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Zootaxa 4521 (4): 553–562 ISSN 1175-5326 (print edition) http://www.mapress.com/j/zt/ Article ZOOTAXA Copyright © 2018 Magnolia Press ISSN 1175-5334 (online edition) https://doi.org/10.11646/zootaxa.4521.4.4 http://zoobank.org/urn:lsid:zoobank.org:pub:F757583B-C025-41F4-A8FE-D7BAC55620B3

First record of the family Bolitophilidae (Diptera: ) from the Lagunas de Zempoala National Park, Mexico, with description a new species

HERON HUERTA Laboratorio de Entomología, Instituto de Diagnóstico y Referencia Epidemiológicos—InDRE, Francisco de P. Miranda No 177, Col. Unidad Lomas de Plateros, Del. Álvaro Obregón, 01480, Ciudad de México, México. E-mail: [email protected]

Abstract

The first record of the family Bolitophilidae from Mexico is reported from the “Lagunas de Zempoala” Natural Reserve, situated between the borders of the states of Morelos and Mexico (included in the Nearctic Region), with a description and illustration of a new species, (Bolitophila) zempoala spec. nov., based on adults males collected with Mal- aise traps at an altitude of 2,841 m. a. s. l. in the Neo-Volcanic Axis mountains. The new species from Mexico is very closely related to Bolitophila (Bolitophila) dubiosa Van Duzee, 1928 and B. (B.) dupla Garrett, 1925.

Key words: Bolitophilidae, Bolitophila, new species, new record, Mexico

Resumen

Primer registro de la familia Bolitophilidae en México, procedente de la Reserva Natural “Lagunas de Zempoala” situada entre los límites de los estados de Morelos y México, incluida en la región Neartica, con la descripción e ilustración de una nueva especie, Bolitophila (Bolitophila) zempoala spec. nov., basada en adultos machos colectados con trampa Mal- aise, a una altitud de 2,841 metros, en el eje neovolcánico montañoso. La nueva especie mexicana, está estrechamente relacionada a Bolitophila (Bolitophila) dubiosa Van Duzee, 1928 y B. (B.) dupla Garrett, 1925.

Palabras clave: Bolitophilidae, Bolitophila, nueva especie, nuevo registro, México

Introduction

The Lagunas de Zempoala National Park is located along the borders of the states of Morelos and Mexico. It is a zone of transition between the Nearctic and Neotropical regions with great floristic richness. It has a temperate sub- humid climate and is a natural protected area which consists of a group of seven lagoons, including a biological corridor named Chichinautzin, approximately 50 km away from Mexico City (Fig. 1). Abundant forests surround the park, including different types of trees such as oaks (Quercus Linnaeus, Fagaceae), cedars (Cedrus Trew, Pinaceae), and pine trees (Pinus Linnaeus, Pinaceae). Some studies of Diptera related to the natural reserve have been conducted, including discovery of several endemic species (Patterson & Mainland 1944; Coscarón et al. 1999; Wang et al. 2006; Huerta & Ibáñez–Bernal 2008; Sinclair & Huerta 2010; Wiedenbrug et al. 2012; Spinelli et al. 2015). However, other Diptera families, such as, for example, Bolitophilidae, , , include species not yet studied. In the particular case of Bolitophilidae, this constitutes the first report of specimens collected in Mexico in this natural reserve. The family Bolitophilidae includes a monotypic genus, Bolitophila Meigen, 1818, and comprises 64 extant species distributed primarily in the Holarctic, with the majority of species known from the Palearctic region. At present, Bolitophila is divided into two subgenera, Bolitophila Meigen (s. str.) with 23 species and Cliopisa Enderlein with 41 species (Bechev & Chandler 2011, Falaschi & Amorim 2013). This genus is widely distributed in the Nearctic (Vockeroth 1981), Palearctic (Plassmann 1988) and Oriental regions (Ševčík & Papp 2004). Records are lacking from other zoogeographical regions, e.g. the Neotropical region (Amorim 2009).

Accepted by O. Kurina: 25 Sept. 2018; published: 16 Nov. 2018 553 The biology of Bolitophilidae species is known mostly for these from the Palaearctic region, where all species with known biology are exclusively mycetophagous. Larvae live inside the fruiting bodies of mainly fleshy and soft Agaricales and Boletales (Rindal et al. 2008; Jakovlev 2011, 2012). The purpose of this paper is to describe, photograph, and illustrate a new species of the subgenus Bolitophila from specimens collected in Mexico, and to provide the first record for the country and the most southern record of the family in the Nearctic region.

FIGURE 1. Distribution of Bolitophila zempoala spec. nov. (solid rectangle) in Mexico.

Material and methods

The type material of the new species was collected by means of a Malaise trap in the Lagunas de Zempoala Natural Park (19°03′21.13″ N, 99°19′12.36″W, altitude 2841 m a. s. l.). The material was preserved in 75% ethanol and subsequently the specimens were cleared in 10% KOH, then dissected and mounted in Euparal. The holotype and paratype were prepared as permanent microscope slides. The photomicrographs were made using Lumenera® Infinity 1 digital camera software, through an Olympus BX50 compound microscope and SZX7 stereoscopic microscope. Some photos were edited using Adobe Photoshop®. Drawings were made using a camera lucida. Explanations of the taxonomic characters used here are found in Søli (1997, 2017), Søli et al. (2000) and Vockeroth (1981). The wing venation terminology follows Cumming & Wood (2017) and Gnats Online. Measurements are given in millimeters. The type specimens of the species described here are deposited in the Colección de Artrópodos con Importancia Médica (CAIM), Mexico City, Mexico. Abbreviations. ae com= aedeagal complex; a gonst= apex of gonostylus; abd st= abdominal sternites 1−8; abd tg= abdominal tergites1−8; app gonst= appendix of gonostylus; C= costal vein; clyp= clypeus; CuA= anterior

554 · Zootaxa 4521 (4) © 2018 Magnolia Press HUERTA branch of cubital veins; CuP= posterior branch of cubital vein; Dors= dorsal side; fc= face; flgm= flagellomeres I−XIV; goncx= gonocoxite; gonst= gonostylus; h= humeral crossvein; Lat= lateral side; lb gonst= lobe of gonostylus; m-cu=medial cubital crossvein; M1, M2 and M4= branches of medial vein; ped= pedicel; pm= paramere; proc gonst= process of gonostylus; R1, R2+3, R5= radial veins; r−m= radial−medial crossvein; Rs= radial sector; s=spine; Sc= subcostal vein; scp= scape; Sc−r= subcostal−radial crossvein; stm= stigma; tb com= tibial comb; tb spr= tibial spur; tb= tibia; tsm= tarsomere; Vent= ventral side.

Taxonomy

Family Bolitophilidae Meigen, 1818

Genus Bolitophila Meigen, 1818: 220.

Type species: Bolitophila cinerea Meigen, 1818, by subsequent designation (Westwood 1840: 127).

Subgenus Bolitophila Meigen, 1818

Bolitophila (Bolitophila) zempoala, new species (Figs 1−8)

Type−material. Holotype, male. MEXICO, Estado de México, Reserva Natural “Parque Nacional Lagunas de Zempoala” [19° 3´ 13.60´´ N, 99° 18´ 54.70´´W], 30−31-Jul-2005, Malaise Trap, Breidenbaugh, M. & Huerta, H. (CAIM). Paratype, male, same data as holotype (CAIM).

Diagnosis. Scutum dark brown, except postpronotum and lateral margins pale yellow; vein R2+3 ending in R1; m−cu crossvein oblique; in ventral view posterior margin of gonocoxites medially emarginated, with a broad U−shaped depression, mesally with a pair of setose lobes; gonostylus in dorsal view with apical margin serrated (sharp spines); appendices of gonostylus strongly sclerotized, with basal portion L−shaped, midportion swollen, bearing lateral short, fine spines.

FIGURE 2. Bolitophila zempoala spec. nov. Male. A. Head, frontal view. B. Face and clypeus, frontal view. Abbreviations: clyp= clypeus; fc=face. Scales: A=0.1 mm, B= 0.05 mm.

FIRST BOLITOPHILIDAE FROM MEXICO Zootaxa 4521 (4) © 2018 Magnolia Press · 555 FIGURE 3. Bolitophila zempoala spec. nov. Male. A. . B. Flagellomeres XIII−XIV. Abbreviations: flgm= flagellomeres I−XIV; ped= pedicel; scp= scape. Scales: A=0.1 mm, B= 0.01.

556 · Zootaxa 4521 (4) © 2018 Magnolia Press HUERTA FIGURE 4. Bolitophila zempoala spec. nov. Male. A. Thorax, lateral view. B. Fore leg (tibia and tarsomere 1), lateral view. tb=tibia; tb com= tibial comb; tb spr= tibial spur; tsm= tarsomere. Scale: A=0.1 mm, B=0.05 mm.

FIGURE 5. Bolitophila zempoala spec. nov. Male. Wing. Abbreviations: C= costal vein; CuA= anterior branch of cubital veins; CuP= posterior branch of cubital vein; h=humeral crossvein; m-cu=medial cubital crossvein; M1, M2 and M4= branches medial vein; r-m= radial−medial crossvein; Rs= radial sector; R1, R2+3, R5= radial veins; Sc= subcostal vein; Sc−r= subcostal−radial crossvein; stm= stigma. Scale= 0.5 mm.

Description Male: Body length 6.0 mm. Head. (Fig. 2A). Brown, wider than long. Eyes dark brown, dichoptic, facets of similar width, length of interommatidial setae close to facet width. Three ocelli present, ocellar triangle brown, ocelli of similar size, distance between ocelli similar to ocellus diameter. Vertex slightly elevated, setose; frons bare, frontal furrow marked by a line, frontal tubercle small, between the bases of the antenna, face with several setae disposed as Fig. 2B. Clypeus with 6 setae. Mouthparts considerably reduced, labella small; premental apodeme Y−shaped. Maxillary palpus longer than labella, five articulated segments. First segments very short, with a subapical seta; second segment cylindrical, shorter than third segment, with two subapical setae; third segment cylindrical,

FIRST BOLITOPHILIDAE FROM MEXICO Zootaxa 4521 (4) © 2018 Magnolia Press · 557 covered with several setae; fourth segment subcylindrical, similar in length to third, with several setae; fifth segment longer than other segments, cylindrical, setose, lighter than other segments, with the base pale, apex rounded. Antenna pale brown, length 4.96 mm (scape, pedicel and flagellomeres) (Fig. 3A), with 14 cylindrical flagellomeres. Scape subquadrate; pedicel moniliform; flagellomere 1 with the base pale; all flagellomeres covered with scattered setae; length of flagellomeres I−XIV (mm): 044, 0.42, 0.50, 0.47, 0.43, 0.42, 0.37, 0.32, 0.29, 0.26, 0.23, 0.18, 0.19, 0.22; last flagellomere rounded apically, with apical setae and a pair of subapical setae (Fig. 3B). Thorax. (Fig. 4A). Scutum dark brown, except postpronotum and lateral margins pale yellow; no transverse suture; notopleural, supra–alar areas and postalar callus without bristles; scutellum dark brown except lateral margin pale brown; mediotergite dark brown; pleural sclerites dark brown; katepisternum with three small setae. Legs. Elongated and slender, uniformly brown, except base of fore femur pale brown; covered with fine trichia; tibial spurs 1:2:2. Coxae setose; femora clothed with fine microtrichia and setation. Fore and hind femur similar in length, mid femur shorter. All tibiae densely covered with microtrichia and regular rows of setae. Tibiae all similar in length with hind tibia slightly longer. Fore tibia with apical spur (Fig. 4B) about 1.05 times length of tibial diameter at apex, external mid spur similar in length to fore tibial spur and external hind spur about 1.4 times length of fore tibial spur. Apical comb of setae present at inner face of tibiae. First tarsomere of fore leg similar in length to tibia; first tarsomere of mid and hind legs shorter than tibia of each leg. All legs with dense microtrichia and with ventral row of spines. Tarsal claws dark brown, with basal inner teeth.

FIGURE 6. Bolitophila zempoala spec. nov. Male. Abdominal segments, lateral view. Abbreviations: abd tg= abdominal tergites1−8; abd st= abdominal sternites 1−8. Scale= 0.5 mm.

558 · Zootaxa 4521 (4) © 2018 Magnolia Press HUERTA FIGURE 7. Bolitophila zempoala spec. nov. Male genitalia. A−B, ventral view. C−E, dorsal view. Abbreviations: ae com= aedeagal complex; pm= paramere. Scale: A, C= 0.16 mm; B, D, E= 0.1 mm.

Wing (Fig. 5). Length, 4.63 mm; width, 1.42 mm. Membrane covered with abundant microtrichia, without macrotrichia. Stigma faint. All veins reaching wing margin; veins R1, R5, M1, M2 and M4 with dark macrotrichia mainly in the apex. Costa long, reaching tip of wing, barely extending beyond tip of R5. Sc long, ending in C, and before the base of Rs; R1 long, curved at apex, extending about 3/4 of wing length. Base of Rs oblique, running considerably far from R1. R2+3 ending in R1, short, sinuate; medial fork arising beyond the node of Rs and r-m; r−m

FIRST BOLITOPHILIDAE FROM MEXICO Zootaxa 4521 (4) © 2018 Magnolia Press · 559 oblique; M4 ends at wing margin almost the same level of the apex of R1; CuA curved to the apex, reaching wing margin almost at the same level as the medial fork; m−cu crossvein distinct. CuP extending slightly more beyond the middle of the wing. Halteres brown, pedicel and capitulum covered with short setae; elongated, similar in length to thorax, length 1.0 mm. Abdomen. (Fig. 6). Segments brownish, elongated, length 4.5 mm, segments cylindrical, except last segment shorter.

FIGURE 8. Bolitophila zempoala spec. nov. Male genitalia. A. Ventro−lateral view (right gonostylus removed); B. Gonostylus, lateral view; C. Gonostylus, posterior view; D. Appendix of gonostylus, lateral view; E. Cerci, dorsal view. Abbreviations: a gonst= apex of gonostylus; app gonst= appendix of gonostylus; Dors= dorsal side; Lat= lateral side; lb gonst= lobe of gonostylus; proc gonst= process of gonostylus; goncx=gonocoxite; gonst=gonostylus; s=spine; Vent= ventral side. Scale: A, C=0.1 mm; B, D, E= 0.05 mm.

Male genitalia (Figs 7−8). Brownish. Length 0.30 mm, wide 0.36 mm. Gonocoxites robust, setose, fused ventromedially, anterior margin transverse, posterior margin of gonocoxites medially emarginated, with a broad U−shaped depression (Figs 7A–B); mesally a pair of setose lobes. Gonostylus robust, shorter than gonocoxite, lobe densely setose (Figs 8A–B), in dorsal view with serrated margin apically (Fig. 8C); subbasal appendices spinelike, strongly sclerotized, with basal portion L−shaped, mid-portion swollen, bearing lateral short, fine spines, distal portion with pointed tip (Figs 8B, D); cuplike process with distal margin comblike (Fig. 8B). Aedeagal complex

560 · Zootaxa 4521 (4) © 2018 Magnolia Press HUERTA (Fig. 7E) consisting of a simple, straight process with a pair of short lateral branches on anterior end, an opening at apex, ventrally covered by fused parameres (Figs 7C–E). Tergite 9 with setation along posterior margin. Cercus short, with apex pointed, covered with setae (Fig. 8E). Female. Unknown. Distribution. Mexico (boundary between the states of Morelos and Mexico). The type locality is natural reserve “Parque Nacional Lagunas de Zempoala’’ (Fig. 1). Etymology. The specific name is a noun in apposition, and refers to the name of type locality. Remarks. Bolitophila (B.) zempoala spec. nov. is very closely related to Bolitophila (Bolitophila) dubiosa Van Duzee, 1928 and B. (B.) dupla Garrett, 1925. The three species exhibit similar characteristics of the male genitalia, however, the differences are mainly in the gonostyle: in B. dubiosa and B. dupla, the sclerotized appendices of the gonostylus is V or U−shaped without a lateral spine (Kjærandsen 2018a, b), whereas in B. zempoala it is L-shaped, with the lateral margin of the midportion bearing a lateral short spine (Fig. 8D). With respect to B. dupla the original description included no details, however, Shaw (1962) indicated the postpronotum (humeri) is brown, whereas in B. zempoala it is pale yellow. Otherwise, two similar Palaearctic species, Bolitophila (B.) basicornis (Mayer, 1951) and Bolitophila (B.) tenella Winnertz, 1864, exhibit similar appendices of the gonostylus, in B. basicornis it is L-shaped with bifid apex (Hutson et al. 1980) and B. tenella present U−shaped with apex pointed (Hutson et al. 1980).

Acknowledgements

I am grateful to Dr. Mark S. Breidenbaugh (U.S. Air Force Aerial Spray Unit) for his visit and assistance with fieldwork in the Natural Reserve. I also thank Dr. Lawrence J. Hribar, Keys Control District at Florida their helpful reviews of an earlier draft of the manuscript. Special thanks to Dr. Vladimir Blagoderov (National Museums Scotland, UK), Dr. Scott J. Fitzgerald (Pacific Northwest Diptera Research Lab, USA) and Dr. Jan Ševčík (University of Ostrava, Czech Republic) for their valuable comments and suggestions on the manuscript.

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