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Feather mites (Acariformes: Astigmata) of the brown noddy, Anous stolidus (L.) (Charadriiformes: Laridae), with description of two new species from Brazil

Akashi Hernandes, Fabio 1 and Brito, Guilherme R. R. 2

1✉ Departamento de Ecologia e Zoologia, CCB/ECZ, Trindade, Universidade Federal de Santa Catarina, 88040-970 - Florianópolis, SC, Brazil & CNPq-Brazil Researcher.
2Departamento de Ecologia e Zoologia, CCB/ECZ, Trindade, Universidade Federal de Santa Catarina, 88040-970 - Florianópolis, SC, Brazil.

2022 - Volume: 62 Issue: 2 pages: 317-331

https://doi.org/10.24349/rblu-98ly
ZooBank LSID: 9BE80328-4846-4217-B2EE-43BA05D6A3A4

Original research

Keywords

Neotropics systematics taxonomy ectoparasites seabird Anoinae Alloptidae Syringobiidae Xolalgidae

Abstract

We inspected feather mites (Acariformes: Astigmata) associated with the brown noddy, Anous stolidus stolidus (Linnaeus), for the first time in the Southern hemisphere. Three feather mites are herein reported, including two new species: Alloptes (Sternalloptes) hidasii sp. nov. (Analgoidea: Alloptidae), Analloptes tintinnabulus sp. nov. (Analgoidea: Xolalgidae), and Grenieria bicaudata Dabert & Atyeo, 1997 (Pterolichoidea: Syringobiidae). The latter species was originally described from a different subspecies of this host in Hawaii.


Introduction

The brown noddy, Anous stolidus (Linnaeus, 1758) (Charadriiformes: Laridae), is a tropical seabird, resembling terns in general appearance. This highly pelagic species wanders in tropical waters searching for food, often small fish and squid taken by hover and contact dipping. Distributed in pantropical marine areas – with the true extent of marine occurrence unknown – it is seldom seen close to shore away from breeding areas, with few published records of vagrant individuals in NE and SE Brazil. The nest sites are on land with highly variable substrates: bare rock, sand, gravel, soil, vegetation such as tree branches, base of palm fronds, cacti, grass, and tree leaves (Simpson and Simpson 2010; Pereira et al. 2015; Chardine et al. 2020).

Implemented by Cracraft (2013), the arrangement of Laridae in five subfamilies included Anous Stephens, 1826 in a separate subfamily Anoinae Bonaparte, 1854. Relationships with the remaining Laridae indicate Anoinae as the most basal lineage within the family (Baker et al. 2007). Even with the scarceness of published records and museum specimens of this bird from the Brazilian coastline, a fair number of records are present in citizen science portals (e.g. Wikiaves and eBird), with most presence in more tropical latitudes. Subtropical records are rare, with only four records found – two in Wikiaves (Farias 2019a; Kerber 2019), two in eBird (Soares 2017; Farias 2019b – one of them redundant making the total number of historical localities only three: Florianópolis and Bombinhas in Santa Catarina State and Rio Grande in Rio Grande do Sul State).

To this date, the only feather mite (Acariformes: Astigmata) described from the brown noddy is Grenieria bicaudata Dabert & Atyeo, 1997 (Pterolichoidea: Syringobiidae), from Anous stolidus pileatus (Scopoli, 1786) from Hawaii (Dabert and Atyeo 1997).

In Brazil, feather mites were previously reported from only two birds of the order Charadriiformes: five species from the southern lapwing, Vanellus chilensis (Molina, 1782) (Charadriidae) (Pedroso et al. 2015) and three species from the white-rumped sandpiper, Calidris fuscicollis (Vieillot, 1819) (Scolopacidae) (Gomes et al. 2015). Since there are 92 charadriiform birds occurring in Brazil (Pacheco et al. 2021), certainly many more feather mites remain to be described and reported from these hosts.

In this study, we report feather mites on the brown noddy (nominal) for the first time in the Southern Hemisphere, including the description of two new species.

Materials and methods

The bird was found stranded in Praia do Campeche, Florianópolis/SC in 27 Feb 2021 very weakened and taken to the rehabilitation center managed by the NGO ''Associação R3 Animal'' for stabilization and treatment. It died after a few days and was donated to the Federal University of Santa Catarina for scientific study due to the scarcity and importance of the register – as far as we know, this is the first specimen to this date ever collected in Santa Catarina State.

The mites were collected from a brown noddy skin removed from the carcass by GB with the ruffling technique described by Gaud and Atyeo (1996). In laboratory, the mites found on a tray were picked up with a fine brush and cleared in 30% lactic acid for 24h at 50ºC, and finally mounted on microscope slides using Hoyer's medium (Krantz and Walter 2009). After drying and heating for 5 days at 50ºC, the slides were sealed with transparent varnish and labeled. The specimens were studied with an Olympus CX31 microscope and illustrations were prepared from pictures of the mites (Omax A35140U 14mpx camera attached to ocular lenses) using Adobe Illustrator CS5 and a Wacom Bamboo Create tablet. The chaetotaxies of idiosoma and legs follow Griffiths et al. (1990) and Atyeo and Gaud (1966), respectively, with corrections for coxal setae proposed by Norton (1998). Type specimens are deposited at the Department of Ecology and Zoology of the Universidade Federal de Santa Catarina (ECZ–UFSC).

Taxonomy

Superfamily Analgoidea Trouessart & Mégnin, 1884

Family Alloptidae Gaud, 1957

Subfamily Alloptinae Gaud, 1957

Genus Alloptes Canestrini, 1879

Subgenus Sternalloptes Mironov, 1992 (in: Kivganov and Mironov 1992)

Type species: Pterocolus bisetatus Haller, 1882, by original designation.

The subgenus Sternalloptes currently comprises 21 species, including the new species described below (Haller 1882; Trouessart 1885; Dubinin 1951, 1952; Gaud 1957, 1960, 1976; Mironov 1991; Vasyukova and Mironov 1991; Kivganov and Mironov 1992; Mironov and Kivganov 1993; Kivganov 1996; Han et al. 2021). These mites are associated with birds of the order Charadriiformes (Lari: Laridae, Stercorariidae) (Choe and Kim 1989; Muzaffar and Jones 2005; Dabert et al. 2015; Gomes et al. 2015; Tomás et al. 2018; Han and Min 2019; Mironov and Hernandes 2020; Seniczak et al. 2020; Han et al. 2021), with a few questionable records on Procellariiformes (Dubinin 1949). Mites of this subgenus are characterized by the following combination of features: in both sexes, seta mG of genu II is tooth-like with blunt apex (Figs. 3B, F) and idiosomal setae e1 are absent; in males, the posterior end of opisthosoma is widened, and in females, setae f2, ps1, and ps2 are absent.

Alloptes (Sternalloptes) hidasii Hernandes & Brito sp. nov.

ZOOBANK: 81105099-16FD-4955-808A-27B890012B87

(Figs. 1–4)

Figure 1. Alloptes (Sternalloptes) hidasii sp. nov. (Alloptidae) male habitus: dorsal (A) and ventral (B) views.

Figure 2. Alloptes (Sternalloptes) hidasii sp. nov. (Alloptidae) female habitus: dorsal (A) and ventral (B) views.

Figure 3. Alloptes (Sternalloptes) hidasii sp. nov. (Alloptidae): male legs I–IV (A–D), female legs I–IV (E–H), dorsal view of opisthosoma of male (I) and female (J).

Figure 4. Alloptes (Sternalloptes) hidasii sp. nov. (Alloptidae) microphotographs: male habitus (A), ventral views of anterior (B) and posterior idiosoma (C); female habitus (D), ventral views of anterior (E) and posterior (F) idiosoma.

Type material — Holotype male, paratypes 2 females ex Anous stolidus stolidus (Linnaeus, 1758) (Charadriiformes: Laridae), CAUFSC00389, Praia do Campeche, Florianópolis, Santa Catarina, Brazil (lat -27.6893423, long -48.4811854), 27. Feb. 2021, R3 Animal col.

DescriptionMale (Holotype) (Figs. 1, 3A–D, I, 4A–C). Idiosoma size, length × width, 297 × 137. Prodorsal shield: posterior margin sinuous, surface without ornamentation, greatest length 58, width of posterior part 67, distance between setae se 71. Length of hysterosoma from sejugal furrow to bases of setae h2 215. Distance between prodorsal and hysteronotal shields along midline 18. Hysteronotal shield (Fig. 1A): greatest length from anterior end to bases of setae h2 201, width at the very anterior margin 42, anterior margin concave, anterolateral corners blunt-angular, lateral margin with small incision at the level of trochanters III, setae d2 posterior to these incisions, surface without ornamentation. Subhumeral setae c3 thin spiculiform, 11 in length; seta cp 100 in length. Opisthosoma hourglass-shaped, with constriction at level of femoragenu IV, width at level of this constriction 22, greatest width of posterior end 42; length of interlobar septa 63. Terminal lamella with three pairs of smooth-edged festoons. Setae h2 whip-like without noticeable enlargement in basal half, greatest width 4. Setae h3 absent, setae ps2 greatly reduced. Distance between dorsal setae: c2:c2 103, c2:d2 44, d2:e2 110, h2:h2 21.

Epimerites I fused into a Y, sternum about half the total length of epimerites, with narrow sclerotized areas; epimerites II straight, coxal fields II roughly rectangular in shape, almost closed. Coxal fields III open, coxal fields IV closed. Length of genital apparatus 17, width 13. Pregenital sclerite Y-shaped, connecting inner ends of epimerites IIIa and apex of paragenital arch. Adanal shields split into pairs of anterior comma-shaped pieces and posterior longitudinal pieces. Coxal setae 4b and 3a roughly at the same transverse level, pseudanal setae ps3 and coxal setae 4a at the same level (Fig. 1B). Setae 4a on the striated tegument, setae ps3 on small comma-shaped sclerites (anterior pieces of adanal shields). Posterior pieces of adanal shields flanking adanal suckers laterally. Adanal suckers 9 in diameter, distance between centers of discs 18. Distance between ventral setae: 4a4a 27, 3ag 23, gps3 30.

Seta mG of genu I spine-like, straight, with acute apex; seta mG of genu II stout, tooth-like with bluntly rounded apex (Fig. 3B). Solenidion σ of genu III subequal in length to tibia III. Solenidion φ of tibia III subequal to corresponding tarsus and ambulacrum combined. Length of legs from anterior margin of trochanter to tip of ambulacrum: leg III 152, leg IV 196. Length of solenidia: σI 27, σII 8, σIII 29, φI 56, φII 73, φIII 43, φIV 60, ω1I 23, ω3I 37, ω1II 71.

Female (Range for 2 paratypes) (Figs. 2, 3E–H, J, 4D–F). Idiosomal size, length × width, 389–393 × 114–117. Prodorsal shield as in the male, length 68–70, width of posterior part 59–63; distance between setae se:se 68–69. Hysteronotal shield: anterior margin convex, surface without ornamentation, greatest length from anterior margin to level of setae h3 271–287, width of anterior part 56–57 (Fig. 2A, B). A pair of small lateral sclerites present at level of trochanters IV. Setae c3 thin spiculiform 10–11. Setae e1, f2, ps1, ps2, ps3 absent; setae h1 and e2 approximately at the same transverse level. Distance between prodorsal and hysteronotal shields along midline 20–22. Opisthosomal lobes strongly elongated, with long and acute membranous extensions, sclerotized part of lobes about 3 times longer than wide at base. Terminal cleft a narrow U, length from tip of membranous apex to the anterior end roughly at the level of setae h2 96–101. Distance between dorsal setae: c2:d2 56–57, d2:e2 100–102, e2:h2 66–69, h2:h3 53–58, h2:h2 41–42, h3:h3 22–23. Supranal concavity circular, separated from terminal cleft. Coxal fields I, II as in the male. Epigynum bow-shaped, length × width, 15–17 × 40–44 (Fig. 2B). Legs I, II as in the male. Length of solenidia: σI 30–36, σII 10–11, σIII 29–31, φI 50–50, φII 65–66, φIII 17–18, φIV 15–19, ω1I 16–17, ω3I 25–26, ω1II 35–37.

Differential diagnosis — The new species is most similar to Alloptes (Sternalloptes) leptolobus Gaud, 1976 described from Sternula albifrons (Pallas, 1764) (Laridae) in having the opisthosomal lobes of females strongly elongated, 3 or more times longer than wide. Alloptes (St.) hidasii sp. n. can be distinguished in having the following features: in males, the adanal shields are split into two pieces, the pregenital sclerite is Y-shaped, and setae h2 are whip-like, without any enlargement; and in females, the anterior end of the terminal cleft slightly surpasses the level of the setae h2, setae h1 and e2 are arranged in a transverse row, and a pair of small lateral sclerites are present at the level of trochanters IV. In males of A. (St.) leptolobus, the adanal shields are entire, shaped as an inverted L, the pregenital sclerite is V-shaped, and setae h2 are enlarged and flattened at their midlength; in females, the terminal cleft barely reaches the level of setae h2, setae h1 are distinctly anterior to the level of setae e2, and lateral sclerites are absent.

Etymology — The species is named after the recently deceased naturalist José Hidasi (1929–2021). Ifjú Vitéz Hidasi József Péter was born in Hungary, arrived in Brazil soon after the WWII, and adopted a Brazilian name, seeking his dream to become a naturalist in the tropics. He started with a professional bond and friendship with Helmut Sick (1910–1991), the German naturalist, and assisted him in the Central Brazil expeditions of Fundação Brasil Central. Hidasi never left the region, settling down in Goiânia (Goiás State) fulfilling his dream and becoming a very prolific and competent naturalist, gathering specimens for several institutions and collections, natural history exhibitions and assembling what would become the Ornithological Museum of Goiânia (Perotti 2005; Dornas 2009).

Family Xolalgidae Dubinin, 1953

Subfamily Ingrassiinae Gaud & Atyeo, 1981

Genus Analloptes Trouessart, 1885

Type species: Analloptes megnini Trouessart, 1885, by original designation.

Analloptes currently comprises 14 species, including the new one described herein. Their host associations are among the most diverse of all feather mite genera, with species recorded from quite distantly related taxonomic groups of birds (Prum et al. 2015; Feng et al. 2020): hornbills (Bucerotiformes: Bucerotidae), rails and trumpeters (Gruiformes: Rallidae, Psophiidae), ibises (Pelecaniformes: Threskiornithidae), ospreys (Accipitriformes: Pandionidae), buttonquails (Charadriiformes: Turnicidae), and passerines (Passeriformes: Corvidae, Conopophagidae, Tyrannidae) (Trouessart 1885; Berlese 1886; Canestrini and Kramer 1899; Gaud 1980, 1982; Gaud and Atyeo 1981; Atyeo and Gaud 1984; Mironov 1997; Mironov and Hernandes 2014; Mu et al. 2016; Valdebenito et al. 2018). A number of undescribed species have also been reported from limpkins (Gruiformes: Aramidae) (Gaud and Atyeo 1981), passerines (Cotingidae, Furnariidae, Grallariidae) (Barreto et al. 2012), jacamars (Galbuliformes: Galbulidae) (Enout et al. 2012), and cormorants (Suliformes: Phalacrocoracidae) (FAH pers. obs.). The new species is the first one described from the bird Order Charadriiformes in the Western hemisphere.

Analloptes tintinnabulus Hernandes & Brito sp. nov.

ZOOBANK: 0DE79C05-6DC6-4D96-B229-92D5253AF88D

(Figs. 5–7)

Figure 5. Analloptes tintinnabulus sp. nov. (Alloptidae) male habitus: dorsal (A) and ventral (B) views.

Figure 6. Analloptes tintinnabulus sp. nov. male legs in dorsal view: trochanter–tarsus I (A), II (B), genu, tibia, and tarsus III (C), tibia and tarsus IV (D).

Figure 7. Analloptes tintinnabulus sp. nov. male, microphotographs: habitus (A), dorsal view of anterior idiosoma (B), and ventral view of opisthosoma (C).

Type Material — Holotype male and 1 paratype male ex Anous stolidus stolidus (Linnaeus, 1758) (Charadriiformes: Laridae), (CAUFSC00389), Praia do Campeche, Florianópolis, Santa Catarina, Brazil (lat -27.6893423, long -48.4811854), 27 Feb. 2021, R3 Animal col.

DescriptionMale (holotype, range for 1 paratype in parentheses) (Figs. 5–7). Length of idiosoma 331 (342), greatest width 158 (155), length of hysterosoma 235 (240). Prodorsal shield: longitudinal plate slightly enlarged posteriorly, occupying median part of prodorsum, posterior margin convex, reaching the level of scapular setae se, surface smooth, greatest length 65 (66), greatest width roughly at level of se 21 (25) (Fig. 5A). Setae ve absent. Scapular setae se 84 (81), bases separated by 53 (56); setae si on striated tegument. Scapular shields narrow, inner margin slightly convex, surface smooth, without suprategumental extension. Humeral shields small; seta c2 situated on inner margin of this shield. Setae c3 short filiform, much shorter than trochanters III, setae cp long whip-like, similar in length to idiosoma width. Hysteronotal shield: anterior margin slightly concave, moderately darkened, with two lateral finger-like projections arising near bases of setae d1, longitudinally split in two halves by long and wide incision occupying median area of hysteronotum and almost reaching the anterior margin of shield; length of the shield from anterior end to bases of setae h3 206 (222), width at anterior margin 74 (79), width including lateral finger-like extensions 101 (114), surface smooth. Anterior area of incision between the levels of setae d1 and e1 with longitudinal striae. Dorsal setae c1, h1 absent. Length of setae: d2 23 (27) and e2 32 (33). Opisthosomal lobes long, almost parallel, with a pair of roughly oval lightly sclerotized areas between bases of setae f2 and ps1. Interlobar membranes extending from level of trochanter IV onto lobar apices, with rounded terminal extension beyond lobar apices bearing setae h3, overlapping each other inside terminal cleft, except small median longitudinal ellipsoid void anterior to level of setae f2. Surface of interlobar membranes with several widely spaced striae on distal halves. Distances between dorsal setae: c2:c2 138 (140), c2:d2 53 (56), d2:e2 66 (72), e2:h3 75 (78), f2:f2 81 (90), ps1:ps1 45 (50), h3:h3 51 (61), h2:h2 65 (74).

Epimerites I fused into a Y (Fig. 5B), sternum about ¼ of total length of epimerites I. Coxal fields I–III open. Inner ends of epimerites IIIa with short irregular sclerotized plate. Coxal fields IV closed, inner ends of epimerites IIIa and corresponding bases epimerites IVa connected by oblique long rib-like sclerite. Epimerites IV fused with pregenital apodeme in a high arch-shaped structure. Genital apparatus small, situated at level of trochanters III. Genital papillae situated at level of genital apparatus and setae 4a. Genital and adanal shields absent. Genital setae g minute, situated posterior to level of setae 4a. Setae 4b situated on inner ends of epimerites IIIa. Setae ps3 situated on striated tegument. Setae 3a, 4a, and 4b short filiform, not exceeding length of trochanters III. Adanal suckers 16 (16) in diameter, surrounding membrane with radiate striation. Distance between ventral setae: 4b:4b 44 (42), 4b:3a 9 (10), 4b:g 51 (55), g: ps3 25 (27).

Legs III thin, legs IV more robust than other legs. Tarsus I without apico-dorsal extension; seta wa much shorter than ra. Tarsus II with small apico-dorsal extension near base of seta d, solenidion ω1on medium-sized dorsal hump. Tarsi I, II with two rounded ventral expansions between seta wa and base of tarsal stalk. Tibia I, II with spine-like ventral processes. Tarsus III excluding ambulacrum 52 (54) long. Tarsus IV 78 (86) long, with small extension bearing base of seta r, setae d, e reduced to alveoli (Fig. 6D). Length of legs III and IV excluding ambulacra 161 (159) and 227 (222), respectively. Length of solenidia: σ I 48 (50), σII 20 (21), σIII 31 (29), φI 68 (63), φII 84 (92), φIII 60 (62), φIV 86 (94), ω1I 23 (26), ω3I 38 (38), ω1II 55 (61).

Female unknown.

Differential diagnosis — The new species is close to Analloptes psophiae (Trouessart and Neumann, 1888) described from Psophia crepitans Linnaeus (= Psophia agami) (Gruiformes: Psophiidae) by the similar shape of male lobes, with overlapping interlobar lamellae with largely spaced striae. It differs from the latter species, however, in a number of features. In males, the anterior corners of the hysteronotal shield near bases of setae d1 have two short finger-like extensions pointing postero-laterally, the longitudinal incision in the hysteronotal shield almost reaches the anterior margin of the shield, setae cp are similar in length to idiosoma width, seta c2 is much shorter than se (about 1/5 its length), solenidion σ on genu I is as long as genu + tibia combined, solenidion ω3 on tarsus II about 1.5 times the length of the segment. In males of A. psophiae, the anterior extensions on the hysteronotal shield are long and fused with metapodosomal sclerites, the longitudinal incision in the hysteronotal shield does not reach the anterior margin of the shield, setae cp are large spiculiform, about ¼ the distance between their bases, seta c2 are about as long as seta se, solenidion σ on genu I is about 1/3 the length of tibia alone, and solenidion ω1 on tarsus II is shorter than the tarsus.

Etymology — The specific name is derived from tintinnabulum (L. small bell.), adjective, masculine. The species name is an allusion to the adornments and pendants – small bells – possessed by the court jesters employed to entertain noblemen from the Medieval and Renaissance times. The scientific name of the host can be translated as characteristics often attributed to court jesters (G. Anous = stupid, foolish; L. stolidus = stupid, foolish) (Jobling 2010).

Superfamily Pterolichoidea Trouessart & Mégnin, 1884

Family Syringobiidae Trouessart, 1897

Genus Grenieria Gaud & Mouchet, 1959

Type species: Pterolichus simplex Trouessart, 1886, by original designation.

Seven Grenieria species have been described, all associated with terns (Charadriiformes: Laridae: Sterninae) (Dabert and Atyeo 1997). The only two species previously reported in the Neotropics are G. simplex (Trouessart, 1886) from Sterna forsteri Nuttal, 1834 in Mexico, and G. phaetusae from Phaetusa simplex (Gmelin, 1789) in Paraguay; the remaining Grenieria species are known only from the Northern hemisphere (Dabert and Atyeo 1997; Dabert 2003).

Grenieria bicaudata Dabert & Atyeo 1997

(Fig. 8)

Figure 8. Grenieria bicaudata Dabert & Atyeo 1997 (Syringobiidae) microphotographs: male (A–C) habitus (A), prodorsal region (B), and opisthosomal region (C); female habitus (D), ventral views of genital area (E), and opisthosoma (F).

Material examined — 9 males, 5 females ex Anous stolidus stolidus (Linnaeus, 1758) (Charadriiformes: Laridae), (CAUFSC00389), Praia do Campeche, Florianópolis, Santa Catarina, Brazil (lat -27.6893423 long -48.4811854), 27 Feb. 2021, R3 Animal col.

Remarks — This species was described from Anous stolidus pileatus (Scopoli, 1786) from Hawaii (Dabert and Atyeo 1997), and until this date remained the only feather mite reported from terns of the genus Anous Stephens. Grenieria bicaudata is herein reported for the first time after the original description. Syringobiids are normally found inside the quills, but may eventually be found outside of their normal habitat (e.g. Phyllochaeta spp., Gaud and Atyeo 1996). The specimens reported herein were found on the surface of the feathers, rather than inside the quills.

Acknowledgements

The authors thank the NGO ''Associação R3 Animal'' (Florianópolis, Brazil) for donating the deceased specimen of the brown noddy for scientific study.



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Date received:
2021-12-22
Date accepted:
2022-03-09
Date published:
2022-03-11

Edited by:
Auger, Philippe

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2022 Akashi Hernandes, Fabio and Brito, Guilherme R. R.
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