DOI: 10.2478/s11686-014-0229-z © W. Stefański Institute of Parasitology, PAS Acta Parasitologica, 2014, 59(2), 197–205; ISSN 1230-2821

INVITED PAPER

A new feather of the Neumannella Trouessart, 1916 (Analgoidea, Dermoglyphidae) from the Red-winged rufescens (Temminck, 1815) (Aves, Tinamiformes) with remarks to the evolution of host-parasite associations of the genus

Jacek Dabert Department of Morphology, Faculty of Biology, Adam Mickiewicz University, Umultowska 89, 61-614 Poznań, Poland

Abstract Neumannella skorackii, a new species of the family Dermoglyphidae (, Astigmata) is described from the Red-winged Tinamou Rhynchotus rufescens (Temminck, 1815) (Aves, Tinamiformes) from and a key to all known species of the genus is provided. The phylogenetic relationships (MP analysis of 25 morphological characters) between Neumannella species along with the evolutionary history of host-parasite associations revealed by Jungle reconciliation method are reconstructed. Relatively low cospeciation contribution to the recent host-parasite associations is discovered.

Keywords Quill feather ; new species; morphology; Tinamiformes; phylogenetic relationships; host-parasite associations; cospeciation

Introduction Materials and Methods

Tinamous (Tinamiformes) constitute a small of archaic The mite material was collected from the flight feather quills (less than 50 species) living in South and Central Amer- of a dry skin of the Red-winged Tinamou Rhynchotus ica and are considered as closely related to the flightless rufescens found in the collection of the Bavarian State Col- (see Gussekloo and Bout 2002, Livezey and Zusi lection of Zoology in Munich, Germany (ZSM). The mites 2007). They harbour a specific feather mite acarofauna con- were cleared and softened in lactic acid, then mounted in sisting of genera and species not found on any other or- polyvinyl lactophenol medium, and examined under a light ders (Gaud et al. 1973). microscope (Olympus BX51) with DIC illumination. The The present paper is a continuation of our previous stud- type material is deposited at the Department of Animal Mor- ies on quill inhabiting dermoglyphids of the genus Neuman- phology, AMU. The nomenclature of idiosomal chaetotaxy nella Trouessart, 1916. Here I describe a new species from follows Griffiths et al. (1990) and the leg chaetotaxy is that the museum dry skin of the Red-winged Tinamou Rhyncho- of Gaud and Atyeo (1996). All measurements are given in tus rufescens (Temminck, 1815). I present also a key for the micrometres and taken by a digital camera Olympus DP71 determination of all described species of the genus and dis- with CellˆD 2.8 software (Olympus Soft Imaging Solutions cuss the evolutionary history of the Neumannella- GmbH). The body measurements were conducted after the associations. procedure applied for Neumannella by Dabert and Skoracki

Corresponding author: [email protected] 198 Jacek Dabert

(2004). English and Latin names of birds are those of Dick- as follow: cospeciation = 0, duplication = 2, line sorting = 1, inson (2003). host switching = 3. The topology of the host tree was the one The most parsimonious tree was reconstructed applying of Bertelli and Porzecanski (2004). branch-and-bound procedure as implemented in PAUP 4 soft- ware (Swofford 2002). The analysis was conducted on 25 dis- crete morphological characters (20 of male, 5 of female) and Results six currently known Neumannella species (Appendix). As a close outgroup was used Tinamoglyphus parvus Gaud, Atyeo Neumannella skorackii sp. nov. et Berla, 1973, another dermoglyphid mite inhabiting feather quills of tinamous; as a distant outgroup was constructed fully Diagnosis homoplastic hypothetical ancestor. Five hundred bootstrap replications and Bremmer support were applied for the esti- Male: Central sclerite of prodorsal shield narrow, as wide as mation of clade stability. 1/3 distance si-si. Body ovate with rounded terminus and The reconstruction of host-parasite evolutionary history minute terminal cleft. Adanal succers with corolla stretched was done by jungle version of reconciliation method as im- posteriorly into minute spine. Tibiae I–III with apico-ventral plemented in TreeMap 2.02 software (Charleston and Page apophyses. Hysteronotal shield deeply incised anteriorly and 2002). The weights for particular cophylogenetic events were with small incision posteriorly, H-shaped. Distance d2-d2 a

Fig. 1. Male of Neumannella skorackii sp. nov. A – ventral view, B – dorsal view A new species of the feather mite genus Neumannella 199

bit shorter than distance gl-gl. Legs IV hypertrophied with tively, P/H 0.3 (0.3). Body stocky, almost ovoid. Opisthoso- tibiae and tarsi modified to big pincers. Pregenital sclerite mal terminus rounded with minute triangular cleft. Prodorsal absent. shield narrow, as wide as 1/3 of distance between setae si; Female: Width of prodorsal shield as 1/2 distance of central part with two longitudinal adjoining medial furrows. si-si; hysteronotal shield present. Setae d2 twice shorter than Scapular setae inserted on two separate ovate parts of prodor- distance between them, as long as e2. Setae ps2 short, as long sal shield. Scapular shields absent. Hysteronotal shield H- as ps1. shaped with reduced medial part and square-like incision in posterior part; exceed anteriorly the level of setae d2. All dor- Type material sal shields uniformly doted. Idiosomal setae simple, piliform. Setae si set slightly anterior to the level of se. Setae se shaped Holotype male, 9 male, 6 female, 6 TN paratypes (AMU as long macrosetae reaching the level of setae d2, setae si 01756) from quill of secondary flight feather of Rhynchotus short, not longer than distance between their bases. Long rufescens, end of 19th century, Paraguay, no other data. setae c2 inserted slightly posterior to the level of scapular setae. All hysteronotal setae shaped as long macrosetae and Description set on margins of hysteronotal shield except setae d2 and e2 that are situated on the striated tegument. Setae d2, e2, f2 and Males (Figs 1, 2): Gnathosoma nearly square, relatively ps1 of similar length, h2 and h3 very long. Distance between small, length in holotype 54 (52–56 in paratypes), width 51 setae d2-d2 slightly shorter than distance between setae e2-e2. (50–52), L/W 1.1 (1.0–1.1). Idiosoma, length 479 (475–489), Pori gl set much closer to setae e2 than to d2; distance gl-e2 width 332 (315–333), L/W 1.4 (1.5). Propodosoma and hys- about 1.5 times longer than distance e2-f2. Distances between terosoma lengths 110 (113–119) and 369 (360–370) respec- bases of dorsal setae and pori: se-se 63 (55–64), c2-c2 240

Fig. 2. Details of male of Neumannella skorackii sp. nov. A – leg I, B – leg IV, C – leg III, D – leg II, E – apical part of tarsus IV, F – genital region. AC– genital papillae, GA – genital arch, GS – genital sclerite 200 Jacek Dabert

Fig. 3. Female of Neumannella skorackii sp. nov. A – dorsal view, B – dorsal view. oviporal region A new species of the feather mite genus Neumannella 201

(223–239), se-c2 89 (83–91), d2-d2 184 (165–187), c2-d2 species are well characterised by legs IV extending by tarsi 157 (134–154), d2-gl 102 (105–114), gl-e2 30 (29–39), e2-e2 the body terminus. 198 (186–206), e2-f2 53 (54–62). Males of N. skorackii are very distinctive and easily to dis- Shields of coxal fields I, II poorly developed, lateral shields tinguish from N. apodemata and all remaining species of the of coxal fields II present. Shields of coxal fields III, IV well de- genus by the following characters: veloped and connected at inner ends making coxal fields III – N. skorackii has regularly ovate idiosoma; idiosoma is nar- closed. Pregenital sclerite absent, genital papillae and setae 3a rowing terminally in remaining species, set on striated tegument anterior to genital arch. Genital sclerite – hysteronotal shield of N. skorackii is reduced medially in elongated, triangular, encompassing bases of genital setae g form of H-shaped plate; hysteronotal shield is absent or (Fig. 3F). Genital papillae located much closer to setae 3a than shaped as narrow, longitudinal plate in remaining species, to g. Distance between levels of setae 3a and 4a approximately – ventral setae g and 4a are situated on the same transverse twice longer than distance between levels of setae 3a and g. level in N. skorackii; setae 4a are set anterior to g in re- Adanal suckers 27 (23–36) in length, 23 (17–23) in width, with maining species, posterior margin of corolla stretched as acute angle; suckers – legs III are very long and distinctly extend the tarsi of legs variable in form from nearly rounded to twice longer than wide. IV in N. skorackii; legs III do not extend terminally legs IV Tibiae of legs I and II with small apico-ventral apophyses. in remaining species. Legs III twice longer than anterior legs, reaching body termi- Females of N. skorackii and N. apodemata differ mainly in nus with medial part of tibiae and extending beyond tarsi of shape of dorsal sclerotization. In N. skorackii, the posterior legs IV. Tibiae and tarsi III with apico-ventral spines. Legs IV part of the prodorsal shield is twice narrower than the distance hypertrophied and strongly sclerotized. Complex tibia-tarsus si-si and scapular setae are set on small ovate sclerites separate IV modified into big pincers. Femur IV with flat ventral from the main shield; in N. apodemata, the posterior part of expansion. Tibia IV with relatively short and rounded apico- the prodorsal shield is enlarged and encompasses the bases of ventral apophysis and triangular apico-dorsal extension. Genu scapular setae. The hysteronotal shield in the new species is and tibia IV with dorsal crests. Setae d and e of legs IV shaped shaped as a narrow parallel-sided band; in N. apodemata, the as microsetae (Fig. 2E). hysteronotal shield is distinctly enlarged in the anterior half, Females (Fig. 3): Gnathosoma rectangular, length 57, 2–3 times wider than in the posterior part. width 56–57, L/W 1.0. Idiosoma length 413–433, width 188– 194, L/W 2.2. Propodosoma and hysterosoma lengths 105– Etymology 114 and 307–319 respectively, P/W 0.3–0.4. Body elongated, narrow with rounded terminus. Prodorsal shield narrow, sim- The new species is dedicated to Dr. Maciej Skoracki who is ilar in shape to that of male, as wide as 1/3 of distance be- the well-known expert of quill inhabiting mites (Syringophil- tween setae si. Hysteronotal shield present, shaped as idae) and my good associate for many years. longitudinal narrow band stretching from the level slightly posterior to setae c2 to the level anterior to pori gl. Copulatory Key to species of the genus Neumannella opening with inverted V-shaped sclerotization around them. All idiosomal setae piliform. Setae c2 and d2 short, not longer Males than 1/4 idiosomal width. Setae d2 set in middle distance between c2 and e2. Distance between gland openings gl and 1. Corolla of adanal suckers pyriform or with acute posterior setae e2 slightly shorter than distance e2-f2. Distances extension ...... 2. between bases of dorsal setae and pori: se-se 51–56, c2-c2 – Corolla of adanal suckers regularly rounded ...... 4. 170–173, se-c2 64–66, d2-d2 83–89, c2-d2 116–135, d2-gl 2. Pregenital apodeme encompasses genital acetabules and 89–95, gl-e2 27–29, e2-e2 104–126, e2-f2 37–38. bases of setae 3a ...... N. tinamidarum Posterior ends of paragynal sclerites of oviporus inserted – Pregenital apodeme not reaching bases of setae 3a or ab- anterior to ends of epimeres IV. Setae 3a set on level of ante- sent ...... 3. rior edge of oviporus. Setae g slightly anterior to the level of 3. Hysteronotal shield shaped as a median band narrowing an- setae 3b (Fig. 3B). Setae ps1 shorter than distance between teriorly; pregenital apodeme present; setae 4a situated far them, as long as setae ps2. posterior to setae g ...... N. tataupai – Hysteronotal shield without median part, H-shaped; pre- Differential diagnosis genital apodeme absent; setae 4a and g situated on the same transverse level ...... N. skorackii Neumannella skorackii seems to be most similar morpholog- 4. Genital sclerite shaped as a large plate encompassing setae ically to N. apodemata. Males of both species are character- g and ps3; legs IV reach the body terminus by tips of tarsi ized by short body 1–1.5 times longer than wide with rounded only ...... N. apodemata terminus, absence of the pregenital sclerite, and short setae c2, – Genital sclerite small, encompasses bases of setae g only; clearly shorter than distance between them. Females of both legs IV well extend the body terminus by tibiae ...... 5. 202 Jacek Dabert

5. Posterior part of the prodorsal shield several times narrower – Legs IV reaching body terminus by apical part of tarsi; setae than distance si-si; setae si shaped as macrosetae reaching 3b and g situated approximately on same transverse level .. 4. the body terminus ...... N. astacus 3. Distance g-4a at most twice as long as distance 3a-g – Posterior part of prodorsal shield widened, as wide as dis- ……………………………………………….... N. tataupai tance si-si; setae si short, as long as distance between them – Distance g-4a three times longer than distance 3a-g ...... N. chelifer ...... N. chelifer 4. Hysteronotal shield present ...... 5. Females – Hysteronotal shield absent ...... N. astacus 5. Posterior part of prodorsal shield encompasses setae si and 1. Apico-ventral spine on tibiae III and IV present ...... se; hysteronotal shield greatly expanded in anterior part, ...... N. tinamidarum pyriform ...... N. apodemata – Apico-ventral spine on tibiae III and IV absent ...... 2. – Setae si and se set on small sclerites separated from central 2. Legs IV reaching body terminus by basal part of tarsi; setae part of the prodorsal shield; hysteronotal shield as narrow 3b situated posterior to setae g ...... 3. band, not widened anteriorly ...... N. skorackii

Fig. 4. Optimal maximum parsimony tree for Neumannella species. Character states defining the clades and terminal are figured on the branches. Support values refer to bootstrap and Bremer index, respectively A new species of the feather mite genus Neumannella 203

Phylogenetic affinities of Neumannella skorackii and 3a placed posterior to anterior edge of oviporus, and setae ps1 cophylogenetic reconstruction of host-parasite associa- shaped as long macrosetae. Finally, the uppermost clade built tions by N. chelifer and N. tinamidarum is clearly defined by ab- sence of hysteronotal shield and shortening the setae c2 that Phylogenetic analysis yielded one most parsimonious tree are not longer than distance between them. (Fig. 4) of 30 steps (characters RI reweighted) with very good The results of cophylogenetic analysis are shown on the support of all clades and low homoplasy load (CI excluding figure 5. The parasite map shows a relatively complicated uninformative characters = 0.974). The most basal position structure of numerous cophylogenetic events concerning such occupies N. apodemata being plesiomorph to remaining limited number of taxa. The best solution in 13 less costly Jun- species by very short setae si in males and setae 3a situated an- gle results required 2 cospeciations, 7 sortings (losses), 2 du- terior to oviporus in females. The new species N. skorackii plications, and one host switching. The null hypothesis about has an intermediate position between N. astacus and remain- cospeciation as a key factor of the origin of the observed host- ing Neumannella species characterised by the following male parasite associations was not supported statistically (p = 0.9 ± synapomorphies: elongated body, presence of pregenital scle- 0.03). The first of two cospeciacions occurred in the most rite, and setae c2 shaped as macrosetae much longer than dis- basal part of the host tree between Neumannella skorackii tance between them. In this clade, the N. astacus is a sister from Rhynchotus rufescens and hypothetical Neumannella taxon to remaining species well defined by having the rounded from the ancestor of remaining tinamous. The second cospe- male body terminus with small incision and distinctive fe- ciation was much more recent and concerned the Neumannella males characterized by setae 3b situated posterior to g, setae species from the genus . The most basal event,

Fig. 5. The less costly Jungle solution for reconciled trees of tinamous (wide branches) and Neumannella species (narrow lines) 204 Jacek Dabert preceding even the first cospeciation was the duplication into References two evolutionary lineages, one undergoing numerous sortings (losses or “missing the boat”) and represented recently by only Bertelli S., Porzecanski A.L. 2004. Tinamou (Tinamidae) systemat- one species, N. apodemata, and the second line grouping all ics: a preliminary combined analysis of morphology and mol- remaining species. The second duplication took place on the ecules. Ornitologia Neotropical, 15 (Suppl.), 93–99. Charleston M.A., Page R.D.M. 2002. TreeMap (Jungle Edition). ancestor of Crypturellus and the most spectacular consequence Version 2.0.2 (Beta). http://taxonomy.zoology.gla.ac.uk/%7 of this event is the simultaneous inhabiting the same host in- emac/treemap/index.html. dividuals of C. tataupa by two different mite species, N. Dabert J. 2003. The feather mite family Syringobiidae Trouessart, tataupa and N. astacus. The sole host transfer was supposedly 1896 (Acari, Astigmata, Pterolichoidea). II. Phylogeny and either from Crypturellus cinnamomeus or from the ancestor host-parasite evolutionary relationships. Acta Parasitologica, 48 (Suppl.), 185–233. of clade C. cinnamomeus-C. soui to the clade. After Dabert J. 2005. Feather mites (Astigmata; Pterolichoidea, Analgo- switching and speciation (N. tinamidarum) no divergence on idea) and birds as models for cophylogenetic studies. new hosts took place (evolutionary inertia). Phytophaga, 14, 409–424. The real taxonomic diversity of the Neumannella species Dabert. J., Skoracki M. 2004. Two new species of the genus Neu- is most probably much greater than currently described. Pre- mannella Trouessart, 1916 (Analgoidea, Dermoglyphidae) from the Crypturellus tataupa (Temminck, liminary results of the formal cophylogenetic analysis show 1815) (Aves, Tinamiformes). Acta Parasitologica, 49, 237– low level of the evolutionary parallelism of mites with the 245. phylogenetic routes of tinamous. In comparison to several re- Dickinson E.C. (Ed.). 2003. The Howard & Moore complete check- sults of cophylogenetic analyses conducted so far for various list of the birds of the world. 3rd Edition. Christopher Helm, taxa of feather mites, including also quill inhabitants, a low London, 1039 pp. Gaud J., Atyeo W.T., Berla H.F. 1973. Acariens contribution of the cospeciation as a main cophylogenetic plumicoles parasites des tinamous. Acarologia, 14, 393–453. event driving the Neumannella evolution is rather unusual Gaud J., Atyeo W.T. 1996. Feather mites of the World (Acarina, (Dabert 2003, 2005). Probably some crucial facts concerning Astigmata): the supraspecific taxa. Musée Royal de l’Afrique the mite dispersal strategy and/or some elements of behaviour Centrale, Annales, Sciences Zoologiques, 277, 1–193 (Pt. 1, of tinamous (e.g. interspecific physical contacts) remain still text), 1–436 (Pt. 2, illustrations). Griffiths D.A., Atyeo W.T., Norton R.A., Lynch E.A. 1990. The idio- unknown. Nevertheless, drawing more general conclusions for somal chaetotaxy of astigmatid mites. Journal of Zoology, the genus Neumannella at this stage of investigation seems to London, 220, 1–32. DOI: 10.1111/j.1469-7998.1990.tb04291.x. be premature. Gussekloo S.W.S., Bout R.G. 2002. Non-neotenous origin of the palaeognathous (Aves) pterygoidpalate complex. Canadian Journal of Zoology, 80, 1491–1497. DOI: 10.1139/z02-148. Acknowledgements. I would like to thank Prof. Gerhard Haszprunar Livezey B. C., Zusi R. L. 2007. Higher-order phylogeny of modern (Director of the ZSM) for making the ornithological collection avail- birds (Theropoda, Aves: Neornithes) based on comparative able for the present study. I thank also Maciej Skoracki for sampling anatomy. II. Analysis and discussion. Zoological Journal of the mites described in this paper. the Linnean Society, 149, 1–95. DOI: 10.1111/j.1096-3642. 2006.00293.x. Swofford D.L. 2002. PAUP*. Phylogenetic Analysis Using Parsi- mony (*and Other Methods). Version 4. Sinauer Associates, Sunderland, Massachusetts. DOI:10.1234/12345678.

Received: December 9, 2013 Revised: January 1, 2014 Accepted for publication: January 31, 2014 A new species of the feather mite genus Neumannella 205

Appendix. Morphological characters applied in phylogeny reconstruction of Neumannella species. Tinamoglyphus parvus and hypothetical taxon (fully plesiomorph) used as a close and distant outgroups, respectively. Putative plesiomorph character states are coded as “0”, apo- morph states as 1,2,3. Inapplicable states are coded as “–“, missing data as “?”

1. Both sexes, setae of tarsus III: (0) 3; (1) 2. 2. Male, body L/W: (0) 1–1.5; (1) >2. 3. Male, hysterosoma shape: (0) narrowing terminally; (1) ovate. 4. Male, body terminus: (0) rounded; (1) rounded with small incision; (2) small lobes . 5. Male, adanal discs: (0) well developed; (1) rudimentar. 6. Male, adanal discs shape: (0) rounded; (1) pyriform; (2) tear-like, strongly elongated. 7. Male, pregenital sclerite: (0) absent; (1) present. 8. Male, shape of pregenital sclerite: (0) encompassing genital acetabules and bases of 3a; (1) encompassing only genital acetabules; (2) extending anteriorly the setae 3a. 9. Male, genital sclerite: (0) absent; (1) present. 10. Male, shape of genital sclerite: (0) encompassing setae g; (1) a big plate encompassing setae g and ps3. 11. Male, hysteronotal shield: (0) present; (1) absent. 12. Male, shape of hysteronotal shield: (0) single central plate; (1) reduced medially, H-shaped plate. 13. Male, posterior part of pronotal shield: (0) encompassing setae se; (1) as wide as si-si distance; (2) at least twice narrower than si-si distance; (3) several times narrower than si-si distance. 14. Male, legs IV: (0) extend the body terminus; (1) reach the body terminus. 15. Male, setae si: (0) much shorter than distance between them; (1) as long as distance between them or slightly longer; (2) reaching setae d2; (3) reaching body terminus. 16. Males, setae c2: (0) shorter than distance between them; (1) as long as distance between them; (2) distinctly longer than distance between them. 17. Males, setae g and 4a: (0) 4a anterior to g; (1) on one level. 18. Males, apico-ventral spines on tibiae I–II: (0) absent; (1) present. 19. Male, apico-ventral spine of tibia IV: (0) long, sharp; (1) short, rounded; (2) long, rounded. 20. Male, length of legs III: (0) extending IV; (1) not extending IV. 21. Female, setae 3b and g: (0) 3b and g on similar level; (1) 3b posterior to g. 22. Female, apico-ventral spine on tibiae III–IV: (0) absent; (1) present. 23. Female, legs IV: (0) extending the terminus; (1) reaching the terminus. 24. Female, anterior edge of oviporus and setae 3a: (0) 3a anterior to the edge; (1) 3a posterior to the edge; (2) 3a at the level of the edge. 25. Female, setae ps2: (0) as short as ps1, piliform; (1) macrosetae.

Character # Species 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 N. chelifer 0 1 0 1 0 0 1 1 1 0 1 – 1 0 1 1 0 0 0 1 1 0 0 1 0 N. tinamidarum 0 1 0 1 0 1 1 0 1 0 1 – 1 0 1 1 0 0 0 1 ? 1 0 ? 1 N. tataupai 0 1 0 1 0 2 1 2 1 0 0 0 1 0 2 2 0 0 0 1 1 0 0 1 1 N. astacus 0 1 0 2 1 0 1 0 1 0 0 0 3 0 3 2 0 1 0 1 0 0 0 2 0 N. apodemata 0 0 0 0 1 0 0 – 1 1 0 0 0 1 0 0 0 1 2 1 0 0 1 0 0 N. skorackii 0 0 1 0 0 1 0 – 1 0 0 1 2 0 1 0 1 1 1 0 0 0 1 2 0 T. parvus 1 0 0 0 0 0 0 – 0 – 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 hypothetical 0 0 0 0 0 0 0 – 0 – 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0