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Abstract
Abstract
Hoatzin, a unique species endemic to Neotropics, has puzzled avian systematists since it was described 244 years ago. Despite its enigmatic origin and unparalleled life cycle, behavior, and mode of life, its parasites only occasionally were investigated. In this study, a new species Calamicoptes hoazinus n. sp. (Laminosioptidae: Fainocoptinae) was described, based on females found in the quill-wall of the primary feather of the hoatzin Opisthocomus hoazin (Statius Muller) (Opisthocomiformes: Opisthocomidae). Following on this we also constructed the key to all known species of the genus Calamicoptes. Importantly, our finding represents the first record of the family Laminosioptidae from the opisthocomiform bird and the first record of this mite family in the Neotropical realm. Scarce records of parasite-host interactions in this group, missing molecular data, and the absence of any phylogenetic study allows only to speculate about evolutionary events leading to observed distribution on the extant Neornithian host tree.
http://zoobank.org/urn:lsid:zoobank.org:pub:F312CDE8-FB1F-4509-85BC-900F534E5EA8
http://zoobank.org/urn:lsid:zoobank.org:act:F1EC0F86-BD68-4340-950E-1E1BB9734B09
Introduction
The hoatzin (Opisthocomus hoazin), the only extant species of the order Opisthocomiformes, is a folivorous bird endemic to riverine floodplains in the Amazonian region (Winkler et al. 2020). However, fossils of modern-type Opisthocomiformes are known also from Europe and Africa and the hoatzin lineage may even originate in the Old World (Mayr 2014; Mayr & De Pietri 2014). The bird presents some unique characteristics, including wing claws in chicks and foregut fermentation, which make its systematic relationships to other birds difficult to determine. Despite hoatzin´s unusual and primitive morphology, genetic studies have shown the species is not as primitive as once thought, and it could be a very derived bird that retains (or reverted to) some plesiomorphic traits (Fain & Houde 2004; Hacket et al. 2008; Jarvis et al. 2014). Its phylogenetic position among Neornithes still constitutes one of the biggest mysteries in the avian systematics (Sibley & Ahlquist 1973, 1990; Sorenson et al. 2003; Ericson et al. 2006; Kimball et al. 2013; McCormack et al. 2013; Prum et al. 2015; Dos Santos et al. 2018; Houde et al. 2019). There have been various attempts to place it in different parts of the bird tree, but phylogenetic analyses mostly have shown low supporting values (Dos Santos et al. 2018). However, the most recent molecular phylogeny with robust statistical support placed hoatzin as the sister taxon of the Caprimulgiformes in basal landbirds clade (Kuhl et al. 2020); only future researches can confirm this position.
Despite this intriguing systematics and biology, hoatzin parasites and symbionts in general only rarely were studied. As the hoatzin´s ruminant-like digestion is unique in birds, the most attention was paid to its crop microorganism’s community structure and ecology (e.g. Godoy-Vitorino et al. 2010, 2012; Bardele et al. 2017). Haemoparasites were investigated by Renjifo et al. (1952), Gabaldon (1998), and Pacheco et al. (2019); some parasitic nematodes were studied by Renjifo et al. (1952) and Pinto and Gomes (1985). Of ectoparasites, feather lice (Mallophaga) (Kellog 1915), and feather mites (Acari) (Atyeo & Gaud 1971; Hernandes & Mironov 2015; Hernandes et al. 2017) have been recorded from this enigmatic host.
During our study of mite fauna of the hoatzin, we found a new species of the rarely collected representatives of the subfamily Fainocoptinae Lukoschus & Lombert 1979 (Acariformes: Astigmata: Analgoidea: Laminosioptidae).
Members of the subfamily Fainocoptinae are obligate viviparous parasites inhabiting the follicles of developing wing and contour feather germs. They live directly in the quill-wall or depressions on the outer surface of quills and feed on the outer layers of the non-keratinized base of the quills (Lukoschus & Lombert 1979, 1980; Skoracki et al. 2014). The presence of fainocoptines in the quill wall can cause reactions of surrounding host tissues – the feather sheath of the epidermis of the feather groove becomes activated to hyperkeratosis (Lukoschus & Lombert 1980).
The subfamily Fainocoptinae comprises 24 described species grouped in seven genera. Except for Calamicoptes Lukoschus & Lombert, 1979 and Fainocoptes Lukoschus & Lombert, 1979, all other genera (i.e. Aratingocoptes Fain & Perez, 1990a; Colicoptes Lombert & Lukoschus, 1981; Podicipedicoptes Lombert, Kethley & Lukoschus, 1979; Streetaearus Lukoschus & Lombert, 1979; Rallicoptes, 1980) are monospecific and known from single host orders (see ).
Table I. Distribution and associations of faincoptine genera with orders and families of avian hosts
Table II. Host associations and distribution of Calamicoptes species of the World
In this paper, we i) describe a new species Calamicoptes hoazinus n. sp.; ii) present a key to all known members of genus Calaminoptes, the most species-rich genus of the family; iii) summarise data on the distribution and host associations of the subfamily Fainocoptinae with orders and families of avian hosts and iv) discuss the known knowledge on hosts and habitats of sister and ancestral phylogenetic lineages related to Laminosioptidae.
Materials and methods
We examined 1 primary, 1 secondary, 2 greater wing coverts, 2 under tail coverts, 10 contour feathers of each of three hoatzin individuals deposited in the Biodiversity Institute & Natural History Museum, The University of Kansas, United States (KUNHM); 5 under- and 5 upper-tail coverts and 10 contour feathers of two individuals deposited in the Bavarian State Collection of Zoology, Munich, Germany (ZSM), and two deposited in the Alexander Koenig Research Museum, Bonn, Germany.
Before mounting, mites were softened and cleared in Nesbitt’s solution at room temperature for three days. Mites were mounted on slides in Hoyer’s medium and investigated using a light microscope (ZEISS Axioscop2+, Germany) with differential interference contrast (DIC) illumination.
In the descriptions below, the idiosomal setation follows Griffiths et al. (1990) with modifications by Norton (1998). The leg setation follows Grandjean (1941). All measurements are in micrometers. Body length was measured from the anterior margin of the gnathosoma to the posterior end. Idiosoma width was measured at the level of setae c2. Measurements of distances between idiosomal setae of different pairs refer to the distance between transverse rows formed by setal pairs.
Specimen depositories and reference numbers are cited using the following abbreviations: AMU – Adam Mickiewicz University, Poznań, Department of Animal Morphology; ZSM – Bavarian State Collection of Zoology, Munich, Germany.
Prevalence and 95% confidence interval (Sterne) were calculated with Quantitative Parasitology 3.0 (Rozsa et al. 2000; Reiczigel et al. 2019).
Results
One primary feather of one hoatzin from KUNHM was infested by laminosioptids (two females in two separate tunnels in the same quill wall); the prevalence is 33.3% (Sterne´s CI at 95% = 1.7–86.5).
Family: Laminosioptidae Vitzthum, 1931Subfamily: Fainocoptinae Lukoschus & Lombert 1979Genus: Calamicoptes Lukoschus & Lombert, 1979
Calamicoptes hoazinus n. sp.(Figures 1 and 2)
Published online:
19 December 2020Figure 1. Calamicoptes hoazinus n. sp., female: (a) – dorsal view; (b) – ventral view. Abbreviations: gw – gnathosomal wing, pw – prodorsal wing, ep – epimerites IIa
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Figure 1. Calamicoptes hoazinus n. sp., female: (a) – dorsal view; (b) – ventral view. Abbreviations: gw – gnathosomal wing, pw – prodorsal wing, ep – epimerites IIa
Published online:
19 December 2020Figure 2. Calamicoptes hoazinus n. sp., female: (a) leg I; (b) leg II; (c) leg III; (d) leg IV
![]({"type":"image","src":"/na101/home/literatum/publisher/tandf/journals/content/tizo21/2021/tizo21.v088.i01/24750263.2020.1849437/20220216/images/medium/tizo_a_1849437_f0002_b.gif"})
Figure 2. Calamicoptes hoazinus n. sp., female: (a) leg I; (b) leg II; (c) leg III; (d) leg IV
Description
Female, holotype
Total body length 680 (650 in 1 paratype), width 165 (165).
Gnathosoma
Gnathosoma ovate, densely granulated ventrally, 55 (55) long, and 55 (55) wide. Lateral extensions of pseudorutellum (gnathosomal wings) present.
Dorsal idiosoma
Dorsal and ventral striations as in Figure 1(a,b). Propodonotal shield ovate, 90 (95) long, and 70 (75) wide, with heavily sclerotized lateral and posterior margins. Setae se about 16 times longer than si and 4.1–4.6 times longer than setae cp. Short lateral wing-like protrusions (prodorsal wings) situated behind legs II and not reaching epimerites IIa. Cuticle of opisthosoma and region around bases of setae d1 and d2 smooth, intergrading into finely striated regions. Setae d2 long, c1, d1, e1, h1, f2 minute. Setae d2 3.4 times longer than cp.
Ventral idiosoma
Setae c3 and e2 subequal in length and located ventrally. Epimerites I–IV well developed. Epimerites IIa on ventral side longer than on dorsal side. Setae 4a about twice as long as setae 3a. Setae 4b 4–5 times longer than setae g. Setae g and ps3 minute. Oviporus situated at level of anterior part of epimerites III. Terminal extensions of opisthosoma absent. Anus placed subterminally, pseudanal setae ps3 situated near its anterior end. Lengths of idiosomal setae: si 20 (25), se 320 (310), c1 5 (5), c2 35 (30), c3 30 (35), cp 70 (75), d1 5 (5), d2 235 (205), e1 5 (5), e2 30 (35), h1 5 (5), h2 (450), f2 5 (5), 1a 40, 3a 35 (40), 4b 20 (25), 4a 60 (60), ps3 5 (5), g 5 (5). Distances between setal bases: se–se 85 (85), c1–c1 20 (25), c2–c2 155 (135), cp–cp 145 (140), d2–d2 90 (85), d1–d1 60 (60), h1–h1 55 (50), h1–f2 20 (15), e2–e2 120 (110), se–d2 190 (180), c1–d2 140 (125), e2–ps3 75 (70).
Legs
Tarsi I and II with two, and tarsi III and IV with one strongly sclerotized dorso-apical processes. Setae vF of femora II longer than legs II. Chaetotaxy of legs: tarsi I–IV 8–8–4–5, tibiae 1–1–1–1, genua 2–2–0–0, femora 1–1–0–0, trochanters 1–1–1–1. Solenidia ω1 on tarsi II twice as long as ω1I; solenidia σ genua I more than 3 times longer than σII; solenidia φ on tibiae III more than 5 times longer than φIV. Lengths of solenidia: ω1I 20 (20), ω3I 30 (25), φI 40 (35), σI 10 (10), ω1II 60 (60), φII 55 (50), σII short, less than 5, φIII 20 (20), φIV short, less than 5.
Male and immature stages
Not found.
Type material
Female holotype and 1 female paratype from two separate tunnels in the quill-wall of one primary feather of the hoatzin Opisthocomus hoazin (Statius Muller) (Opisthocomiformes: Opisthocomidae); PERU: Loreto Prov., Teniente Lopez, Rio Corrientes, 2°34ʹ60.0”S 76°07ʹ00.0”W, 23 July 1993, coll. D.M. Webb (host reg. no. KUNHM-87,763).
Type material deposition
The holotype is deposited in the AMU (AMU-LAMI-002, paratype in the ZSM (reg. no. ZSMA20190426).
Etymology
The name is derived from the specific name of the host.
Differential diagnosis
Among 11 species of the genus known to date, Calamicoptes hoazinus sp. n. is morphologically most similar to C. fringillae Lombert, Kethley & Lukoschus, 1979 described from Pooecetes gramineus (Gmelin) (Passeriformes: Passerellidae) from the United States (Lombert et al. 1979). In females of both species, the wing-like protrusions do not extend beyond epimerites IIa; whip-like setae se are long and extend beyond the level of setae d2, and setae d1 and g are present. The new species differs from C. fringillae by the following features: in females of C. hoazinus, the total body length is 650–680 µm; setae e2 are 30–35 µm long; setae 4b are 4–5 times longer than setae g; solenidia φ on tibiae III are more than 5 times longer than φIV. In females of C. fringillae, the total body length is 495–525 µm; setae e2 are 183 µm long; setae 4b and g are subequal in the length; solenidia φ on tibiae III and IV subequal in length.
Key to the Calamicoptes species (Females)
Setae g absent
2 – Setae g present
4 Lateral wing-like protrusions very large, 125–130 µm long
C. hymenopterus – Lateral wing-like protrusions medium-sized, about 50 µm long
3 Bases of setae d1 and d2 situated on the same transverse level
C. galli – Bases of setae d1 situated posterior to level of setal bases d2
C. monedula Setae se does not reach the level of setal bases d2. Setae d2 very short, 15 µm long
C. anatidus – Setae se reach below the level of setal bases d2. Setae d2 long, more than 100 µm long
5 Distal tip of lateral wing-like protrusions situated behind legs II not extending posteriorly below epimerites IIa
6 – Lateral wing-like protrusions situated behind legs II extending posteriorly below epimerites IIa
7 Setae e2 30–35 µm long; setae 4b 4–5 times longer than setae g. Solenidia φ on tibiae III more than 5 times longer than φIV
C. hoazinus n. sp. – Setae e2 183 µm long. Setae 4b and g subequal in length. Solenidia φ on tibiae III and IV subequal in length
C. fringillae Solenidia φII 60 µm long; φIII 4 times longer than φIV
C. meliphagae – Solenidia φII less than 35 µm long; φIII less than 2.5 times longer than φIV
8 Setae c3 14 µm long
C. zumpti – Setae c3 28–41 µm long
9 Length of setae ps3 14 µm long
C. conopophilae – Setae ps3 as microsetae 3–6 µm long
10 Leg setae vFII 106 µm. Setae 4b and g subequal in length
C. arenariae – Leg setae vFII 67 µm. Setae 4b 1.6 times longer than g
C. vanelli
Remark
The species C. lomberti Fain & Perez, 1990 is known only from males (Fain & Perez 1990b) and is not included in the above key. On the other hand, males of this species have a unique feature among Calamicoptes, i.e. lack of setae d1; taking into consideration that fainocoptines are without pronounced sexual dimorphism, this character is highly probably present also in females.
Discussion
To this day, fainocoptines were only known from primaries and wing coverts, but also body feathers of a wide spectrum of neoavian birds (Lukoschus & Lombert 1979; 1980; Fain 1981; Lombert et al. 1984; Fain & Perez 1990a, b; Skoracki et al. 2014).
Members of the genus Calamicoptes are known from the majority of zoogeographic regions (), but our finding from Peru is the first confirmation of the family Laminosioptidae in the Neotropical region. Considering the enormous avian diversity in this region (Jetz et al. 2014; Billerman et al. 2020), it would be interesting to focus on this ectoparasite group in future research.
The wide spectrum of host lineages occupied by fainocoptines and an even more extensive range of unexplored bird groups indicate that their currently described fauna is only a tip of an iceberg of their real species richness. Taking into account their life-cycle and high host specificity (all known species are monoxenous), it is possible to expect much greater diversity of this group (Costello 2016; Okamura et al. 2018).
Within the superfamily Analgoidea, the family Laminosioptidae is phylogenetically closely related to the family Dermoglyphidae (Klimov & OConnor 2013), living in cavities of feather quills of a large spectrum of bird orders - the paleognath order Tinamiformes, as well as neognath orders Anseriformes, Galliformes (= Galloanserae), Columbiformes, Coraciiformes, Passeriformes, Piciformes (= Neoaves). Dabert & Mironov (1999) suggested that both families probably originated from the ancestor living on down feathers.
It seems that the more ancestral families, e.g. Analgidae (recorded from paleognathous Apterygiformes and Tinamiformes, as well as Galloanserae and Neoaves), and Psoroptoididae (known from paleognathous Casuariformes and neognathous Neoaves) remain on down feathers while the more advanced families entered into the quills (Dermoglyphidae), or moved to the feather follicles (Laminosioptidae: Fainocoptinae) and subcutaneous layers of skin (Laminosioptidae: Laminosioptinae) during the co-evolution with their hosts (Dabert & Mironov 1999).
Considering the distribution of fainocoptines on the phylogenetic tree of their avian hosts, it is possible to expect that these mites parasitized at least the ancestor of Neognathae, as Calamicoptes, the most diversified genus (), is well established in their both clades, Galloanserae (both extant orders, Anseri- as well as Galliformes) and different neoavian orders (Charadriiformes, Columbiformes, Coliiformes, Gruiformes, Passeriformes, Podicipediformes, and Psittaciformes). It could mean that their origin is Mesozoic, as Neoaves split from Galloanseres is suggested to happen in Mid-Cretaceous, before the C-Pg boundary (Chiappe & Dyke 2002; Brusatte et al. 2015; Worthy et al. 2017).
Taken together, while morphologically more derived Fainocoptinae and Laminosioptinae are confirmed only on Neognatha, the sister clade, Dermoglyphidae, and other ancestral and more primitive analgoids like Analgidae and Psoroptoididae are associated with both extant Paleo- and Neognatha (Gaud et al. 1973; Mironov 2007; Dabert 2014). Moreover, considering a diverse assemblage of extinct Neornithes, bushy tree of Euornithes with many vanished lineages and a long evolutionary history of the feather itself (Prum 1999; Chuong et al. 2000; Sumida & Brochu 2000; Gauthier & de Queiroz 2001; Clarke et al. Zhang 2006; Xu 2006; Livezey & Zusi 2007; Hu et al. 2009; Xu et al. 2009; Zheng et al. 2009; Dimond et al. 2011; Xing et al. 2016; Kundrát et al. 2020), it seems premature to hypothesize that Laminosioptidae, including quill wall mites, evolved as late as with Neornithes.
Since we do not have any fossil evidence on Laminosioptidae and Analgoidea in general, we can base our conclusions only on indirect data. Based on the data of host associations, we can more or less assuredly state that Laminosioptidae originated on the ancestors of Neognathae. Moreover, the split into two subfamilies took place on these ancestors. The test of hypothesis of earlier laminosioptid origin, i.e. on Neornithes (meaning all extant birds), needs careful investigations of Paleognathae.
| Mite genus (N of species) | Host order and families (N of host species) | Distribution |
|---|---|---|
| Aratingocoptes Fain & Perez, 1990 (1) | Psittaciformes (Psittacidae (1)) | Mexico |
| Calamicoptes Lukoschus & Lombert, 1979 (12) | Anseriformes (Anatidae (1)); Galliformes (Phasianidae (2)); Opisthocomiformes (Opisthocomidae (1)); Charadriiformes (Charadriidae (1), Scolopacidae (1)) Passeriformes (Passerellidae (1), Corvidae (2), Dicruridae (1), Meliphagidae (2)) | see |
| Colicoptes Lombert & Lukoschus, 1981 (1) | Coliiformes (Coliidae (1)) | Namibia |
| Fainocoptes Lukoschus & Lombert, 1979 (7) | Columbiformes (Columbidae (7)) | USA, Australia, South Africa, Togo, Netherlands |
| Streetaearus Lukoschus & Lombert, 1979 (1) | Psittaciformes (Psittacidae (1)) | Australia |
| Podicipedicoptes Lombert, Kethley & Lukoschus, 1979 (1) | Podicipediformes (Podicipedidae (1)) | USA |
| Rallicoptes Lukoschus & Lombert, 1980 (1) | Gruiformes (Rallidae (1)) | Netherlands |
| Mite species | Host species | Host order/family | Locality | References |
|---|---|---|---|---|
| C. anatidus Skoracki, Kavetska, Ozminski & Zawierucha, 2014 | Aythya marila Linnaeus | Anseriformes: Anatidae | Poland | Skoracki et al. 2014 |
| C. fringillae Lombert, Kethley & Lukoschus, 1979 | Pooecetes gramineus (Gmelin) | Passeriformes: Passerellidae | United States | Lombert et al. 1979 |
| C. hoazinus sp. n. | Opisthocomus hoazin (St. Muller) | Opisthocomiformes: Opisthocomidae | Peru | Current paper |
| C. monedulae Lukoschus & Lombert, 1980 | Corvus monedula Linnaeus | Passeriformes: Corvidae | Netherlands | Lukoschus & Lombert 1980 |
| C. hymenopterus (Jones & Gaud, 1962) | Corvus brachyrhynchos Brehm | Passeriformes: Corvidae | United States | Jones & Gaud 1962; Lukoschus & Lombert 1980 |
| C. lomberti Fain & Perez, 1990 | Lagopus lagopus (Linnaeus) | Galliformes: Phasianidae | Russia | Fain & Pérez 1990b |
| C. galli Lombert, Gaud & Lukoschus, 1984 | Gallus gallus domesticus | Galliformes: Phasianidae | Morocco | Lombert et al. 1984 |
| C. zumpti Lombert, Gaud & Lukoschus, 1984 | Dicrurus adsimilis (Bechstein) | Passeriformes: Dicruridae | Botswana | Lombert et al. 1984 |
| C. arenariae Lombert, Gaud & Lukoschus, 1984 | Arenaria interpres (Linnaeus) | Charadriiformes: Scolopacidae | Morocco | Lombert et al. 1984 |
| C. vanelli Lombert, Gaud & Lukoschus, 1984 | Vanellus vanellus (Linnaeus) | Charadriiformes: Charadriidae | Morocco | Lombert et al. 1984 |
| C. meliphagae Lukoschus & Lombert, 1979 | Philemon citreogularis (Gould) | Passeriformes: Meliphagidae | Australia | Lukoschus & Lombert 1979 |
| C. conopophilae Lukoschus & Lombert, 1979 | Conopophila rufogularis (Gould) | Passeriformes: Meliphagidae | Australia | Lukoschus & Lombert 1979 |
Acknowledgements
We want to thank Mark Blair Robbins and Andrew Townsend Peterson from the Biodiversity Institute & Natural History Museum, Kansas University for the access to Birds’ collections. We also thank two anonymous reviewers for their comments which improved the manuscript substantially.
Disclosure statement
No potential conflict of interest was reported by the authors.