Complementary Description of Africoseius Lativentris and Placement of Africoseius in Podocinidae (Acari, Mesostigmata) Based on Molecular and Morphological Evidences

Complementary description of Africoseius lativentris and placement of Africoseius in Podocinidae (Acari, Mesostigmata) based on molecular and morphological evidences

Authors: Rueda-Ramírez, Diana, Santos, Jandir C., Sourassou, Nazer Famah, Demite, Peterson R., Puerta-González, Andrés, et al. Source: Systematic and Applied Acarology, 24(12) : 2369-2394 Published By: Systematic and Applied Acarology Society URL: https://doi.org/10.11158/saa.24.12.7

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Downloaded From: https://bioone.org/journals/Systematic-and-Applied-Acarology on 17 Jun 2020 Terms of Use: https://bioone.org/terms-of-use Access provided by University of Guelph Systematic & Applied Acarology 24(12): 2369–2394 (2019) ISSN 1362-1971 (print) http://doi.org/10.11158/saa.24.12.7 ISSN 2056-6069 (online)

Article http://zoobank.org/urn:lsid:zoobank.org:pub:C2228554-2382-4207-915C-4D76994B1C77 Complementary description of Africoseius lativentris and placement of Africoseius in Podocinidae (Acari, Mesostigmata) based on molecular and morphological evidences

DIANA RUEDA-RAMÍREZ1,*, JANDIR C. SANTOS2, NAZER FAMAH SOURASSOU3, PETERSON R. DEMITE4, ANDRÉS PUERTA-GONZÁLEZ5 & GILBERTO J. DE MORAES6 1 Departamento de Entomologia e Acarologia, ESALQ-Universidade de São Paulo, Avenida Pádua Dias, 11, 13418-900 Piracicaba, São Paulo, Brazil. Present address: Facultad de Ciencias Agrarias, Universidad Nacional de Colombia, Car- rera 30 No. 45-03, Edificio 500, Bogotá, Colombia. 2 CNPq Researcher, Departamento de Entomologia e Acarologia, ESALQ-Universidade de São Paulo, 13418-900 Piraci- caba, São Paulo, Brazil. Present address: Centre for Diversity Genomics, 50 Stone Road East, University of Guelph, Guelph, Ontario, N1G 2W1, Canada. 3 Departamento de Entomologia e Acarologia, ESALQ-Universidade de São Paulo, Avenida Pádua Dias, 11, 13418-900 Piracicaba, São Paulo, Brazil. Present address: Institut Supérieur des Métiers de l’Agriculture, Université de Kara, BP. 404, Kara, Togo 4 Instituto de Ciências Exatas e Tecnologia, Universidade Federal do Amazonas, UFAM, Itacoatiara, Amazonas, Brazil. Present address: Programa de Pós-Graduação em Zoologia, Instituto de Biociências, Universidade Federal do Mato Grosso, UFMT, Cuiabá, Mato Grosso, Brazil. 5 Universidad de Antioquia, Medellín, Colombia. 6 CNPq Researcher. Departamento de Entomologia e Acarologia, ESALQ-Universidade de São Paulo, Avenida Pádua Dias, 11, 13418-900 Piracicaba, São Paulo, Brazil. *Corresponding author: e-mail: [email protected]

Abstract

Morphological details of specimens collected from several localities in Brazil and identified as Africoseius lativentris (Karg 1982) are provided. The taxonomic position of Africoseius Krantz, 1962 has been debated over the years, with repeated changes in its familial placement. A phylogenetic study based on 18S and 28S rDNA sequences of the Brazilian population of A. lativentris collected at Jaboticabal, São Paulo State, and similar data of 70 taxa representing 11 families of Gamasina indicated that Africoseius is a member of the well-supported Podocinidae (sensu Lindquist et al. 2009) clade. The main morphological similarities and differences between Africoseius and the group of species until now placed in Podocinidae sensu Lindquist et al. (2009) are listed. Apomorphic characteristics uniting those taxa include the hypotrichous condition of tibia I (eight and nine setae instead of ten or more in other free-living Gamasina) and the insertions of av2 and pv2, considerably more distal on tarsi II and III than in the majority of the free-living Gamasina. Within Podocinidae, a new subfamily, Africoseiinae, is proposed, based on uniquely apomorphic characteristics of the setae ad4 and pd4 (sensu Evans 1969) of tarsi II–IV absent, and setae av4 and pv4 of same basitarsi long, incurved and close to each other and to a posterior longitudinal extension of the peripodomeric suture and on the attenuated form of the lateral (rather than the medial) hypostomatic setae. This subfamily is currently represented by Africoseius areolatus Krantz and Africoseius lativentris (Karg 1982), while all other presently known species of the family are now placed in the subfamily Podocininae.

Keywords: Taxonomy, 18S rDNA, 28S rDNA, Parasitiformes, phylogeny

Introduction

Specimens mostly found in litter and plants from different sites of northeastern, central and southern Brazil have been identified as Africoseius Krantz, 1962. Two species are considered to belong to this

Downloaded From: https://bioone.org/journals/Systematic-and-Applied-Acarology on 17 Jun 2020 Terms of Use: https://bioone.org/terms-of-use Access provided by University of Guelph genus, the type species, Africoseius areolatus Krantz, 1962, and Africoseius americanus Karg & Schorlemmer, 2009. Africoseius was described by Krantz (1962) from Africa and later reported fr o m B r a z i l , M e x i c o , Paraguay, USA and Venezuela (Lindquist & Evans 1965; Karg 1982; Karg & Schorlemmer 2009). In the original description, Africoseius was placed in Aceosejidae Baker & Wharton (= Ascidae sensu Evans & Lindquist 1965). Upon a re-examination of specimens from Mexico and the USA as well as of some of the primary types from Africa, Lindquist and Evans (1965) added other descriptive aspects not mentioned in the original description of Africoseius and not shared with other ascid mites (sensu Lindquist & Evans 1965), removing it from that family and considering it to constitute “a separate subfamily within a broadened concept of Podocinidae sensu Westerboer 1963”. Halliday et al. (1998) also considered Africoseius not to be a member of Ascidae, without referring it to another family. The familial affiliation of this genus remains uncertain. Karg & Schorlemmer (2009) placed Africoseius in Podocinidae, but their concept of Podocinidae is different from the concept of Lindquist et al. (2009). DNA sequences have been increasingly used in mite taxonomy. The nuclear ribosomal genes 18S and 28S have been considered useful for resolving high level phylogeny in mites (Black et al. 1997; Cruickshank & Thomas 1999; Otto & Wilson 2001; Cruickshank 2002; Dowling & OConnor 2010; Matsuda et al. 2014; Famah-Sourassou et al. 2015). The use of molecular tools could provide insights to help the proper placement of Africoseius at the family level. The objective of this paper is to provide morphological details of Brazilian specimens identified as A. lativentris and to discuss the familial placement of Africoseius based on morphological and molecular evidences.

Materials and methods

Determination of Brazilian Africoseius and their morphology Collection data of the specimens, all females, considered in this study are: Alagoas State: two from litter, Arapiraca (09° 68' 0.5'' S, 36° 66' 07.1'' W), 24 March 2012, J.C. Santos (accession numbers MZLQ17271 and MZLQ17272). Goiás State: one from leaf of Caryocar brasiliense A.St.-Hil. (Caryocaraceae), Urutaí (17º 28' S, 48º 12' W), 18 February 2015, P.R. Demite (accession number MZLQ17273); one from leaf of Virola sebifera Aubl. (Myristicaceae), Urutaí (17º 24' S, 48º 11' W), 20 June 2015, P.R. Demite (accession number MZLQ17274). Rio Grande do Sul State: one from leaf of Myrciaria plinioides D. Legrand (Myrtaceae), Lajeado (29º 26' S, 51º 57' W), 04 December 2012, P.R. Demite (accession number MZLQ17275). Santa Catarina State: one from leaf of unidentified Myrtaceae, Serra do Quiriri (26° 01’ S, 48° 57’ W), Garuva, 03 April 2013, P.R. Demite (accession number MZLQ17276); one from moss on a dead wood, Serra do Quiriri (26° 01’ S, 48° 57’ W), Garuva, 03 April 2013, J.C. Santos (accession number MZLQ17277). São Paulo State: three from litter at the base of Guarea guidonia (L.) Sleumer (Meliaceae), Jaboticabal (21° 14' 24'' S, 48° 17' 17'' W), 07 August 2013, 10 September 2013 and 24 August 2016, J.C. Santos (accession numbers MZLQ17278, MZLQ17279 and MZLQ17280); two from leaves of Eugenia ramboi D. Legrand (Myrtaceae), Estação Ecológica de Caetetus (22º 41' S, 49° 10' W), Gália, 11 July 2012, P.R. Demite (accession numbers MZLQ17281 and MZLQ17282); one from litter, São Pedro, 16 February 2000, A.R. Oliveira (accession number MZLQ16102); one from soil, Piracicaba, May 16 2000, A.R. Oliveira (accession number MZLQ16098); one from litter, Luiz Antônio, 26 July 2000, A. R. Oliveira (accession number MZLQ16100).

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Downloaded From: https://bioone.org/journals/Systematic-and-Applied-Acarology on 17 Jun 2020 Terms of Use: https://bioone.org/terms-of-use Access provided by University of Guelph All specimens are deposited at Departamento de Entomologia e Acarologia, Escola Superior de Agricultura “Luiz de Queiroz”, Universidade de São Paulo, Piracicaba, São Paulo State. The collection sites are far apart from each other, the distance between the northern and southern extremes being about 3500 km. All specimens mounted in Hoyer’s medium for examination under phase (Leica, DMLB) and differential interference (Nikon, Eclipse, 80i) contrast microscopy. In addition to the Brazilian specimens, the holotype female and four paratype females of A . americanus as well as four specimens identified by W. Karg as Neojeordensia lativentris Karg, 1982 were also examined. Based on the information provided on the slides and in the original description, it was assumed that one of N. lativentris specimens was the holotype female, another was a paratype female and the remaining were not types; these will be so treated subsequently in this publication. The type specimens of A. americanus were collected from the soil 50 km north of Asunción, Paraguay, by I. Loksa, 1966 (Karg´s accession number 70153–58 and Museum für Naturkunde Berlin accession number ZMB Kat. Nr. 44890–95). According to the original description, the holotype of N. lativentris was collected from a nest of Turdus species in Cabreuva [São Paulo State, Brazil], by K. Lenko, 05 July 1970, (Karg´s accession number 4604 and Museum für Naturkunde Berlin accession number ZMB Kat. Nr. 42491). The paratype was collected in Venezuela, but other details are not given in the original description. As indicated on the slide, it was collected by Prof. Balogh, 1973, from soil (Karg collection number 4605 and Museum für Naturkunde Berlin collection number ZMB Kat. Nr. 42492). Two additional females of this species were collected from Barueri, São Paulo State, by K. Lenko on 25 July 1971, from bird nest (C. rufipes [sic]) (Karg collection number 4602 and 4603 and Museum für Naturkunde Berlin collection number ZMB Kat. Nr. 42489 and 42490). A female of an undescribed Africoseius species from Australia was also examined; this was collected from rainforest canopy with pyrethrum fogging at Far North Queensland, near Cape Tribulation (16º 04' S, 145º 28' E), by D.E. Walter, unspecified date of collection. Type material of A. areolatus could not be located, because the institute where it was deposited (Institute of National Parks of the Belgian Congo and Ruanda-Urundi) is no longer in operation. The specimens could also not be located at the Royal Museum of Central Africa (Tervuren) or the Royal Museum of Natural Sciences (Brussels), to which different specimens from the deactivated institute were transferred. Taxonomically relevant structures of the mites were illustrated with a camera lucida attached to the phase contrast microscope and a digital camera connected to the differential interference contrast microscope. Drawings and photos were processed with a digital tablet, using the Adobe Illustrator® program. Measurements were performed with the use of a graded eyepiece. Details of tarsus and pretarsus were observed and photographed with a scanning electron microscope (Scanning Electron Microscope, Model: LEO 435 VP). Lengths of the shields refer to the maximum distance between the anterior and posterior margins along midline, whereas widths of the shields refer to their maximum width, except for the sternal shield, for which width was taken at level of coxae II. Length of the epigynial shield includes the anterior hyaline region; length of the legs refers to distance between base of the coxa and tip of the tarsus (excluding pretarsus). Length of the fixed cheliceral digit refers to the distance between the dorsal cheliceral lyrifissure and the apex. For each character, the average measurement followed (in parentheses) by the respective minimum and maximum measurements of the Brazilian specimens collected in this study, and the minimum and maximum measurements of type specimens of A. americanus and N. lativentris are given in micrometers. Idiosomal setal notation is based on Lindquist and Evans (1965) and Lindquist (1994). Leg setal notation, chaetotactic formulae and chaetotaxy types are based on Evans (1969). The term “pore” in the description refers to gland pores and the term “lyrifissure” indicates a cuticular proprioreceptor structure, based on Athias-Henriot

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Downloaded From: https://bioone.org/journals/Systematic-and-Applied-Acarology on 17 Jun 2020 Terms of Use: https://bioone.org/terms-of-use Access provided by University of Guelph (1971, 1975). The system of mite classification follows Lindquist et al. (2009), with alternative names for higher categories used by Beaulieu et al. (2011) given in parenthesis.

Morphological comparison of genera An evaluation of all original descriptions as well as redescription of Podocinidae species and an examination of specimens of Podocinum Berlese, 1882a and Podocinella Evans & Hyatt, 1958, genera placed in Podocinidae by Lindquist et al. (2009), were conducted to compare the morphological characteristics of those taxa with Africoseius. All specimens of Podocinum and Podocinella examined in this study were collected from litter and soil; other collection data are as follows: Podocinum pacificum Berlese, 1895: Cundinamarca Department, Colombia: one female, “Granja El Porvenir” (4° 34’ 33.2” N, 74° 18’ 08.5” W), Soacha, 3 July 2016, D. Rueda-Ramírez. São Paulo State, Brazil: one female from litter, Piracicaba, 05 April 1999, J.L.C. Mineiro (accession number MZLQ17150); two females from litter at the base of Euterpe edulis Mart. (Arecaceae), Piracicaba, 7 February 2000, A.R. Oliveira (accession numbers MZLQ17146 and MZLQ17147); one female from litter, São Pedro, 01 April 2000, A.R. Oliveira (accession number MZLQ17148). Podocinum bengalensis Bhattacharyya, 1968: Mato Grosso State, Brazil: three females, Sinop, 21 March 2016, E.P.J. Britto (accession numbers MZLQ17136, MZLQ17137 and MZLQ17138). São Paulo State, Brazil: two females, São Pedro, 16 February 2000, A.R. Oliveira (accession numbers MZLQ17144 and MZLQ17145); two females, Luiz Antônio, 26 January 2000, A.R. Oliveira (accession numbers MZLQ17139 and MZLQ17140). Podocinum sagax (Berlese, 1882b): São Paulo State, Brazil: two females and one m a l e , Jaboticabal, 12 December 2012, J.C. Santos (accession numbers MZLQ17167, MZLQ17168 and MZLQ17170); four females and two males, Piracicaba, 10 November 2013, J.C. Santos (accession numbers MZLQ17163, MZLQ17164, MZLQ17165, MZLQ17166, MZLQ17153 and MZLQ17154). Podocinum tupinamba Santos, Martin, Britto & Moraes, 2017: São Paulo State, Brazil: holotype female and five paratype females, Leme, 7 February 2000, A.R. Oliveira (accession numbers TMZLQ3392, TMZLQ3397, TMZLQ3400, TMZLQ3369, TMZLQ3393 and TMZLQ3395). Podocinella misella (Berlese, 1913): São Paulo State, Brazil: two females, Jaboticabal (21° 14' 24'' S, 48° 17' 17'' W), 27 November 2013, J.C. Santos (accession numbers MZLQ17268 and MZLQ17269). Alagoas State, Brazil: one female, Teotônio Vilela, 12 February 2014, J.C. Santos (accession number MZLQ17270).

Phylogenetic study Sequences of 18S and 28S rDNA were obtained from two Africoseius specimens collected by J.C. Santos on 24 August 2016 from litter at Universidade do Estado de São Paulo (UNESP), Jaboticabal, São Paulo State, Brazil (voucher specimen MZLQ17280). DNA was extracted using the DNeasy Blood and Tissue Kit (Qiagen, Hilden, Germany), while PCR amplification and sequencing were carried out using the same primers and protocols described in Famah Sourassou et al. (2015). The sequences were submitted to GenBank database. Seventy sequences of 18S and 28S rDNA of mesostigmatic mites of the cohort (infraorder sensu Beaulieu et al. 2011) Gamasina of the suborder Monogynaspida available in the GenBank database in January 2016 were used in this study (See Table 1 for GenBank Accession numbers and voucher specimens). Those were sequences obtained by Dowling and OConnor (2010) and Famah-Sourassou et al. (2015), who used their data to assess the phylogeny of selected mite families within the subcohort (hyporder sensu Beaulieu et al. 2011) Dermanyssiae. Two of the sequences referred to species of Parasitidae (subcohort Parasitiae of Gamasina) were used as outgroups. The remaining species represented 11 families presently placed in the subcohort Dermanyssiae.

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Family Species Voucher collection GenBank Accession Number number 18S rDNA 28S rDNA ASCIDAE Asca sp.1 MZLQ15646d KM979609 KM979664 Asca sp.2 MZLQ15647d KM979610 KM979665 Asca sp.3 MZLQ15648d KM979611 KM979666 Asca sp.4 MZLQ15649d KM979612 KM979667 Protogamasellus sp. MZLQ1568d KM979614 KM979669 Gamasellodes sp. MZLQ15652d KM979615 KM979670 Protogamasellus mica (Athias-Henriot, 1961) MZLQ15651d KM979616 KM979671

Antennoseius sp. MZLQ15653d KM979617 KM979672 Protogamasellus sigillophorus Mineiro, Lindquist & Moraes, 2009 MZLQ15654d KM979660 KM979715

Gamasellodes adrianae Walter, 2003 AD256e FJ911809 FJ911744 Andregamasus sp. AD303e FJ911812 FJ911747 MELICHARIDAE Proctolaelaps bickleyi (Bram, 1956) MZLQ15639d KM979627 KM979682 Proctolaelaps belemensis Fain, Hyland & Aitken, 1977 MZLQ15641d KM979629 KM979684

Proctolaelaps sp.1 MZLQ15640d KM979628 KM979683 Proctolaelaps sp.2 MZLQ15644d KM979631 KM979686 Proctolaelaps sp.3 MZLQ15645d KM979632 KM979687 Proctolaelaps sp.4 MZLQ15671d KM979657 KM979712 Proctolaelaps sp. AD290e FJ911811 FJ911746 Tropicoseius sp. MZLQ15643d KM979633 KM979688 Spadiseius sp. MZLQ15670d KM979634 KM979689 Melicharidae sp. MZLQ15642d KM979630 KM979685 AMEROSEIIDAE Neocypholaelaps ampullula (Berlese, 1910) MZLQ6495d KM979654 KM979709 Neocypholaelaps sp. AD595e FJ911807 FJ911742 Ameroseius sp. AD129e FJ911806 FJ911741 BLATTISOCIIDAE Aceodromus convolvuli Muma, 1961 MZLQ15655d KM979618 KM979673 Blattisocius everti Britto, Lopes & Moraes, 2012 TMZLQ2839d KM979619 KM979674

Blattisocius tarsalis (Berlese, 1918) MZLQ15657d KM979620 KM979675 Cheiroseius sp. MZLQ15656d KM979621 KM979676 Lasioseius floridensis (Berlese, 1916) MZLQ15634d KM979622 KM979677 Lasioseius sp.1 MZLQ15635d KM979623 KM979678 Lasioseius sp.2 MZLQ15636d KM979624 KM979679 Lasioseius sp.3 MZLQ15637d KM979625 KM979680 Lasioseius sp. AD281e FJ911810 FJ911745 Platyseius sp. MZLQ15638d KM979626 KM979681 PHYTOSEIIDAE Macrocaudus multisetatus Moraes, McMurtry & Mineiro, 2003 MZLQ15672d KM979635 KM979690

Amblyseius swirskiia Athias-Henriot, 1962 MZLQ6494d KM979636 KM979691 Amblyseius tamatavensis Blommers, 1974 MZLQ15673d KM979637 KM979692 Amblyseius largoensis (Muma, 1955) MZLQ15674d KM979638 KM979693 Neoseiulus tunus (De Leon, 1967) MZLQ15675d KM979639 KM979694 Phytoseiulus macropilis Banks, 1905 MZLQ15676d KM979640 KM979695

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Downloaded From: https://bioone.org/journals/Systematic-and-Applied-Acarology on 17 Jun 2020 Terms of Use: https://bioone.org/terms-of-use Access provided by University of Guelph TABLE 1. (Continued) Family Species Voucher GenBank Accession Number collection 18S rDNA 28S rDNA number Amblydromalus limonicus (Garman & McGregor, 1956) MZLQ15677d KM979641 KM979696 Euseius concordis (Chant, 1959) MZLQ15678d KM979642 KM979697 Neoseiulus barkeri (Hughes, 1948) MZLQ15679d KM979643 KM979698 Propioseiopsis sp. MZLQ15660d KM979659 KM979714 Neoseiulus anonymus (Chant & Baker, 1965) MZLQ15680d KM979658 KM979713 Arrenoseius sp.b AD172e FJ911814 FJ911749 Amblyseius sp. AD551e FJ911815 FJ911750 PODOCINIDAE Podocinium sp. MZLQ15668d KM979653 KM979708 Podocinum sp.1 AD374e FJ911816 FJ911751 Podocinum sp.2 AD266e FJ911817 FJ911752 Africoseius lativentris* (Karg, 1982) MZLQ17280* MH142254* MH142255* RHODACARIDAE Protogamasellopsis zaheric Abo-Schnaf, Castilho & Moraes, 2013 MZLQ15658d KM979648 KM979703 Rhodacarellus sp. MZLQ15663d KM979661 KM979716 Rhodacarus sp. AD376e FJ911833 FJ911768 DIGAMASELLIDAE Dendrolaelaps sp. MZLQ15666d KM979649 KM979704 Dendrolaelaspis sp. MZLQ15665d KM979650 KM979705 Dendrolaelaps sp.1 AD170e FJ911826 FJ911761 Dendrolaelaps sp.2 AD254e FJ911827 FJ911762 Digamasellus sp. MZLQ15667d KM979651 KM979706 OLOGAMASIDAE Neogamasellevans sp. MZLQ15664d KM979652 KM979707 Gamasiphis sp. AD261e FJ911832 FJ911767 Gamasellus discutatus (Lee, 1966) AD260e FJ911831 FJ911766 Eupicrius sp. AD258e FJ911829 FJ911764 LAELAPIDAE Cosmolaelaps jaboticabalensis Moreira, Klompen & Moraes, 2014 TMZLQ2938d KM979644 KM979699 Stratiolaelaps scimitus (Womersley, 1956) MZLQ15681d KM979645 KM979700 Androlaelaps sp. MZLQ15661d KM979646 KM979701 Pseudoparasitus sp. MZLQ15659d KM979647 KM979702 Gaeolaelaps sp. MZLQ15662d KM979663 KM979718 MACROCHELIDAE Glyptholaspis sp. MZLQ2400d KM979655 KM979710 PARASITIDAE Pergamasus sp. AD138e FJ911803 FJ911738 Poecilochirus sp. AD120e FJ911802 FJ911737 UNKNOWN Zygoseius sp. MZLQ15669d KM979656 KM979711

a Named as Typhlodromips swirskii in GenBank b Named as Fundiseius sp. in GenBank c Named as Protogamasellopsis posnaniensis in GenBank and Castilho et al. (2009) d Previously published data in Famah-Sourassou et al. (2015) e Isolate number. Previously published data in Dowling and OConnor (2010) *Sequence obtained in this study

The 18S and 28S sequences were aligned using the multiple alignment program ClustalW2 (Larkin et al. 2007), with default alignment parameters. Alignments were then checked and refined manually using AliView 3.0 [GPLv 3] (Larsson 2014) (TreeBase submission ID 22534). Datasets of the 18S and 28S genes were combined into a single data matrix as in Famah- Sourassou et al. (2015) and Dowling and OConnor (2010). Phylogenetic trees were constructed using Bayesian and Maximum Likelihood (ML) methods. Both analyses were run under the best-fit models, according to the Akaike Information Criterion (AIC), calculated using jModelTest v2.1.6 (Dariba & Posada 2012). The preferred model for the data was the GTR+Γ+I.

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Downloaded From: https://bioone.org/journals/Systematic-and-Applied-Acarology on 17 Jun 2020 Terms of Use: https://bioone.org/terms-of-use Access provided by University of Guelph Bayesian analysis was performed with the aid of MrBayes version 3.2.6 (Ronquist et al. 2012). Four parallel runs of four heated Markov chains were processed for 10 million generations, with likelihood scores printed every 100 generations. Runs were terminated when the standard deviation of split frequencies was <0.01 (0.0084292). The first 25% of the trees were discarded as burn-in, and the remaining 75% of the trees were used to construct consensus tree with Bayesian posterior probabilities. Maximum Likelihood (ML) analysis was performed with RAxML version 8.2.9 (Stamatakis 2014). The ML search for the best-scoring ML tree was calculated from 100 RaxML runs followed by 1000 bootstrap replicates to assess statistical support under the GTR+Γ+I. Well-supported clades refer to supported relationships between taxa based on high values of Bayesian posterior probabilities and Bootstrap frequencies (Erixon et al. 2003). Softwares used in the analysis were run through Linux systems.

Results Determination of the Brazilian Africoseius populations and their morphology The examination of the Brazilian Africoseius specimens and a comparison with literature information and type material led us to identify them as A. lativentris. Details about their morphology and other taxonomic considerations are subsequently provided.

Africoseius lativentris (Karg, 1982) Neojeordensia lativentris Karg 1982: 70. Africoseius lativentris.—Halliday et al. 1998: 46. Africoseius americanus.—Karg & Schorlemmer 2009: 63 (syn. nov.)

Adult female (Figures 1–19)

Diagnosis Epistome divided by two transverse lines into a distal narrower section, a basal broader section and an intermediate section; in some specimens, basal section more sclerotized than others. Podonotal region of dorsal shield with short, wavy, transverse to diagonal lines, with 21 pairs of setae (j1 and z1 absent), each inserted on a tubercle (tubercles discreet for anteromedial setae); setae aciculate and smooth. Opisthonotal region of dorsal shield with a network of rounded to polygonal ornamentation elements, with 19 pairs of setae, each inserted on a tubercle; most setae smooth (always R series, but some to all setae of J, Z and S series from smooth to distinctly barbed). Lyrifissure iv5 posterolaterad of st5, on epigynal shield; peritreme distally abutting peritreme of the opposite side (in some specimens, peritreme recurved posteroventrally, but still abutting each other; in others recurved anteriorly); setae ad4 and pd4 (sensu Evans 1969) of tarsi II-IV absent, and setae av4 and pv4 of same tarsi long, incurved and inserted close to each other and to a posterior longitudinal extension of the peripodomeric suture.

Etymology The name Africoseius is a combination of the term “Africo”, which refers to Africa from where the type specimen of A. areolatus, type species of the genus, was collected (G.W. Krantz, pers. communication), and “seius”, a Roman surname used by authors to form names for genera of Mesostigmata. The specific name lativentris most certainly refers to the broad ventrianal shield of this species.

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Downloaded From: https://bioone.org/journals/Systematic-and-Applied-Acarology on 17 Jun 2020 Terms of Use: https://bioone.org/terms-of-use Access provided by University of Guelph Complementary description (based on 15 newly collected Brazilian specimens, and measurements of type specimens) Gnathosoma (Figures 1–5). Chelicera with spine-like dorsal seta, dorsal and antiaxial lyrifissures distinct (Figure 1); arthrodial process of chelicera shaped as a coronet-like fringe; fixed digit with one tooth in addition to apical hook (subapical offset “Gabelzahn” seemingly absent) and a setiform pilus dentilis inserted on a lobe; movable digit long, with two teeth in addition to apical hook. Epistome divided by two transverse lines into a distal narrower section, a basal broader section and an intermediate section; in some specimens, section posteriad of basal most transverse line more sclerotized than elsewhere (Figure 2). Palp chaetotaxy holotrichous (trochanter–tibia): 2-5-6-14; palp tarsus with two subterminal setae distinctly longer than other setae (Figure 3); apotele two-tined and with a tiny protuberance at the base (Figure 4). Deutosternal groove delimited by subparallel lateral lines, with five distinct transverse lines each bearing two distinct denticles (rarely 3–4); in some specimens, with an additional discreet distal and/or proximal smooth transverse line; corniculus horn-like, reaching nearly midlevel of palp femur; setae h2 inserted slightly anteriad of h3 (Figure 5). Measurements shown in Table 2.

FIGURE 1–5. Africoseius lativentris. Brazilian females. 1. Antiaxial view of chelicera; 2. Epistome; 3. Palp tibia and tarsus; 4. Apotele; 5. Hypostome and proximal palp segments. Dorsal idiosoma (Figures 6–8). Podonotal and opisthonotal shields fully fused. Podonotal region of dorsal shield with short, wavy, transverse to diagonal lines, with 21 pairs of setae (j2-j6, z2-z6, s1-s6 and r2-r6); seven pairs of distinguishable lyrifissures and four pairs of distinguishable pores. Opisthonotal region of dorsal shield with a network of rounded to polygonal ornamentation elements, with 19 pairs of setae (J1-J5, Z1-Z5, S1-S5, R1-R4), nine pairs of distinguishable lyrifissures and two pairs of distinguishable pores. All podonotal setae aciculate and smooth, each inserted on a tubercle (tubercles discreet anteriad of z5). Opisthonotal setae smooth (all R setae, but some to all setae of J, Z and S series from smooth to distinctly barbed; Figures 7–8), each inserted on a tubercle (Figures 6–7). Lyrifissure idR3 (= Rp) distinguishable ventrolaterally. Measurements shown in Table 2.

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Downloaded From: https://bioone.org/journals/Systematic-and-Applied-Acarology on 17 Jun 2020 Terms of Use: https://bioone.org/terms-of-use Access provided by University of Guelph TABLE 2. Length of dorsal idiosomal and gnathosomal setae and other structures of Brazilian specimens identified as Africoseius lativentris (Karg, 1982), the holotype, a paratype and two additional specimens of the same species (identified by Karg as Neojordensia lativentris) and the holotype and paratypes of Africoseius americanus Karg & Schorlemmer, 2009; mean (minimum–maximum); - = seta absent; all specimens adult female.

Brazilian Africoseius Type material and additional specimens Type material of Africoseius Structures lativentris of Africoseius lativentris americanus (n = 13) (n = 4) (n = 5) Fixed digit 35 (31–37) 30–35 37–43

Movable digit 36 (32–37) 32–34 35–40

Corniculus length 26 (24–27) 21–23 25–28

Corniculus width at base 11 (10–13) 12 13–14

h1 32 (29–35) Not visible 35–37

h2 32 (30–35) Not visible 33–35

h3 21 (16–25) Not visible 20–23

sc 29 (22–35) Not visible 32–32

Dorsal shield length 431 (390–470) 430–490 412–428 Dorsal shield width at widest 346 (320–371) 330–460 320–338 point j2 22 (20–26) 23–25 25–26

j3 30 (25–33) 32–35 25–28

j4 30 (25–32) 30–35 26–28

j5 31 (27–32) 31–33 25–26

j6 31 (30–35) 32–34 31–33

J1 40 (37–41) 40 39–43

J2 43 (40–49) 47–60 42–44

J3 44 (41–48) 45–58 43–45

49 (40–54) 54–63 46–48 J4 J5 50 (40–55) 60–66 43–46

z2 31 (24–37) 30–31 30–34

z3 34 (25–38) 33–36 29–30

z4 34 (24–38) 31–35 30–35

z5 30 (28–33) 28–30 27–30

z6 40 (35–43) 32–36 35–38

Z1 44 (41–47) 45–55 42–46

Z2 49 (46–53) 47–65 45–48

Z3 52 (45–56) 56–65 46–49

Z4 54 (49–60) 60–75 45–50

Z5 82 (70–97) 65–81 69–73

s1 28 (22–33) 22–28 26–28

s2 24 (20–28) 21–30 18–20

s3 33 (26–38) 31–35 34–35

s4 36 (30–40) 35–39 33–36

s5 39 (33–43) 32–38 38–39

s6 42 (37–46) 37–48 44–45 ...... continued on the next page

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Downloaded From: https://bioone.org/journals/Systematic-and-Applied-Acarology on 17 Jun 2020 Terms of Use: https://bioone.org/terms-of-use Access provided by University of Guelph TABLE 2. (Continued) Brazilian Africoseius Type material and additional specimens Type material of Africoseius Structures lativentris of Africoseius lativentris americanus (n = 13) (n = 4) (n = 5) S1 41 (38–45) 35–50 40–44

S2 44 (42–47) 37–50 43–45

S3 51 (45–57) 55–65 53–55

S4 66 (57–72) 55–60 69–70

S5 78 (65–94) 65–68 70–83

r2 22 (19–28) 21–25 18–21

r3 34 (24–40) 27–35 40–41

r4 36 (31–40) 31–35 35–38

r5 40 (33–42) 32–39 38–40

r6 43 (35–47) 35–39 42–46

R1 44 (38–48) 41–45 44–45

R2 42 (35–46) 41–50 44–45

R3 43 (35–48) 41–47 45–48

R4 47 (33–50) 43–46 45–48

FIGURE 6–8. Africoseius lativentris. Brazilian females. 6. Dorsal view of idiosoma; 7. Variation on dorsal setae; 8. Photography of variation on some barbed-like dorsal setae.

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Downloaded From: https://bioone.org/journals/Systematic-and-Applied-Acarology on 17 Jun 2020 Terms of Use: https://bioone.org/terms-of-use Access provided by University of Guelph FIGURE 9–13. Africoseius lativentris. Brazilian females. 9. Tritosternum; 10. Ventral idiosoma; 11. Variation of posterior margin of sternal shield; 12. Dorsal view of anterior section of peritreme; 13. Spermathecal apparatus. Lyrifissures and pores enlarged for improved visibility. Abbreviations: in = infundibulum, sc = sacculus, sp.d = sperm duct, t = tubulus.

Ventral idiosoma (Figures 9–11). Whole tritosternum inserted between a pair of presternal platelets; separated section of laciniae corresponding to about 50% of total length of tritosternum, pilose (base of tritosternum only distinguishable in one specimen, ca. 17 [11–15] long and ca. 11 [9– 10] wide proximally, Figure 9–10). Sternal shield striate (Figure 10); posterior margin slightly concave (with two transverse clefts posterolaterad of st3 in about 10% of the specimens examined, Figure 11); with three pairs of setae and two pairs of lyrifissures; with prominent endopodal projections between coxae I and II (pore gst1 indistinct); distance st3–st3 shorter than st2–st2. Setae st4 on metasternal platelets (third pair of lyrifissures, iv3, absent). Anterior section of endopodal plate fused with sternal shield; section behind sternal shield reduced to an undulate strip between posterior margin of coxae II and almost to posterior margin of coxae III. Epigynal shield with

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Downloaded From: https://bioone.org/journals/Systematic-and-Applied-Acarology on 17 Jun 2020 Terms of Use: https://bioone.org/terms-of-use Access provided by University of Guelph longitudinal and diagonal striae; anterior hyaline region rounded, not reaching posterior margin of sternal shield; posterior region slightly convex, extending well behind coxae IV, distinctly broadened posteriad of st5; lyrifissure iv5 posterolaterad of st5, on posterolateral edges of epigynal shield. Metapodal platelets incorporated as discernible sigilla in expanded ventrianal shield (a pair of punctate ellipsoidal anterolateral regions). Pore gvb absent. Ventrianal shield covering most of opisthogaster, bearing all six pairs of opisthogastric setae (Jv1–Jv2, Jv4–Jv5 and Zv2–Zv 3) in addition to circumanal setae, all of which smooth and sharp tipped; para-anal setae inserted well anteriad of anterior margin of anal opening and slightly shorter than post-anal seta; with one pair of pores between Zv2 and Jv4 and one pair of marginal lyrifissures anteriad of Zv3. Anal opening small, about 1/8 of shield length. Unsclerotised cuticle laterad of ventrianal shield with two pairs of lyrifissures. Exopodal plate distinct, in some specimens with discreet interruptions at level between coxae III and IV. Measurements shown in Table 3.

TABLE 3. Length of ventral idiosomal setae, legs and other structures of Brazilian specimens identified as Africoseius lativentris (Karg, 1982), the holotype, a paratype and two additional specimens of the same species (identified by Karg as Neojeordensia lativentris) and the holotype and paratypes of Africoseius americanus Karg & Schorlemmer, 2009; mean (minimum–maximum); mean (minimum–maximum); - = seta absent; all specimens adult female.

Brazilian Africoseius Type material and additional specimens of Type material of Structures lativentris Africoseius lativentris Africoseius americanus (n = 13) (n = 4) (n = 5) Entire tritosternum 83 (80–85) 78–82 80–85 Sternal shield length at mid-line 52 (48–55) 49–51 45–50 Sternal shield width between coxae II 101 (94–109) 95–97 82–85 and III Epigynal shield length 98 (87–105) 83–90 95–103 Epigynal shield width at the widest 120 (93–140) 121–125 120–130 level distance st5-st5 74 (65–82) 76–80 72–79 Ventrianal shield length 170 (144–195) 168–175 170–200 Ventrianal shield width at widest level 257 (212–285) 256–273 270–290 Anal opening length 21 (19–24) 18–19 17–20 st1 17 (15–20) 16–18 13–17 st2 18 (15–20) 15–16 13–17 st3 17 (16–18) 15–17 10–15 st4 22 (21–26) 18–21 15–18 st5 18 (16–20) 16–20 15–17 Jv1 18 (15–20) 17–18 16–18 Jv2 17 (14–21) 15–16 13–15 Jv4 19 (18–21) 18–20 18–20 Jv5 29 (24–32) 24–25 20–25 Zv2 18 (15–22) 15–18 15–16 Zv3 22 (19–25) 22–23 19–20 Para–anal 21 (19–22) 20–23 17–20 Post–anal 32 (29–38) 30–33 22–30 Leg I 293 (285–300) 261–290 243–290 Tarsus I 79 (73–83) 82–85 75–80 Leg II 305 (290–315) 258–270 290–320 Leg III 292 (266–310) 263–288 275–300 Leg IV 338 (320–360) 300–335 320–360 Peritreme and peritrematic plate (Figures 6, 10, 12). Peritreme extending anteriorly to level beyond j2, distally abutting peritreme of the opposite side in 44% of the specimens examined; distal

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Downloaded From: https://bioone.org/journals/Systematic-and-Applied-Acarology on 17 Jun 2020 Terms of Use: https://bioone.org/terms-of-use Access provided by University of Guelph end of peritreme curved anteriorly or posteroventrally in respectively 19 and 37% of the specimens examined (Figure 1k). Peritrematic plate wide, broadly fused anteriorly with dorsal shield, fused posteriorly with exopodal plate laterad of coxa IV; with a lyrifissure and a pore next to coxa III and with two lyrifissures (ips and ip3) and a pair of pores (gp3) posteriad of stigma, gv2 on posterior edge of shield behind coxae IV. Spermatheca (Figure 13). Consistently with what was described by Lindquist & E v a n s ( 1 9 6 5 ) , laelapid-type, and to what was described by Athias-Henriot (1968), type A6-Ascidae (no evidence of a sclerotized calyx and a minor duct); insemination pore (solenostome) apparently located at inner posterior margin at base of coxa IV; infundibulum sometimes distinct, followed by an elongate and slightly curved sclerotized structure (tubulus or canal adducteur, sensu Athias-Henriot 1968) whose outer end is spoon-like and whose inner end is undifferentiated and close to the one from other side, seemingly attached to a globular structure followed by a smaller pouch to which it is connected by a flaring duct (sacculus with sperm duct apparently leading to receptaculum); sclerotized structures seemingly surrounded by a large membranous saccular structure. Legs (Figures 14–19). Measurements shown in Table 3. Setae ad4 and pd4 (sensu Evans 1969) of tarsi II-IV absent, and setae av4 and pv4 of same tarsi long, incurved and close to each other and to a posterior longitudinal extension of the peripodomeric suture (Figures 15–17). All legs with acute, smooth setae; macrosetae absent. Chaetotaxy of legs I–IV: coxae: 0-0/1 0/1-0, 0-0/1 0/1-0, 0- 0/1 0/1-0, 0-0/1 0/0-0; trochanters: 1-0/1 0/1-1, 1-0/1 0/1-1, 1-0/1 0/1-1, 1-0/1 0/1-1; femora: 2-1/2 1/1-2, 2-2/1 2/2-1, 1-2/1 1/0-1, 1 2/1 1/0-1; genua: 1-2/1 2/1-1, 1-2/0 2/0-1, 1-2/0 2/0-1, 1-2/0 2/0-0; tibiae: 1-2/1 2/1-1, 1-1/1 2/1-1, 1-1/1 2/1-1, 1-1/1 2/1-1; tarsi: ~28 (Figure 18), 18, 18, 18 (ad1 and pd1 tiny, inconspicuous, Figure 19).

FIGURE 14–17. Africoseius lativentris. Brazilian females. 14. Leg I; 15. Leg II; 16. Leg III; 17 Leg IV.

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FIGURE 19. Africoseius lativentris. Brazilian females. a. Dorso-distal view of tarsus II and detail of pretarsus; b. Scanning Electron Microscope photo of dorso-distal section of tarsus II, with pretarsus removed; c. Scanning Electron Microscope photo of latero-distal section of tarsus IV and pretarsus.

Most leg segments hypotrichous, as subsequently specified: trochanter I without pv2 and d; trochanters II–IV without pv2; femur I differing from type X chaetotaxy sensu Evans (1963) chaetotaxy by missing ad2 and pd2 and by having an extra pl (pl2) seta (probably due to a change in the accommodation of the setae by an area where another setae is absent); femur II with type Xa; genu I differing from type X by missing al2 and pl2; genu II differing from type VII by missing al2;

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Downloaded From: https://bioone.org/journals/Systematic-and-Applied-Acarology on 17 Jun 2020 Terms of Use: https://bioone.org/terms-of-use Access provided by University of Guelph genu III with type VI; genu IV differing from type VI by missing av1; tibia I differing from type X by missing al2 and pl2; tibia II differing from VII by having one antero-dorsal and two postero- dorsal setae instead of the reverse (but this could be just a matter of interpretation, because the illustration of Evans (1963) actually shows pd2 not exactly aligned with pd1); tibiae III and IV with type VII. As noted by Lindquist and Evans (1965), trochanter I and genu and tibia of all legs with same complement of setae observed in larvae, indicating that setae are not added in the post-larval phases; also, femora I–II with setal deficiencies in relation to usual complement of adults. All legs with pretarsi, each with three rounded pulvillar lobes, and strongly sclerotized claws (Figure 19).

Adult male. Unknown.

Remarks The present description greatly augments the original description of this species, including measurements of all dorsal and ventral idiosomal setae, leg chaetotaxy, and characteristics of palpus and spermatheca. From the original descriptions and the illustrations, A. lativentris differs from A. areolatus by having: (a) podonotal setae longer; (b) Jv5 (described as V8, 29 µm; other ventrianal setae 17–20 µm) longer than other ventrianal setae (Jv5 illustrated in the original description of A. areolatus as very short, not longer than the para-anal and other ventrianal setae); and (c) two small adjacent metapodal platelets next to a lyrifissure (ventral view of idiosoma in the original description of A. areolatus without these structures in the same area). Of the listed differences, only the presence of the metapodal structures would seem to distinguish A. lativentris from the Brazilian specimens collected in this study and the type specimens of A. americanus, the latter only with a lyrifissure in that area. However, in our examination of A. lativentris type specimens and of two additional Brazilian specimens of the same species identified by W. Karg, the metapodal structures were not found, only the lyrifissures being present. The type locality of A. lativentris (Cabreúva, São Paulo state) is close to some sites from which Brazilian specimens examined in this study were collected (as little as 100 km), and those locations belong to the same biome (Atlantic Forest). The type locality of A. lativentris is about 1,000 km from the type locality of A. americanus, at similar latitudes (23o 26´ and 25o 13´ S). The morphological and ecological information led us to conclude that A. lativentris, A. americanus and the Brazilian specimens belong to a single species. Figure 5 of the original description of A. americanus shows the podonotal region of the dorsal shield smooth, anterior region of epistome rounded and hypostome with two long basal transverse lines crossing the deutosternal groove. However, the examination of type specimens of A. americanus showed those structures to be different, and as described for the newly collected Brazilian specimens. Reduction in number of leg setae was highlighted by Lindquist and Evans (1965) for areolatus, but an actual chaetotaxy of leg segments is provided here for the first time for species of this genus. No reference was made in the original description of A. lativentris nor of A. americanus about how they differed from A. areolatus. The unavailability of type material of A. areolatus prevents a direct comparison between this and those other species. Evert E. Lindquist (pers. com. 2018) examined the holotype of A. areolatus in 1962. He noted some differences in relation to what was reported in the original description of the species, as follows: a) s3 present (obscured by ventrally curved lateral margins of dorsal shield of the holotype); b) J4 considerably shorter than distance between its base and base of J5, instead of about as long as distance J4–J5 (superficially appearing longer, due to downward curvature of dorsal shield); c) with only one pair of pre-sternal platelets, instead of two pairs, apparently caused by cuticular distortion; d) sternal shield with anterior and

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Downloaded From: https://bioone.org/journals/Systematic-and-Applied-Acarology on 17 Jun 2020 Terms of Use: https://bioone.org/terms-of-use Access provided by University of Guelph posterior margins straight, instead of appearing respectively convex and concave, due to cuticular distortion; e) sternal and epigynal shields reticulate, instead of smooth; f) in contrast to legs II and III, one of the four setae of basitarsus IV acute, less conspicuously modified and curved, blunt (tarsus II illustrated in the original description shows all basitarsal setae blunt). From what it is now known about the morphology of A. lativentris and A. areolatus, it seems that the former differs from the latter by having: some podonotal setae much longer (about as long as the distance to the respective following seta) and all basitarsal setae acute. However, are such differences sufficient to consider them different species, or should those be considered intraspecific variation? Africoseius lativentris was described based on two females and additional specimens are now available, as previously mentioned in this publication, allowing some inference on its morphological variability. However, unfortunately, the original description of A. areolatus was based on only one female, which excludes the possibility of any consideration on morphological variability. Specimens from Brazil identified in this work as A. lativentris were interpreted to have some J and Z setae rather variable in length and shape (because of observed clines of those characteristics), hence the differences between length of some podonotal setae and shape of basitarsal setae between those putative species could also reflect/indicate intraspecific variation. However, in this publication we refrain from considering A. lativentris a junior synonym of A. areolatus, for lack of information on the degree of intraspecific variability of those characteristics, despite their synonymy by Halliday et al. (1998), which was not accompanied by an explanation. The insertion of the para-anal setae well behind the posterior margin of the anal opening distinguished the undescribed Australian species examined in this study from A. areolatus and A. lativentris.

Phylogenetic study After trimming and removing primer sequence, the lengths of the 18S and 28S regions amplified from Africoseius specimens were 465 and 763 bp, respectively. Base-pair composition (%) was A=28.7, C=15.5, G=24.1, T=31.7 for the 18S, and A=26.8, C=16.3, G=26.4, T=30.6 for the 28S. A NCBI BLAST search on January 4, 2016 in the NCBI database showed the sequences of the Brazilian specimens of Africoseius to be most similar to the only three sequences of podocinid species available in the database, with high similarity scores (98 and 94% for 18S and 28S, respectively). Bayesian (Figure 20) and ML (Figure 21) analyses resulted in topologically similar trees, except for the position of Antennoseius sp. in the tree, which is located closer to Ameroseiidae taxa in Bayesian analysis and to Ascidae in ML analysis (Figure 20–21). Both analyses suggested Africoseius to be a member of the well-supported Podocinidae (sensu Lindquist et al. 2009) clade (PP=84%; BS=46%). Almost all families considered in the study resulted in separate and defined clades. The exceptions were the variable position of Antennoseius, already referred to, and: a) the group of species ‘Blattisociidae + Phytoseiidae’, which formed a clade; b) Rhodacaridae species, scattered in the tree, suggesting a paraphyletic group; and c) Protogamasellopsis zaheri Abo-Shnaf, Castilho & Moraes, 2013 (mentioned in GeneBank as Protogamasellopsis posnaniensis), which is included in the Ascidae clade. These results are similar to those presented by Famah-Sourassou et al. (2015), with some exceptions. In these results, the resolution of the Blattisociidae + Phytoseiidae clade was improved in the Bayesian analysis (Figure 20), in relation to the analysis in Famah-Sourassou et al. (2015). The polytomy between the species of Laelapidae and Glyptholaspis (Macrochelidae) previously reported by Famah-Sourassou et al. (2015) was resolved in this analysis. However, an accurate conclusion in this regard requires a larger number of macrochelid representatives.

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FIGURE 20. Bayesian analysis showing relationships of Africoseius with other Monogynaspida Mesostigmata, based on partial sequences of the 18S and 28S. The tree was rooted with two species of Parasitidae taken from the GenBank. Numbers above the branches indicate Bayesian posterior probabilities (> 0.5).

Placement of Africoseius in Podocinidae The results of the phylogenetic analysis of the present study are in agreement with Lindquist and Evans (1965) in that Africoseius is not a genus of the group they designated as Ascidae. Additionally, the monophyly of the Podocinidae with the inclusion of Africoseius was well-supported in the molecular analysis of this work, suggesting the affiliation of this genus to Podocinidae sensu Lindquist et al. (2009). Karg (1982) and Karg and Schorlemmer (2009) had already placed Africoseius in “Podocinidae” but, as reported by Famah-Sourassou et al. (2015), their concept of Podocinidae is different from the concept of Lindquist et al. (2009). In the concept of Karg (1982) and Karg and Schorlemmer (2009), Podocinidae also includes genera presently placed in different families according to the concept of Lindquist et al. (2009), such as Neojordensia Evans, 1957 (Ascidae), and Aceodromus Muma, 1961 and Lasioseius Berlese, 1916 (Blattisociidae). Andregamasus Costa, 1965, also included in Podocinidae by Karg (1982) and Karg and Schorlemmer (2009), is here considered incertae sedis (see Moraes et al. 2016). The placement of Africoseius in Podocinidae leads to the need to provide a new diagnostic morphological characterization of this family. A morphological characteristic apparently shared exclusively by those taxa is the hypotrichous condition of tibia I (eight setae in Africoseius and Podocinella, a retention of larval complement, and nine setae in Podocinum, instead of ten or more

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Downloaded From: https://bioone.org/journals/Systematic-and-Applied-Acarology on 17 Jun 2020 Terms of Use: https://bioone.org/terms-of-use Access provided by University of Guelph in other Gamasina). Another outstanding set of characteristics shared by those taxa, namely the broad epigynal and ventrianal shields (presence of ventrianal shield was also observed in the deutonymphs of A. areolatus [E.E. Lindquist, pers. com.] and Podocinum pacificum [personal observation]) and the absence of discrete metapodal platelets, is also shared by Zercoseius Berlese, 1916 (Blattisociidae) (Moraes et al. 2016). The spermathecal apparatus of the former (see Athias-Henriot, 1967) is totally different from that of Africoseius and species of Podocinidae sensu Lindquist et al. (2009). Other characteristics shared by Africoseius and Podocinidae sensu Lindquist et al. (2009) but also by other mesostigmatic groups are:

FIGURE 21. Maximum Likelihood analysis showing relationships of Africoseius with other Monogynaspida Mesostigmata, based on partial sequences of the 18S and 28S. The tree was rooted with two species of Parasitidae taken from the GenBank. Numbers above the branches indicate bootstrap values based on 1000 replications (> 50).

- Gnathosoma. Cheliceral digits of similar lengths or fixed digit slightly longer. Movable digit with two teeth in addition to apical hook. Fixed digit seemingly without subapical offset “Gabelzahn” tooth; pilus dentilis setiform. Arthrodial process of chelicera shaped as a coronet-like fringe. Corniculus horn-like.

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Downloaded From: https://bioone.org/journals/Systematic-and-Applied-Acarology on 17 Jun 2020 Terms of Use: https://bioone.org/terms-of-use Access provided by University of Guelph - Dorsal idiosoma. Podonotal and opisthonotal shields fused, in some Podocinum species with deep lateral incisions between setae Z1 and Z3 (P. aciculatum Evans & Hyatt 1958, P. bengalensis Bhattacharyya, 1968, P. jamaicense Evans & Hyatt, 1958, P. protonotum Ishikawa & Saichauae, 1997 and P. ruwenzoriense Evans & Hyatt, 1958). - Ventral idiosoma. Tritosternum usually without discrete base (visible in one of 13 Africoseius specimens examined in this work). Sternal shield with three pairs of setae (st1–st3). Lyrifissure iv3 absent (not observed in several descriptions of Podocinum and Podocinella and in examined specimens of P. pacificum from Brazil and Colombia and P. bengalensis, P. saglet in the original description of Podocinum pugnorum De Leon, 1964. Epigynal shield exteax and P. misella from Brazil; apparently shown on metasternal platending posteriorly well behind coxa IV, usually distinctly broadened posteriad of st5. Anal opening small, at most one fourth as long as ventrianal shield. Anterior section of endopodal shield fused with sternal shield. Metapodal platelets incorporated as discernible sigilla in expanded ventrianal shield. Exopodal plate distinct, usually fused with peritrematic plate (according to B. Halliday, pers. com. in November 2016, exopodal plate represented by a small triangular exopodal plate between coxae II–III and very narrow elongate exopodal plates outside coxae II and III in Podocinum monilicum Halliday, 1990; exopodal plate represented by a small triangular exopodal plate between coxae II–III in Podocinum taylori Halliday, 1990). - Peritreme. Usually extending forward to abut peritreme of opposite side (in some specimens of Africoseius distal end deflected forward or backward and approximated; extending only slightly beyond j1 in P. sagax). - Legs. Insertions of av2 and pv2 considerably more distal on tarsi II and III than shown by Evans (1963) for the majority of the free-living Gamasina and in numerous subsequent publications, as well as in what was observed in our examination of representative free-living species of different families of the subcohort Dermanyssiae of Lindquist et al. (2009) (Ascidae, Blattisociidae, Laelapidae, Macrochelidae, Ologamasidae, Parasitidae, Veigaiidae); femur II with 10 setae and femora III and IV with six setae each. Genua and tibiae with reduced setation. Chaetotaxy of tibia II, 1-1/1 2/1-1 (instead of 1-2/1, 1/1-1, type VII, but see previous explanation), and of tibia III, type VII. Evaluation of the series of specimens available in this study showed some morphological variations within Podocinidae sensu Lindquist et al. (2009), including Africoseius. The morphological differences between Africoseius species on one hand and species of Podocinum and Podocinella on another hand are sufficiently significant to divide Podocinidae in two subfamilies, as informally suggested by Lindquist and Evans (1965): the type subfamily and the subfamily Africoseiinae subfam. nov.. These subfamilies can be separated according to the characteristics shown in Table 4. The following characteristics mentioned in Table 4 are apomorphies of Africoseiinae: h2 attenuated and distinctly longer than h3, which are short; sternal shield short; setae ad4 and pd4 (sensu Evans 1969) of tarsi II–IV absent, and setae av4 and pv4 of same tarsi long, incurved and inserted ventrally and close to each other and to a posterior longitudinal extension of the peripodomeric suture; genu I with eight setae [differing from type X of Evans (1963) by missing al2 and pl2], genu II with six setae [differing from type VII Evans (1963) by missing al2], genu III with type VI, genu IV with five setae. Evans (1969) modified the terminology system for the chaetotaxy of tarsi II–IV in Mesostigmata previously proposed (Evans 1963) based on the complement of setae observed in Sejina and some Tryginaspida. In the system of setae observed by Evans (1969), av4 and pv4 are never developed in Gamasina and the setae md, ad2, pd2, mv, al3, pl3, ad3 and pd3 (sensu Evans 1963) are renamed as ad2, ad3, pd3, av3, al4, pl4, ad4 and pd4, respectively. In Africoseius, the position of the setae in basitarsi II-IV allows us to infer that ad4 and pd4 are absent, while av4 and pv4 are present.

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Character Podocininae Africoseiinae subfam. nov. Teeth on fixed digit 4–7 1 Anterior region of epistome Trispinate Acuminate 5–7; number of denticles not specified in most descriptions, but certainly with many more denticles than in Africoseius according to available illustrations (12–16 denticles in Podocinum aokii Ishikawa, 1970 and up to 32 in Podocinum jamaicense Evans & Hyatt, Transverse lines of denticles of Five; each with two distinct denticles 1958), some species with an additional smooth anterior deutosternum (rarely 3–4) and/ or posterior line(s) (not specified in most descriptions, except for Podocinum anhuense Wen, 1965, Podocinum catenulum De Leon, 1964, Podocinum monilicum Halliday, 1990 and Podocinum sibiricum Volonikhina, 1999) Seta h2 Distinctly shorter than h3 (often tiny) Longer than h3 2-tined and with a tiny protuberance at Palp apotele 2–3-tined the base Two subterminal setae distinctly longer Palp tarsus All setae of about the same length than others 14–23 pairs (only 11 pairs shown in the original description of Podocinella meghalayaensis 40 pairs; j2, s1 and s2 thicker; some Bhattacharyya, 1994); usually few podonotal and most opisthonotal setae barbed; some Number of dorsal shield setae opisthonotal long, thick and pilose (all podonotal and podonotal setae barbed in the opisthonotal in Podocinella plumosa Evans & Hyatt, undescribed Australian species 1958) Pre-sternal plates absent With one pair Not mentioned in most descriptions; not present in specimens of P. pacificum from Colombia and of P. bengalensis, P. pacificum, P. sagax, and P. tupinamba (Santos et al. 2017) and Podocinella misella from Lyrifissure on sternal shield Two distinct pairs (iv1, iv2) Brazil; two pairs in Podocinum monilicum Halliday, 1990 and Podocinum taylori Halliday, 1990, but these difficult to see according to B. Halliday, pers. comm. in November 2016 Short, so that section of endopodal plate Not shortened, so that section of endopodal plate Length of sternal shield behind sternal shield between coxae II- behind sternal shield located between coxae III–IV III Distinctly closer together than setae st2 in some Position of st3 Distinctly closer together than setae st2 Podocinum and Podocinella, but not in others On posterior angle of epigynal shield in Podocinum catenulum De Leon, 1964 and P. sagax (Santos et al. Paragenital lyrifissures (iv5) 2017); not shown in original description in most other On posterior angle of epigynal shield Podocinum and Podocinella species. Without iv5 in other examined Podocinidae Apparently in unscletorized cuticle of many Podocinidae, as also observed in specimens of P. pacificum from Colombia and P. bengalensis, P. pacificum and P. sagax from Brazil; shown in the Pore gv2 (according to original description of P. catenulum; pore-like In the exopodal plate posteriad of coxa interpretation of Narita et al. structure on unsclerotized cuticle next to posterior IV (2013) for Ameroseiidae) corner of epigynal shield of P. aokii, Podocinum catenum Ishikawa, 1970, Podocinum pugnorum De Leon, 1964, P. sibiricum, Podocinum tibetensis Yan, Jin, Wu, Guo & Guo, 2012 and Podocinum tsushimanum Ishikawa, 1970 could also be gv2 ...... continued on the next page

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Downloaded From: https://bioone.org/journals/Systematic-and-Applied-Acarology on 17 Jun 2020 Terms of Use: https://bioone.org/terms-of-use Access provided by University of Guelph TABLE 4. (Continued) Character Podocininae Africoseiinae subfam. nov. Pairs of setae on ventrianal shield in 3–4 6 addition to circumanal setae Well anteriad of anterior margin (A. areolatus Between anterior and posterior margins of the anal Position of para-anal setae and A. lativentris) or posteriad of posterior opening; margin (undescribed Australian species) Pairs of setae on opisthogastric soft Two in P. meghalayaensis and one in P. bengalensis and None cuticle Podocinum pacificum Laelapid-type in some species and phytoseiid-type in Spermathecal apparatus others (Athias- Henriot, 1968; Famah-Sourassou et al., Laelapid-type or A6-Ascidae-type 2015) Slightly shorter than leg IV (both longer Much longer than other legs, without pretarsus and with one than other legs), with pretarsus bearing Leg I or two subterminal tarsal setae much longer than other setae strongly sclerotized claws, three rounded in Podocinella and Podocinum, respectively pulvilarl lobes and setae of similar lengths Setae ad4, pd4, al4, pl4, av4 and Setae ad4, pd4, al4 and pl4 (sensu Evans 1969) of tarsi II– Setae ad4 and pd4 absent. Setae av4 and pv4 pv4 of tarsi II–IV (sensu Evans IV present. Setae av4 and pv4 of tarsi II–IV absent and close to each other and to a posterior extension 1969) and extension of without extension of peripodomeric suture of the peripodomeric suture peripodomeric suture With normal six setae in Podocinum and without pv2 in Setation of trochanter I Without pv2 and d Podocinella Setation of trochanter II-IV With normal five setae Without pv2

Setation of femur I With type X chaetotaxy (Evans, 1963) Without ad2 and pd2 and with pl2

Setation of genu I With type X chaetotaxy Without al2 and pl2 With nine setae in Podocinum, (differing from type X by missing pl2; also with nine setae in Hoploseius tenuis Lindquist, 1965: (Blattisociidae), but with pl2 present and Setation of tibia I with a single ad seta) or with eight setae in Podocinella With eight setae, as in Podocinella (differing from type X by missing al2 and pl2, a characteristic shared with Krantzoseius Seeman, 2012 (Blattisociidae)) With seven setae (differing from type VII by missing al2 With six setae, differing from type VII by Setation of genu II and having av1) missing al2) Setation of genu III With type VII chaetotaxy With type VI chaetotaxy With five setae, differing from type VI by Setation of genu IV With type VI chaetotaxy missing av1 Setation of tibia IV With six setae (differing from type VII by missing pl1) With type VII chaetotaxy

The distinctly longer h2 than the short h3 is a characteristic not reported for Ascoidea or Phytoseiioidea, superfamilies to which Africoseius is most closely related according to Famah- Sourassou et al. (2015). The proximity of av4 and pv4 (sensu Evans 1969) to the longitudinal extension of the peripodomeric suture led Krantz (1962) to suspect that those structures exerted a “sensory function” (most probably referring to a function different from that of those structures in other mesostigmatic mites). This combination of structures was referred to by Karg and Schorlemmer (2009) as “special sensory apparatus”. Another feature of Africoseius is the apparent absence of males, suggesting the occurrence of thelytoky, because they are neither mentioned in descriptions, nor seen among the specimens examined in this work. Males of several podocinid species are known, but Wong (1967) reported P. pacificum to undergo parthenogenetic reproduction. The following characteristics mentioned in Table 4 are apomorphies of Podocininae: h1, h3 and pc attenuated and distinctly longer than h2, which are short; leg I without pretarsi and claws, much longer than legs II–IV, antenna-like, terminating in one or two whip-like subterminal tarsal setae; genu II with seven setae [differing from type VII Evans (1963) by missing al2 and having av1]; tibia IV with six setae [differing from type VII Evans (1963) by missing pl1].

2019 RUEDA-RAMÍREZ ET AL.:PLACEMENT OF AFRICOSEIUS IN PODOCINIDAE 2389

Downloaded From: https://bioone.org/journals/Systematic-and-Applied-Acarology on 17 Jun 2020 Terms of Use: https://bioone.org/terms-of-use Access provided by University of Guelph Biological aspects of Africoseiinae and Podocininae Mites of Podocinum and Podocinella are frequently found associated with edaphic environments as soil and litter (Lindquist et al. 2009; Yan et al. 2012; Santos et al. 2017, 2019). Both genera are predators of small arthropods (Wong 1967). Personal observations allowed to confirm that specimens of P. sagax prey on nematodes. Africoseius is commonly found associated with soil or litter but interestingly some specimens of A. lativentris examined in this work were also found associated with three plant families (Caryocaraceae, Myristicaceae and Myrtaceae). These specimens were collected from different Brazilian states, and could represent different populations. Although there are no studies about the biology and behavior of Africoseius, personal observations of the second author (J.C.S.) allowed t o establish that this mite is capable of preying on nematodes; however, it was not possible to follow the development in laboratory of a few specimens collected. Some species of the families Ascidae, Blattisociidae and Melicharidae have been recorded on both, edaphic environments and plants (Moraes et al. 2015, 2016; Santos et al., 2019a, 2019b, 2019c, 2019d). Esteca et al. (2018) observed that some mesostigmatid species are capable to move from soil environments to plants, especially at night.

Conclusion In summary, a new characterization of A. lativentris is provided; this species could be a junior synonym of A. areolatus, but the unavailability of the type of the latter or complementary specimens does not allow a definitive conclusion in this regard; Africoseius is considered to belong to Africoseiinae subfam. nov., within Podocinidae.

Acknowledgments

This work was supported by FAPESP grants 2012/21412-2 and 2011/08941–3, CNPq grant (401557/2017-0 Proc. 150755/2017) and CNPq/FAPEG within the “Desenvolvimento Científico e Tecnológico Regional (DCR)” Program (Proc. no. 303016/2014-0 and 2014/0267000874). We thank COLCIENCIAS (Departamento Administrativo de Ciencia, Tecnología e Innovación, Colombia) for the scholarship to the first author (Process No. 617-2013, Chapter 3). We also thank: Gerald W. Krantz for the suggestions, valuable information and for lending us the single specimen of an undescribed Australian Africoseius species; Evert E. Lindquist, for the valuable suggestions and comments to previous versions of this manuscript and for allowing the inclusion in this document of his unpublished observations; and Jason Dunlop and Anja Friederichs, Museum für Naturkunde, Leibniz Institute for Evolution and Biodiversity Science, for lending the type specimens of A. americanus and Neojeordensia lativentris.

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Submitted: 31 Jan. 2019; accepted by Shahrooz Kazemi: 20 Jul. 2019; published: 20 Dec. 2019

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