented from passerines belonging to 62 families (out of 143, or 43%). Among the genera parasitising passerine birds, several are exclusively associated with this order, including Aulobia Kethley, 1970, Aulonastus Kethley, 1970, Betasyringophiloidus Skoracki, 2011, Corvisyringophilus gen. n., Fritschisyringophilus Bochkov, Fain & Skoracki, 2004, Torotrogla Kethley, 1970, and Phipicobia Glowska & Schmidt, 2014 [2,3,40,44]. In the remaining genera, the majority of species are primarily associated with passerines, with only a small fraction exhibiting host switching to non-passeriform birds: Krantziaulonastus Skoracki, 2011, Neoaulonastus Skoracki, 2004, Neosyringophilopsis Skoracki & Sikora, 2005, Syringophiloidus Kethley, 1970, Syringophilopsis Kethley, 1970, Neopicobia Skoracki, 2011, Picobia Haller, 1878, Pipicobia Glowska & Schmidt, 2014, and Rafapicobia Skoracki, 2011 [2,3,4,45,46]. Interestingly, in two instances, passerines of the family Paradisaeidae appear to have “adopted” quill mites from non-passeriform birds. These mites belong to the genera Gunabopicobia Skoracki & Hromada, 2013 and Peristerophila Kethley, 1970 [47].
The family Corvidae includes some of the most well-known birds in the world. Ravens and crows are particularly renowned for their social behaviour and intelligence. Corvids inhabit nearly every terrestrial environment on Earth, from Arctic tundra and arid deserts to urban streets and tropical rainforests. [48]. Although many species within this family are common, our understanding of the parasitic fauna associated with these birds is quite limited. Of the 130 species in this family, parasitic mites have been recorded on only 12 corvid species (8% of the total), representing just 9 mite species belonging to six genera (including one newly established herein). This underscores the significant gaps in our knowledge regarding the diversity of quill mites that parasitise this group of hosts. A similar situation arises when analysing the quill mite fauna associated with birds of the genus Corvus. Unfortunately, our current understanding of the quill mite fauna associated with jackdaws, crows, and ravens also remains far from satisfactory. Presently, only 3 species of syringophilids have been recorded on 4 host species from the genus Corvus out of 46 described (constituting just 9%). These are Syringophiloidus glandarii (Fritsch, 1958), found on the American Crow, C. brachyrhynchos Brehm in the USA, the Rook C. frugilegus Linnaeus, and the Eurasian Jackdaw, C. monedula Linnaeus in Kazakhstan, Corvitorotroglus alpha Skoracki & Bochkov, 2010, found on C. frugilegus in Kazakhstan [41,46,49], and Corvisyringophilus krummi parasitising the Common Raven, Corvus corax in Iceland. Therefore, it is imperative to thoroughly examine the entire genus Corvus for the presence of syringophilids. This is crucial for unequivocally describing the host–parasite interactions within the Syringophilidae–Corvus system. A future comprehensive analysis of the quill mites associated with birds of the genus Corvus will significantly contribute to improving our understanding of syringophilid parasites within the entire Corvidae family.

5. Conclusions

This study reveals the complex evolutionary relationships between syringophilid mites and their avian hosts, highlighting their distribution across major avian clades: Palaeognathae, Galloanserae, and Neoaves. Our research introduces the new genus Corvisyringophilus, which is closely related to the genera Kalamotrypetes and Colinophilus found on Galliformes and forms a sister clade to Blaszakia and Charadriphilus. The distribution of syringophilid mites in early-divergent bird clades supports the hypothesis of multiple host switching followed by co-speciation events.
The limited knowledge of syringophilid fauna associated with hosts of the genus Corvus underscores the need for comprehensive examinations of this avian genus to better understand the host–parasite dynamics within the Syringophilidae–Corvus system. Additionally, this study highlights the value of museum specimens as a vital resource for taxonomic and ecological analyses, providing insights into the diversity and evolutionary history of syringophilid mites. Museum collections enable comprehensive studies that are often challenging to perform in the field, offering rich opportunities to uncover new species and explore ecological interactions.

Supplementary Materials

The following supporting information can be downloaded at https://www.mdpi.com/article/10.3390/ani14192790/s1. Table S1: List of characters used in the phylogenetic analysis. Table S2: Data matrix.

Author Contributions

Conceptualisation, M.S., Ó.K.N. and B.S.; methodology, M.S. and B.S.; vali-dation, M.S., Ó.K.N. and B.S.; formal analysis, M.S., Ó.K.N. and B.S.; investigation, M.S. and B.S.; material collection, M.S. and B.S.; data curation, M.S.; writing—original draft preparation, M.S., Ó.K.N. and B.S.; writing—review and editing, M.S., Ó.K.N. and B.S.; visualisation, M.S.; supervision, M.S.; project administration, M.S. and B.S.; funding acquisition, M.S. and B.S. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the Excellence Initiative Program “Mobility” of the UAM Research University—UAM ID-UB 094/07/POB1/0013 (to M.S.) and UAM UD-UB 094/07/POB1/0012 (to B.S.).

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Data are available upon request from the corresponding author.

Acknowledgments

We would like to thank Anna Sveinsdóttir and Matthías Alfreðsson (IINH) for their invaluable help during our (M.S. and B.S.) stay at IINH. We also thank the anonymous reviewers for their critical review of the manuscript.

Conflicts of Interest

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

References

  1. Lavoipierre, M.M.J. The undescribed male and female of the Pigeon quill mite, Syringophilus columbae Hirst, 1920. Trans. R. Soc. Trop. Med. Hyg. 1953, 47, 7. [Google Scholar]
  2. Kethley, J.B. A revision of the family Syringophilidae (Prostigmata: Acarina). Contrib. Am. Entomol. Inst. 1970, 5, 1–76. [Google Scholar]
  3. Skoracki, M. Quill mites (Acari: Syringophilidae) of the Palaearctic region. Zootaxa 2011, 2840, 1–414. [Google Scholar] [CrossRef]
  4. Skoracki, M.; Sikora, B.; Spicer, G.S. A review of the subfamily Picobiinae Johnston and Kethley, 1973 (Acariformes: Prostigmata: Syringophilidae). Zootaxa 2016, 4113, 1–95. [Google Scholar] [CrossRef]
  5. Zmudzinski, M.; Skoracki, M.; Sikora, B. An Updated Checklist of Quill Mites of the Family Syringophilidae (Acariformes: Prostigmata). 2023. Available online: https://figshare.com/articles/dataset/An_updated_checklist_of_quill_mites_of_the_family_Syringophilidae_Acariformes_Prostigmata_/16529574 (accessed on 1 August 2024).
  6. Glowska, E.; Chrzanowski, M.; Kaszewska, K. Checklist of the quill mites (Acariformes: Syringophilidae) of the World. Zootaxa 2015, 3968, 1–81. [Google Scholar] [CrossRef]
  7. Skoracki, M.; Fajfer, M.; Hromada, M.; Hušek, J.; Sikora, B. Tinamiphilopsis temmincki sp. n., a New Quill Mite Species from Tataupa Tinamou, and the Early History of Syringophilid Mites. Animals 2023, 13, 2728. [Google Scholar] [CrossRef]
  8. Kethley, J.B. Population regulation in quill mites (Acari: Syringophilidae). Ecology 1971, 52, 1113–1118. [Google Scholar] [CrossRef]
  9. Bochkov, A.V. The classification and phylogeny of the mite superfamily Cheyletoidea (Acari, Prostigmata). Entomol. Rev. 2002, 82, 643–664. [Google Scholar]
  10. Bochkov, A.V. New observations on phylogeny of cheyletoid mites (Acari: Prostigmata: Cheyletoidea). Proc. Zool. Inst. RAS 2008, 312, 54–73. [Google Scholar] [CrossRef]
  11. Skoracki, M.; Glowska, E.; Bochkov, A.V. Phylogeny of quill mites of the family Syringophilidae (Acari: Prostigmata) based on their external morphology. Eur. J. Entomol. 2013, 110, 663–675. [Google Scholar] [CrossRef]
  12. Bochkov, A.V. A review of mites of the parvorder Eleutherengona (Acariformes: Prostigmata)—Permanent parasites of mammals. Acarina 2009, 1 (Suppl. S1), 1–149. [Google Scholar]
  13. Bochkov, A.V.; Skirnisson, K. Description of the life stages of quill mite Mironovia lagopus sp. nov. (Acari: Syringophilidae) parasitizing the rock ptarmigan Lagopus muta (Phasianidae) from Iceland. Parasitol. Res. 2011, 108, 715–722. [Google Scholar] [CrossRef]
  14. Skírnisson, K.; Nielsen, O.K. Quill mite infestation of Rock Ptarmigan Lagopus muta (Aves: Phasianidae) in relation to year and host age, sex, body condition, and density. Parasitol. Res. 2019, 118, 2643–2650. [Google Scholar] [CrossRef]
  15. Skírnisson, K.; Pálsdóttir, G. Past and present status of poultry parasites in Iceland. Icel. Agric. Sci. 2020, 33, 3–14. [Google Scholar] [CrossRef]
  16. Skoracki, M.; Sikora, B.; Zmudzinski, M.; Skirnisson, K.; Hromada, M. A new species, Stibarokris nielseni sp. nov. (Acariformes: Syringophilidae) parasitizing Puffinus puffinus (Procellariiformes: Procellariidae) in Iceland, with notes on host associations of the genus Stibarokris. Syst. Appl. Acarol. 2022, 27, 649–659. [Google Scholar] [CrossRef]
  17. Walter, D.E.; Krantz, G.W. Collecting, rearing, and preparing specimens. In A Manual of Acarology; Krantz, G.W., Walter, D.E., Eds.; Texas Tech University Press: Lubbock, TX, USA, 2009; pp. 83–96. [Google Scholar]
  18. Grandjean, F. Les segments post-larvaires de l’hystérosoma chez les Oribates (Acariens). Bull. Soc. Zool. Fr. 1939, 64, 273–284. [Google Scholar]
  19. Grandjean, F. Observations Sur Les Acariens de La Famille Des Stigmaeidae. Arch. Sci. Phys. Nat. 1944, 26, 103–131. [Google Scholar]
  20. Kethley, J.B. Acarina: Prostigmata (Actinedida). In Soil Biology Guide; Dindal, D.L., Ed.; John Wiley & Sons: New York, NY, USA, 1990; pp. 667–756. [Google Scholar]
  21. Bochkov, A.V. Mites of the family Cheyletidae (Acari: Prostigmata): Phylogeny, distribution, evolution and analysis of parasite-host relationship. Parazitologia 2004, 38, 122–138. (In Russian) [Google Scholar]
  22. Bochkov, A.V.; O’Connor, B.M.; Wauthy, G. Phylogenetic position of the family Myobiidae within the Prostigmata (Acari: Acariformes). Zool. Anz. 2008, 247, 15–45. [Google Scholar] [CrossRef]
  23. Swofford, D.L. PAUP. Phylogenetic Analysis Using Parsimony (* and Other Methods), Version 4; Sinauer Associates: Sunderland, MA, USA, 2001. [Google Scholar]
  24. Skoracki, M.; Sikora, B. Blaszakia, a new genus of quill mites (Acari: Syringophilidae) parasitising Turacos (Aves: Musophagiformes). Ann. Zool. 2008, 58, 327–332. [Google Scholar] [CrossRef]
  25. Bochkov, A.V.; Chystiakov, D.V. Description of Charadriphilus lyudmilae gen et sp. n. (Acari: Syringophilidae) from Scolopax rustica (Aves: Scolopacidae) in NW Russia. Zoosyst. Ross. 2001, 9, 295–297. [Google Scholar]
  26. Clements, J.F.; Rasmussen, P.C.; Schulenberg, T.S.; Iliff, M.J.; Fredericks, T.A.; Gerbracht, J.A.; Lepage, D.; Spencer, A.; Billerman, S.M.; Sullivan, B.L.; et al. The eBird/Clements Checklist of Birds of the World. 2023. Available online: https://www.birds.cornell.edu/clementschecklist/download/ (accessed on 27 July 2024).
  27. del Hoyo, J.; Collar, N.J.; Christie, D.A.; Elliott, A.; Fishpool, L.D.C.; Boesman, P.; Kirwan, G.M. HBW and BirdLife International Illustrated Checklist of the Birds of the World. Volume 2: Passerines; Lynx Edicions: Barcelona, Spain; BirdLife International: Cambridge, UK, 2016. [Google Scholar]
  28. Hackett, S.J.; Kimball, R.T.; Reddy, S.; Bowie, R.C.K.; Braun, E.L.; Braun, M.J.; Chojnowski, J.L.; Cox, W.A.; Han, K.L.; Harshman, J.; et al. A phylogenomic study of birds reveals their evolutionary history. Science 2008, 320, 1763–1768. [Google Scholar] [CrossRef]
  29. Sangster, G.; Braun, E.L.; Johansson, U.S.; Kimball, R.T.; Mayr, G.; Suh, A. Phylogenetic definitions for 25 higher-level clade names of birds. Avian. Res. 2022, 13, 100027. [Google Scholar] [CrossRef]
  30. Jarvis, E.D.; Mirarab, S.; Aberer, A.J.; Li, B.; Houde, P.; Li, C.; Ho, S.Y.W.; Faircloth, B.C.; Nabholz, B.; Howard, J.T.; et al. Whole-genome analyses resolve early branches in the tree of life of modern birds. Science 2014, 346, 1320–1331. [Google Scholar] [CrossRef] [PubMed]
  31. Prum, R.O.; Berv, J.S.; Dornburg, A.; Field, D.J.; Townsend, J.P.; Lemmon, E.M.; Lemmon, A.R. A comprehensive phylogeny of birds (Aves) using targeted next-generation DNA sequencing. Nature 2015, 526, 569–573. [Google Scholar] [CrossRef] [PubMed]
  32. Skoracki, M.; Sikora, B.; Ozminski, M. A new quill mite species (Acari: Syringophilidae) parasitising tinamous (Aves: Tinamiformes). Syst. Parasitol. 2012, 81, 109–113. [Google Scholar] [CrossRef]
  33. Mayr, G.; Pohl, B.; Peters, D.S. A well-preserved Archaeopteryx specimen with theropod features. Science 2005, 310, 1483–1486. [Google Scholar] [CrossRef]
  34. Xu, X.; Zhou, Z.; Wang, X. Exceptional dinosaur fossils show ontogenetic development of early feathers. Nature 2010, 464, 1338–1341. [Google Scholar] [CrossRef]
  35. Xu, X.; You, H.; Du, K.; Han, F. An Archaeopteryx-like theropod from China and the origin of Avialae. Nature 2011, 475, 465–470. [Google Scholar] [CrossRef]
  36. Godefroit, P.; Cau, A.; Dong-Yu, H.; Escuillié, F.; Wenhao, W.; Dyke, G. A Jurassic avialan dinosaur from China resolves the early phylogenetic history of birds. Nature 2013, 498, 359–362. [Google Scholar] [CrossRef]
  37. Casto, S.D. A new genus of syringophilid mites from galliform birds in Texas. Texas J. Sci. 1980, 32, 233–240. [Google Scholar]
  38. Kethley, J.B. A new genus and species of quill mites (Acarina: Syringophilidae) from Colinus virginianus (Galliformes: Phasianidae) with notes on developmental chaetotaxy. Fieldiana (Zool.) 1973, 65, 1–8. [Google Scholar]
  39. Skoracki, M.; Sikora, B. New ectoparasitic mites of the family Syringophilidae (Acari: Prostigmata: Cheyletoidea) associated with birds from Argentina. Zootaxa 2002, 27, 1–8. [Google Scholar] [CrossRef]
  40. Bochkov, A.V.; Fain, A.; Skoracki, M. New quill mites of the family Syringophilidae (Acari: Cheyletoidea). Syst. Parasitol. 2004, 57, 135–150. [Google Scholar] [CrossRef]
  41. Skoracki, M.; Bochkov, A.V. Quill mites from Kazakhstan. Zootaxa 2010, 2546, 52–68. [Google Scholar] [CrossRef]
  42. Stiller, J.; Feng, S.; Chowdhury, A.A.; Rivas-González, I.; Duchêne, D.A.; Fang, Q.; Deng, Y.; Kozlov, A.; Stamatakis, A.; Claramunt, S.; et al. Complexity of avian evolution revealed by family-level genomes. Nature 2024, 629, 851–860. [Google Scholar] [CrossRef] [PubMed]
  43. Fjeldså, J.; Christidis, L.; Ericson, P.G.P. The Largest Avian Radiation: The Evolution of Perching Birds, or the Order Passeriformes; Lynx Edicions: Barcelona, Spain, 2020. [Google Scholar]
  44. Glowska, E.; Schmidt, B.K. New quill mites (Cheyletoidea: Syringophilidae) parasitizing the black-headed paradise flycatcher Terpsiphone rufiventer (Passeriformes: Monarchidae) in Gabon. Zootaxa 2014, 3786, 57–64. [Google Scholar] [CrossRef]
  45. Glowska, E.; Schmidt, B.K. New taxa of the subfamily Picobiinae (Cheyletoidea: Syringophilidae) paraziting antbirds and gnateaters (Passeriformes: Thamnophilidae: Conopophagidae) in Guyana. Zootaxa 2014, 3861, 193–200. [Google Scholar] [CrossRef]
  46. Skoracki, M.; Spicer, G.S.; OConnor, B.M. A systematic review of the subfamily Syringophilinae (Acari: Syringophilidae) of the Nearctic region. Part 1: Quill mites associated with passerines (Aves: Passeriformes). Zootaxa 2016, 4084, 451–494. [Google Scholar] [CrossRef]
  47. Skoracki, M.; Unsoeld, M.; Kosicki, J.Z.; Melzer, R.R.; Friedrich, S.; Sikora, B. Enigmatic host-mite relationships: Unraveling the distribution of quill mites on Birds-of-Paradise. Int. J. Parasitol. 2024, 54, 415–427. [Google Scholar] [CrossRef]
  48. Winkler, D.W.; Billerman, S.M.; Lovette, I.J. Crows, Jays, and Magpies (Corvidae), version 1.0. In Birds of the World; Billerman, S.M., Keeney, B.K., Rodewald, P.G., Schulenberg, T.S., Eds.; Cornell Lab of Ornithology: Ithaca, NY, USA, 2020. [Google Scholar] [CrossRef]
  49. Skoracki, M.; Unsöld, M.; Sikora, B. Redescription of Syringophilioidus glandarii (Fritsch, 1958) with new records of hosts and localities (Acariformes, Syringophilidae). Spixiana 2022, 45, 39–44. [Google Scholar]
Animals 14 02790 g003
Figure 3. Majority rule consensus of the three most parsimonious trees (tree length 129, CI for only informative characters—0.45, RI—0.69, RC—0.31.) found using the heuristic search option for the unordered and unweighted dataset. Numbers above branches = % trees with the respective node.
Figure 3. Majority rule consensus of the three most parsimonious trees (tree length 129, CI for only informative characters—0.45, RI—0.69, RC—0.31.) found using the heuristic search option for the unordered and unweighted dataset. Numbers above branches = % trees with the respective node.
Animals 14 02790 g003
Animals 14 02790 g004
Figure 4. The most parsimonious tree of the primitive syringophilid genera (genera with the full complement of setae) and their host associations (orders of birds). The numbers at the genera names indicate the species in each genus.
Figure 4. The most parsimonious tree of the primitive syringophilid genera (genera with the full complement of setae) and their host associations (orders of birds). The numbers at the genera names indicate the species in each genus.
Animals 14 02790 g004
Table 1. Morphological differences between Corvisyringophilus gen. nov. and two closely related genera, Blaszakia and Charadriphilus.
Table 1. Morphological differences between Corvisyringophilus gen. nov. and two closely related genera, Blaszakia and Charadriphilus.
CharacterCorvisyringophilusBlaszakiaCharadriphilus
Posterior end of stylophoreroundedroundedconstricted
Hypostomal apexunornamentedtwo pairs of protuberancesunornamented
Hypostomal lipslargesmallsmall
Leg thicknessI thicker than II–IVI thicker than II–IVall subequal in thickness
Apodemes Iparallelslightly divergentslightly divergent
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.

Share and Cite

MDPI and ACS Style

Skoracki, M.; Nielsen, Ó.K.; Sikora, B. Corvisyringophilus, a New Genus in the Family Syringophilidae (Acariformes: Prostigmata) and Its Phylogenetic Position among Primitive Genera. Animals 2024, 14, 2790. https://doi.org/10.3390/ani14192790

AMA Style

Skoracki M, Nielsen ÓK, Sikora B. Corvisyringophilus, a New Genus in the Family Syringophilidae (Acariformes: Prostigmata) and Its Phylogenetic Position among Primitive Genera. Animals. 2024; 14(19):2790. https://doi.org/10.3390/ani14192790

Chicago/Turabian Style

Skoracki, Maciej, Ólafur K. Nielsen, and Bozena Sikora. 2024. "Corvisyringophilus, a New Genus in the Family Syringophilidae (Acariformes: Prostigmata) and Its Phylogenetic Position among Primitive Genera" Animals 14, no. 19: 2790. https://doi.org/10.3390/ani14192790

APA Style

Skoracki, M., Nielsen, Ó. K., & Sikora, B. (2024). Corvisyringophilus, a New Genus in the Family Syringophilidae (Acariformes: Prostigmata) and Its Phylogenetic Position among Primitive Genera. Animals, 14(19), 2790. https://doi.org/10.3390/ani14192790

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop