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Cretaceous Research 86 (2018) 24e32

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Cretaceous Research

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Early Cretaceous parasitism in amber: A new species of Burmazelmirafly (Diptera: Archizelmiridae) parasitized by a Leptus sp. mite (Acari,Erythraeidae)

Antonio Arillo a, Vladimir Blagoderov b, Enrique Pe~nalver c, *

a Departamento de Zoología y Antropología Física (Entomología), Facultad de Biología, Universidad Complutense, E-28040 Madrid, Spainb Department of Natural Sciences, National Museums Scotland, Chambers St., Edinburgh EH1 1JF, UKc Museo Geominero, Instituto Geol�ogico y Minero de Espa~na, C/Cirilo Amor�os 42, E-46004 Valencia, Spain

a r t i c l e i n f o

Article history:Received 7 August 2017Received in revised form30 January 2018Accepted in revised form 7 February 2018Available online 13 February 2018

Keywords:DipteraArchizelmiridaeNew speciesParasitismCretaceousAmber

* Corresponding author.E-mail addresses: arillo@educa.madrid.org (A. Ari

(V. Blagoderov), e.penalver@igme.es (E. Pe~nalver).

https://doi.org/10.1016/j.cretres.2018.02.0060195-6671/© 2018 Elsevier Ltd. All rights reserved.

a b s t r a c t

A new species of the extinct family Archizelmiridae, Burmazelmira grimaldii n. sp. (Diptera: Sciaroidea), isdescribed from the Spanish Lower Cretaceous (upper Albian) amber of San Just outcrop in the Maes-trazgo Basin (Province of Teruel) based on two complete specimens. A comparison with the only pre-viously known species of the genus, Burmazelmira aristica Grimaldi, Amorim and Blagoderov, 2003, isprovided. The new species is diagnosed based on antennal features. One of the flies is parasitized by alarval Leptus sp. mite (Acari, Erythraeidae). Despite the abundance of Leptus mites in several localities ofSpanish amber, it is only the third record of a Leptus attached to a host. Records of parasitism are veryrare in Cretaceous ambers, unlike in Cenozoic ones. A list of the known records of dipterans parasitizedby mites in amber, virtually the only medium that can preserve this relationship in the fossil record, isprovided.

© 2018 Elsevier Ltd. All rights reserved.

1. Introduction

Amber is known as an exceptional medium that provides directevidence of the interactions among organisms, and it is true forvirtually all important amber deposits (Martínez-Delcl�os et al.,2004; Grimaldi and Engel, 2005; Labandeira, 2014). This kind ofinformation is of interest to paleontologists, ecologists and ethol-ogists. Records of parasitism are very uncommon in the fossil re-cord, but relatively common in amber, mainly as an arthropod thatlived at the expense of another arthropod. Amber is also anexceptional medium for preservation of very tiny organisms, thusbeing the most important source of information of some extinctDiptera clades, preserving very delicate body details (e.g. at thefamily level, Tethepomyiidae, Zhangsolvidae, Eremochaetidae orChimeromyiidae). Inclusions of flies of these extinct families arevery rare even in very well-known ambers as in the case of thefamily Archizelmiridae.

llo), V.Blagoderov@nms.ac.uk

Despite the huge collection of fossil Diptera from Spanish �Alavaamber (upper Albian, northern Spain) and El Soplao amber (upperAlbian, Province of Cantabria), no archizelmirids have been foundto date from these two sources (Alonso et al., 2000; Najarro et al.,2009; Pe~nalver and Delcl�os, 2010). However, among the smallcollection from Spanish San Just amber (upper Albian, Province ofTeruel, eastern Spain), there are two well-preserved specimens of anew species belonging to the genus Burmazelmira Grimaldi,Amorim and Blagoderov, 2003. Here we describe them as a newspecies and present an uncommon case of parasitism in one of thespecimens by a larval Leptus sp. mite.

2. Material studied and methods

The new species was found in the upper Albian amber-bearingdeposit of San Just (Maestrazgo Basin, Utrillas municipality, Prov-ince of Teruel; see Pe~nalver et al., 2007), one of the most importantSpanish outcrops from the only nine that have provided fossil ar-thropods as bioinclusions (Pe~nalver and Delcl�os, 2010). The twoamber pieces come from a gray-black claystone level with abun-dant plant macroremains, such as ferns of the genus Cladophlebis,several conifers such as Arctiopitys, Brachyphyllum, Glenrosa, and

A. Arillo et al. / Cretaceous Research 86 (2018) 24e32 25

Frenelopsis, and ginkgoales such as Eretmophyllum and Pseudotor-ellia (see Delcl�os et al., 2016). The deposit is situated in the UtrillasGroup (sensu Rodríguez-L�opez et al., 2009), which corresponds inthis area to a fluvial delta swamp deposit (Querol et al., 1992), orwet areas in a fore-erg system (Rodríguez-L�opez et al., 2009). SanJust amber was discovered recently, in 2003 (Pe~nalver et al., 2007;Pe~nalver and Delcl�os, 2010), thus the current arthropod collectionfrom this deposit is moderate. Up to now, several insect andarachnid species, including diverse mites, have been describedfrom this deposit. Only some Diptera families have been recog-nized: Limoniidae, Psychodidae, Ceratopogonidae, Chironomidae,Scatopsidae, Mycetophilidae, Keroplatidae, Rhagionidae, Chimer-omyiidae, Dolichopodidae and Phoridae (e.g., Arillo et al., 2008a,2009; Szadziewski et al., 2016).

The two archizelmirid specimens from San Just amber (specimennumbers CPT-3342 and CPT-4166; CPT-4167 for the mite specimen)are housed at the Fundaci�on Conjunto Paleontol�ogico de Teruel-Din�opolis (Province of Teruel, Spain). The specimenswere embeddedin epoxy resin (EPO-TEK 301) as described in Corral et al. (1999) andNascimbene and Silverstein (2000), which allowed physical protec-tion and optimal study in ventral, lateral and dorsal views.

Camera lucida drawings were made using an Olympus U-DAdrawing tube attached to a microscope Olympus BX51. Micropho-tography was done by a digital camera ColorView IIIu Soft ImagingSystem attached to the same microscope. Habitus photographswere taken with a digital camera Canon EOS 650D using the soft-ware “Macrofotografía”, version 1.1.0.5. Most of the photographsare reconstructions of extended depth of field based on consecutivepictures taken at successive focal planes.

3. Systematic paleontology

Class Insecta Linnaeus, 1758Order Diptera Linnaeus, 1758Superfamily Sciaroidea Billberg, 1820Family Archizelmiridae Rhodendorf, 1962

Remarks. The extinct family Archizelmiridae was proposed byRhodendorf (1962) to include a rather incomplete specimen of anew genus and species (Archizelmira kazachstanica) from the UpperJurassic Konservat-Lagerst€atte of Karatau (Kazakhstan). Later,Grimaldi et al. (2003) emended the diagnosis of the family toinclude a new compression fossil species (Archizelmira baissa) fromthe Lower Cretaceous outcrop of Baissa (Transbaikal, RussianFederation) and three new genera and species from Cretaceousambers: Zelmiarcha lebanensis (Lebanon, Barremian), Burmazelmiraaristica (Myanmar, Cenomanian, see Shi et al., 2012) and Archi-melzira americana (New Jersey, Turonian). Hippa and Vilkamaa(2005) redefined Sciaridae and included Archizelmiridae in thelatter family as a subfamily (Archizelmirinae), together with severalother groups, a proposal not followed in the present study. Archi-zelmiridae is undoubtedly a monophyletic group. It has been sug-gested to be a sister group of Sciaridae (Grimaldi et al., 2003; Hippaand Vilkamaa, 2005) although this relationship is unclear (Amorimand Rindal, 2007).

Genus Burmazelmira Grimaldi, Amorim and Blagoderov, 2003Type species: Burmazelmira aristica Grimaldi, Amorim andBlagoderov, 2003, by original designation.

Burmazelmira grimaldii sp. nov.LSID: 12FEB8A0-B035-4F5A-8BC7-F5F36EE47B76Figs. 1e3

Type locality and horizon. The specimens were found in amber fromgray-black claystones with abundant plant remains in the Utrillas

Group (sensu Rodríguez-L�opez et al., 2009; Barr�on et al., 2015),Lower Cretaceous, middleeupper Albian (sensu Villanueva-Amadoz et al., 2010), upper Albian (E. Barr�on, pers. com. 2015;based on an accurate palynological study), which corresponds to adeposit of a fluvial deltaic swamp. The outcrop of San Just (Pe~nalveret al., 2007; Pe~nalver and Delcl�os, 2010) is located in the munici-pality of Utrillas (Province of Teruel, Arag�on Autonomous Com-munity, eastern of Spain).Etymology. The species epithet is dedicated to Dr. David Grimaldi,American Museum of Natural History, New York, to acknowledgehis contribution to the study of the ancient and extant dipterans.Diagnosis. Male. Basal 7 flagellomeres partially fused in a thickcone-shaped structure. Intermediate 6 flagellomeres moniliform,more or less cylindrical. Aristate apical flagellomere, approximatelyas long as the pedicel and the rest of the flagellum together. Femaleunknown.Holotype. Specimen CPT-3342 (complementary number SJ-07-9), avirtually complete male specimen, preserved in a clear-orangeturbid piece of amber trimmed to 5 � 3 � 2 mm (in an Epoxyresin trapezoid 23 � 15 � 2 mm). This specimen has been selectedas holotype due to the good preservation of the antennae, wing,legs and genitalia. The holotype was discovered during the 2007paleontological excavation in a piece from the rich level of theoutcrop. Housed at the Fundaci�on Conjunto Paleontol�ogico de Teruel-Din�opolis (Province of Teruel, Spain).Paratype. Specimen CPT-4166 (complementary number SJ-07-113),a virtually complete male specimen, preserved in a clear-orangeturbid piece of amber trimmed to 5 � 3 � 1 mm (in an Epoxyresin trapezoid 20� 13� 1mm), and accompanied by a Leptusmite(CPT-4167; complementary acronym SJ-07-114). The paratype wasdiscovered during the 2007 paleontological excavation in an amberpiece from the slagheap originated during the construction of theroad that exposed the amber-bearing level. Housed at the sameinstitution that the holotype.Description (following Grimaldi et al. (2003) description ofB. aristica).Male. Body gracile (Figs. 1 and 2), 1.9 mm long measuredfrom the paratype. Head: Eyes large, occupying entire lateral sur-face of head; dichoptic (Fig. 1), without dorso-ventral differentia-tion of facets (diameter of facet ¼ 18.5 mm and 20 mm; measuredfrom the holotype and paratype, respectively), with scarce inter-facetal setulae and a row of setae close the margins. Three ocellipresent (visible on the holotype; diameter ¼ ca. 40 mm), not on aprominent mound; there is at least one strong ocellar seta betweenocelli. Mouthparts with labellumwell developed, reaching the apexof the second palpomere; palpus well developed, 0.16 mm long(measured from the paratype), with three segments not cylindrical,but slightly flattened; proximal palpomere the longest and thewidest, second palpomere the shortest, apical palpomere with astrong apical seta (Figs. 1 and 3). Antenna (Figs. 1e3), total length0.65 mm, with long, narrow scape (length ca. 2.5 times the width),with row of short, stiff setae on distal rim and transversal,discontinuous rows of setulae (less number of rows than in thepedicel); pedicel large, scoop-shaped, with row of short, stiff setaeon distal rim and ca. 25 transversal, discontinuous rows of setulae.Flagellomeres highly differentiated: basal 7 flagellomeres greatlyfused into a thick cone-shaped structure (faint annuli discernibleunder high magnification). Base of partially fused basal flag-ellomeres with a long, narrow condyle inserted into the apex of thepedicel (Figs. 1 and 3). Intermediate 6 flagellomeres moniliform,more or less cylindrical. Apical flagellomere long (length ca.0.3 mm), whip-like (conforming an arista), with dense pubescence.Cervix elongate. Thorax: Pleura: not well visible. Legs: Long,slender. Coxae relatively long. Fore:mid:hind tibial spurs 1:2:2(Figs. 1 and 3); tibial spurs finely pilose. Posterior margin of the forefemur showing a row of ca. 12 sparse, fine setae (Figs. 2 and 4),

Fig. 1. Camera lucida drawings of the CPT-3342 holotype male (1e2 and 5e9), and CPT-4166 paratype male (3e4) of Burmazelmira grimaldii sp. nov. (Diptera: Archizelmiridae). 1)habitus of the holotype in lateral view, 2) anterior body part in dorsal view (1 and 2 at the same scale), 3) mouthparts in lateral view, 4) antenna of the paratype, 5e6) left and rightantennae of the holotype (4e6 at the same scale), 7) details of the legs (from above to down), distal mesotibia and distal metatibia, 8) wing venation, 9) male genitalia.

A. Arillo et al. / Cretaceous Research 86 (2018) 24e3226

posterior margin of the hind tibia showing a row of ca. 25 dense,sharp setae (Fig. 3) and anterior margin of the hind basitarsomerewith a row of ca. 15 similar setae. Fore tibiae apparently withoutapical comb of fine setae, unlike in B. aristica from Burmese amber,but present in distal mesotibiae (Fig. 1). Well-developed empodiaand pulvilli (Fig. 3). Wing: wing rounded (Figs. 1 and 2), 1.8 mmlong measured from the holotype; C and R veins dark; others light.Sc fairly long, abruptly ended just proximal to level of Rs crossvein.Vein C ends slightly beyond the apex of R4þ5 and distant from apexof M1. R vein field narrow. R1 and R4þ5 with row of evenly-spacedsetulae along most of its length. Bases of M1þ2, CuA1, and CuA2nearly parallel, attached to posterior wall of large basal cell partiallyformed by vein composed of r-m and m-cu. CuA2 slightly sinuous,nearly straight. CuP and A1 well developed, but abruptly incom-plete, lengths more than half the distance from wing base tomargin. Anal lobe large, slightly projecting; alula inconspicuous.

Abdomen: Genitalia: Male with gonocoxite short; gonostylus andgonocoxite approximately equal in thickness and not gracile; gon-ostylus with apical pair of tooth-like spines pointing mediad. 9thtergite transverse, wide and short, roughly trapezoid and slightlyrounded (Figs. 1 and 3).Discussion. The new species belongs to the genus Burmazelmiramainly having well-developed CuP and A1 veins and Sc reachingnearly to Rs, eyes with short interfacetal setulae and with basalflagellomeres packed into a conical structure and apical flag-ellomere aristate, approximately as long as the pedicel and the restof the flagellum together, but it is notably longer in B. aristica.Grimaldi et al. (2003) indicate in the diagnosis of the genus Bur-mazelmira that possibly the arista is constituted by the two distalflagellomeres. The two specimens of the new species have only onecomplete antenna each. One antenna shows a straight, long distalflagellomere (Fig. 1), but the other looks like it is composed by two

Fig. 2. Photomicrographs of the CPT-3342 holotype male (1e3), and CPT-4166 paratype male (4), of Burmazelmira grimaldii sp. nov. (Diptera: Archizelmiridae) and a parasitic mite.1) habitus in lateral view of the holotype, 2) antenna, 3) wing, 4) habitus in lateral view of the paratype, 5) detail from the photomicrograph 4 of the parasitic mite of the genusLeptus (Erythraeidae) attached to the fore femur (black arrow indicates some preserved remains of the leg muscles and white arrows indicate the row of sparse, fine setae on theposterior margin of the femur).

A. Arillo et al. / Cretaceous Research 86 (2018) 24e32 27

flagellomeres (Figs. 1 and 2). We interpreted the latter as bentduring the process of inclusion of the specimen into the resin, butwe cannot discard a possibility of two-segmented structure. Apartof the diagnostic characters, Burmazelmira grimaldii differs fromB. aristica, from the Cenomanian of Myanmar, the only species ofthe genus know up to now, having scarce interfacetal setulae (vs.

dense setulae) and amale genitalia with gonocoxite and gonostylusless gracile and 9th tergite short and wide.

The absence of Burmazelmira in �Alava and El Soplao ambers isremarkable considering the large collections of bioinclusions fromthese deposits and the fact that they are dated as late Albian as is

Fig. 3. Photomicrographs of some anatomical details of the CPT-3342 holotype male (1e2, 4, 7), and CPT-4166 paratype male (3, 5e6), of Burmazelmira grimaldii sp. nov. (Diptera:Archizelmiridae). 1) detail of the antenna, 2) partially fused basal flagellomeres with a long, narrow condyle of pedicel inserted into the consolidated base of antenna (arrows) (thesame than 1 with different focal plane), 3) mouthparts with labellum well developed and three-segmented palpi, 4) fore tibia showing a spur, 5) mid leg distal tarsomere showingwell-developed empodium and pulvilli (arrow indicates an untoothed claw), 6) posterior margin of the hind tibia showing a row of sharp setae, 7) male genitalia, with well-developed spines distally on gonostyle. Only photomicrographs 3 and 5 made with consecutive pictures taken at successive focal planes.

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San Just amber (E. Barr�on, com. pers.), constituting these three themost important amber deposits in the Iberian Peninsula. A com-parison of the three collections shows a few shared taxa betweentwo deposits as the species Archaeromma hispanicum (Hymenop-tera, Mymarommatidae) in �Alava and El Soplao (Ortega-Blancoet al., 2011), and Protoculicoides skalskii and Leptoconops zherikhini(Diptera, Ceratopogonidae) in �Alava and San Just (Arillo et al.,2008a), but also unique taxa in each deposit. For example thethrips of families Melanthripidae, Stenurothripidae and Thripidaewere only found in �Alava, San Just and El Soplao ambers, respec-tively, which, however, could be due to sampling bias.

The present discovery extends the paleographic distribution andage interval (late AlbianeCenomanian) of the genus, but the com-ments by Grimaldi et al. (2003) about the phylogenetic relation-ships among the four genera of Archizelmiridae correlated withstratigraphic occurrence (see page 380 of that article) remain valid.The new species is ca. 6 myr older than B. aristica and shows a clear

less fusion of the flagellomeres, according to the sequencedescribed by Grimaldi et al. (2003) for the four genera of Archi-zelmiridae. These authors indicated that the antennal changesobserved along the time for the four genera is exactly as hypothe-sized by Stuckenberg (1999) for the evolution of the flagellum inbrachyceran Diptera.

The Mesozoic family Archizelmiridae is extremely rare in thefossil record but new discoveries have increased the known pale-odiversity; currently, the family has 6 species in 4 genera. Each ofthese 6 species are known from a different deposit (Jurassic-Cretaceous) suggesting that more specimens are present in thepaleoentomological collections but there is a bias in the study of thefossil record of Diptera, favoring other families.

Class Arachnida Cuvier, 1812Subclass Acari Leach, 1817Superorder Acariformes Zakhvatkin, 1952

Fig. 4. Camera lucida drawing of a larval Leptus sp. mite (CPT-4167) parasitizing theparatype specimen of Burmazelmira grimaldii sp. nov.

Fig. 5. Photomicrographs of an isolated larval Leptus sp., SJNB-2012-33-02, from SanJust amber. Lower photomicrograph made with consecutive pictures taken at succes-sive focal planes.

A. Arillo et al. / Cretaceous Research 86 (2018) 24e32 29

Order Trombidiformes Reuter, 1909Family Erythraeidae Robineau-Desvoidy, 1828

Genus Leptus Latreille, 1796

Leptus sp.Figs. 2.5 and 4

Specimen. CPT-4167.

Description (larval stage). Body length 451 mm (from tip of themouthparts to the posterior part of the idiosoma). Idiosoma 390 mmlength and 228 mm width, with elongated oval outline (probablyengorged) (Fig. 4). Dorsally covered by a milky coat, obscuring finedetails of the integument, but some setae visible. Gnathosomaattached to the fore femur of the host's leg. Basal part of chelicersand palpi visible, but distal parts obscured by the host. Legs well-preserved, including setae (right leg I not visible in dorsal view).Ventral side is not visible due to the position among the legs of thehost.Discussion. The family Erythraeidae is characterized by the pres-ence of a larval stage that frequently are ectoparasites of otherarthropods. The observed morphological characters fit well inthe genus Leptus and the new fossil mite is as other larval mites ofthe genus Leptus known from Spanish Cretaceous amber (seeFig. 5 and Delcl�os et al., 2007); however some features, such asthe chaetotaxy, are not visible in this specimen, mainly due to themilky coat.

4. Parasitic relationship and taphonomical notes

Parasitism and parasitoidism are the most abundant source ofinterspecific interactions preserved in amber (Labandeira, 2014). Infact, the manner in which resins captured terrestrial arthropodsthat became engulfed by the subsequent resin flows and thenpreserved them in fine fidelity immobilizing them and avoidingdisarticulation and deformation explains why the ancient resins(amber and copal) virtually constitute the only geological materialthat contains direct evidence of parasitism. The described presenceof a parasitic Leptus sp. larva (Acari, Erythraeidae) attached to a

foreleg of the paratype of an archizelmirid dipteran corresponds toan unknown host-parasitic relationship; despite Leptus-Dipterainteractions are relatively common in the amber fossil record sincethe Lower Cretaceous, namely the Barremian of the Lebanon amber(Table 1). The fine preservation in San Just amber includes somemuscle fascicles in the foreleg with the mite and other legs asshowed in Fig. 2. That fine preservation in this amber depositallowed the detailed description of other minute mites as Ame-troproctus valeriae by Arillo et al. (2008b), Cretaceobodes martinezaeby Arillo et al. (2010), Trhypochthonius lopezvallei by Arillo et al.(2012) and Tenuelamellarea estefaniae and Hypovertex hispanicusby Arillo et al. (2016). Additional isolated larvae of Leptus sp. havebeen found in San Just amber (Fig. 5) and in the rest of theimportant Cretaceous Spanish ambers.

As evident in Table 1, Baltic and Dominican ambers contain themain record of such as interactions, but the Mesozoic amber record(Cretaceous) contains interesting examples all involving the mitefamily Erythraeidae (possibly all of them belonging to the genusLeptus), except to the case of a dolichopodid fly parasitized byMicrothrombidiidae in Campanian Canadian amber (Poinar et al.,1993). The Mesozoic records have been reported in Canadian,Raritan (New Jersey), Lebanon and Spanish ambers affecting thedipteran families Ceratopogonidae, Cecidomyiidae, Chironomidae,Dolichopodidae, and now Archizelmiridae as well (see Table 1). The

Table 1Known fossil dipterans parasitized by mites from the literature. The entire record has been preserved in amber.

Limoniidae� Dominican amber (Early to mideMiocene); Boucot and Poinar (2010); fig. 46 (Acari indet.) (Poinar coll. SY-1-71)� Baltic amber (middle Eocene); Weitschat and Wichard (1998); fig. 14d (Leptus, Erythraeidae)� Baltic amber (middle Eocene); Weitschat (2009); fig. 36 (Leptus, Erythraeidae)� Baltic amber (middle Eocene); Boucot and Poinar (2010); fig. 49 (Trombidiformes) (thrombitiform [sic]) (Andrew Cholewinski coll.)Mycetophilidae� Baltic amber (middle Eocene); Weitschat and Wichard (1998); fig. 14c (Leptus, Erythraeidae)Sciaridae� Dominican amber (Early to mideMiocene); Poinar and Poinar (1999); fig. 154 (Trombidiformes)Archizelmiridae� Spanish amber (upper Abian); this paper (Leptus, Erythraeidae) (attached to Burmazelmira)Ceratopogonidae� Canadian amber (Campanian); Poinar et al. (1993) (Microthrombidiidae)� Canadian amber (Campanian); Poinar et al. (1993) (Erythraeidae) (�3)� Lebanese amber (Barremian); Poinar et al. (1994) (Leptus, Erythraeidae)� Lebanese amber (Barremian); Poinar and Milki (2001); pls. 17, 18 (Leptus, Erythraeidae)� Lebanese amber (Barremian); Boucot and Poinar (2010); fig. 40 (Erythraeidae)Cecidomyiidae� Raritan (New Jersey) amber (Turonian); Grimaldi et al. (2000); fig. 42h (Erythraeidae?)Anisopodidae� Baltic amber (middle Eocene); Kobbert (2005); pg. 181 (Leptus, Erythraeidae) (Kobbert coll. T438)Chironomidae� Dominican amber (Early to mideMiocene); Poinar (1985) (Hydracarina)� Baltic amber (middle Eocene); Schlee and Gl€ockner (1978) (Hydracarina)� Canadian amber (Campanian); Poinar et al. (1997) (Erythraeidae) (attached to Metriocnemus)� Spanish amber (upper Albian); Alonso et al. (2000); fig. 9.4 (Leptus, Erythraeidae)� Lebanese amber (Barremian); Azar et al. (2010); fig. 37B (Erythraeidae)Empididae� Baltic amber (middle Eocene); Kobbert (2005); pg. 180 (Leptus, Erythraeidae) (Kobbert coll. T162)� Baltic amber (middle Eocene); Kobbert (2005); pg. 180 (Erythraeidae) (Kobbert coll. T190)Dolichopodidae� Dominican amber (Early to mideMiocene); Labandeira (2014); fig. 6I (Leptus, Erythraeidae; erroneously considered as phoretic in the original publication)� Baltic amber (middle Eocene); Weitschat and Wichard (1998); fig. 14e (Leptus, Erythraeidae)� Baltic amber (middle Eocene); Janzen (2002); fig. 115 (Leptus, Erythraeidae) (von Holt coll.)� Baltic amber (middle Eocene); Janzen (2002); fig. 114 (Leptus, Erythraeidae)� Baltic amber (middle Eocene); Janzen (2002); fig. 116 (Leptus, Erythraeidae)� Baltic amber (middle Eocene); Geirnaert (2002); fig. 164 (Acari indet.)� Baltic amber (middle Eocene); Poinar (2003); fig. 45 in Boucot and Poinar (2010) (Trombidiformes) (Poinar coll. SY-1-137)� Baltic amber (middle Eocene); Kobbert (2005); pg. 178 (Leptus, Erythraeidae) (Kobbert coll. T407)� Baltic amber (middle Eocene); Kobbert (2005); pg. 178 (Leptus, Erythraeidae) (Kobbert coll. T210)� Baltic amber (middle Eocene); Kobbert (2005); pg. 179 (Leptus, Erythraeidae) (Kobbert coll. T312)� Baltic amber (middle Eocene); Arillo (2007); fig. 1F (Trombidiformes) (Brost coll.)� Baltic amber (middle Eocene); Szwedo and Sontag (2009); fig. 4 (Leptus, Erythraeidae) (coll. Museum of Amber Inclusions, University of Gda�nsk)� Baltic amber (middle Eocene): Szwedo and Sontag (2009); fig. 5 (Leptus, Erythraeidae) (coll. Museum of Amber Inclusions, University of Gda�nsk)� Baltic amber (middle Eocene); Weitschat (2009); fig. 34 (two Leptus, Erythraeidae)� Baltic amber (middle Eocene); Weitschat (2009); fig. 35 (two Leptus, Erythraeidae)� Baltic amber (middle Eocene); Penney and Green (2011); pg. 87 (Leptus, Erythraeidae)� Baltic amber (middle Eocene); Weitschat (2012); fig. 9 (Leptus, Erythraeidae)� Baltic amber (middle Eocene); Penney and Jepson (2014); fig. 191 (Leptus, Erythraeidae) (attached to Prohercostomus)� Spanish amber (upper Abian); Arillo (2007) (Leptus, Erythraeidae)Drosophilidae� Dominican amber (Early to mideMiocene); Ross (1998); fig. 74 (Acari indet.)

A. Arillo et al. / Cretaceous Research 86 (2018) 24e3230

relative scarcity of records of parasitism in Cretaceous ambers, incomparison to Cenozoic ones, most likely is a consequence of asampling bias, linked with a research bias, due to that historicallythe bioinclusions in Cenozoic ambers has been intensively studied,mainly in Baltic amber, in comparison to Mesozoic ambers. How-ever, this circumstance has changed during the last two decades,due to the intensification of the study of the Cretaceous Burmeseamber and the discovery of new Cretaceous amber outcrops veryrich in bioinclusions in diverse parts of theworld. For that reason, issurprising the absence of these records in Burmese amber, alsoconsidering that this amber has yielded one of the most diversebiotas from the Cretaceous period, mainly arthropods, in remark-able abundance. Most likely, this kind of interspecific interaction inBurmese amber has not received attention for now.

It is not surprising that both the Mesozoic and Cenozoic amberrecords of arthropods parasitized by mites mainly involve larvae ofthe genus Leptus. The life cycle of parasitic larval stages of thiscosmopolitan genus in the Recent biota includes a wide range of

arthropods (insects and arachnids) as hosts, while nymphs andadults are free living. Insects as potential hosts of these mites havereceived little attention, but this interspecific interaction could bevery frequent; for example, 102 heteropterans were captured in asecondary forest in Brazil, from which a total of 12 Leptus mites ofan undescribed species were sampled in 11 specimens of bugsobserved as hosts (Pereira et al., 2012). Parasitic erythraeid larvaeattach to their hosts on areas of soft cuticle above pockets ofcirculating hemolymph (Åbro, 1988). Diptera was a diverse andabundant order in the resiniferous forests, and well recorded inamber, having in general a soft cuticle and active behaviors visitingdiverse areas of the ecosystems, multiplying the opportunities forparasitic mites.

5. Conclusions

The new discovery corroborates proposed progressivemorphological specialization noted in evolution of antenna in

A. Arillo et al. / Cretaceous Research 86 (2018) 24e32 31

Archizelmiridae (Grimaldi et al., 2003). Occurring in older depositsthan a species from Burmese amber, B. grimaldii has antennae lessconsolidated, with moniliform flagellomeres 8e13 not fused to abulbous base. Modification of antennae along the diversification ofArchizelmiridae during the Cretaceous took slightly differentroutes, with the appearance of an arista in Burmazelmira and thereduction of the number of flagellomeres in Archimelzira. However,in both cases antenna became more mobile according to functionalmorphology inferred from the fossils, which most likely led toimprovement of communication and olfactory functions.

Discovery of a new archizelmirid in the Lower Cretaceous ofSpain confirms that the group, though scarce in fossil record, waswidely distributed through Upper Jurassic-Cretaceous at least inNorthern hemisphere warm temperate zone. Their rarity in fossilrecord might be due to unusual biology and/or their study is biasedrespect to other dipteran families.

One of the new specimens of archizelmirids provided new evi-dence of parasitism involving the mite family Erythraeidae for thescarce Mesozoic record of interspecific interactions between ar-thropods, increasing the known number of dipteran familiesparasitized by mites in the past.

Acknowledgements

We thank the staff of the Fundaci�on Conjunto Paleontol�ogico deTeruel-Din�opolis, in particular Dr. Luis Alcal�a and Mr. EduardoEspílez, for curation and access to specimens. Authors wish also toexpress their gratitude to the two anonymous reviewers and to theEditor Dr. E. Koutsoukos for their helpful comments and input,which improved the manuscript. Paleontological excavation wassponsored by Diputaci�on General de Arag�on (Direcci�on General dePatrimonio Cultural) and Caja Rural de Teruel. This study is sup-ported by the Spanish Ministry of Economy and Competitivenessproject CGL2014-52163 “Iberian amber: An exceptional record ofCretaceous forests at the rise of modern terrestrial ecosystems”.

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