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Research 86 (2018) 24e32

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Cretaceous Research

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Early Cretaceous in : A new of Burmazelmira fly (Diptera: Archizelmiridae) parasitized by a sp. (, )

* Antonio Arillo a, Vladimir Blagoderov b, Enrique Penalver~ c, a Departamento de Zoología y Antropología Física (Entomología), Facultad de Biología, Universidad Complutense, E-28040 Madrid, Spain b Department of Natural Sciences, National Museums Scotland, Chambers St., Edinburgh EH1 1JF, UK c Museo Geominero, Instituto Geologico y Minero de Espana,~ C/Cirilo Amoros 42, E-46004 Valencia, Spain article info abstract

Article history: A new species of the extinct family Archizelmiridae, Burmazelmira grimaldii n. sp. (Diptera: ), is Received 7 August 2017 described from the Spanish Lower Cretaceous (upper ) amber of San Just outcrop in the Maes- Received in revised form trazgo Basin (Province of ) based on two complete specimens. A comparison with the only pre- 30 January 2018 viously known species of the genus, Burmazelmira aristica Grimaldi, Amorim and Blagoderov, 2003, is Accepted in revised form 7 February 2018 provided. The new species is diagnosed based on antennal features. One of the flies is parasitized by a Available online 13 February 2018 larval Leptus sp. mite (Acari, Erythraeidae). Despite the abundance of Leptus in several localities of Spanish amber, it is only the third record of a Leptus attached to a host. Records of parasitism are very Keywords: Diptera rare in Cretaceous , unlike in ones. A list of the known records of dipterans parasitized Archizelmiridae by mites in amber, virtually the only medium that can preserve this relationship in the record, is New species provided. Parasitism © 2018 Elsevier Ltd. All rights reserved. Cretaceous Amber

1. Introduction Despite the huge collection of fossil Diptera from Spanish Alava amber (upper Albian, northern Spain) and El Soplao amber (upper Amber is known as an exceptional medium that provides direct Albian, Province of ), no archizelmirids have been found evidence of the interactions among organisms, and it is true for to date from these two sources (Alonso et al., 2000; Najarro et al., virtually all important amber deposits (Martínez-Delclos et al., 2009; Penalver~ and Delclos, 2010). However, among the small 2004; Grimaldi and Engel, 2005; Labandeira, 2014). This kind of collection from Spanish San Just amber (upper Albian, Province of information is of interest to paleontologists, ecologists and ethol- Teruel, eastern Spain), there are two well-preserved specimens of a ogists. Records of parasitism are very uncommon in the fossil re- new species belonging to the genus Burmazelmira Grimaldi, cord, but relatively common in amber, mainly as an that Amorim and Blagoderov, 2003. Here we describe them as a new lived at the expense of another arthropod. Amber is also an species and present an uncommon case of parasitism in one of the exceptional medium for preservation of very tiny organisms, thus specimens by a larval Leptus sp. mite. being the most important source of information of some extinct Diptera clades, preserving very delicate body details (e.g. at the 2. Material studied and methods family level, Tethepomyiidae, Zhangsolvidae, Eremochaetidae or fl Chimeromyiidae). Inclusions of ies of these extinct families are The new species was found in the upper Albian amber-bearing very rare even in very well-known ambers as in the case of the deposit of San Just ( Basin, municipality, Prov- family Archizelmiridae. ince of Teruel; see Penalver~ et al., 2007), one of the most important Spanish outcrops from the only nine that have provided fossil ar- thropods as bioinclusions (Penalver~ and Delclos, 2010). The two amber pieces come from a gray-black claystone level with abun- * Corresponding author. E-mail addresses: [email protected] (A. Arillo), [email protected] dant plant macroremains, such as ferns of the genus Cladophlebis, (V. Blagoderov), [email protected] (E. Penalver).~ several such as Arctiopitys, Brachyphyllum, Glenrosa, and https://doi.org/10.1016/j.cretres.2018.02.006 0195-6671/© 2018 Elsevier Ltd. All rights reserved. A. Arillo et al. / Cretaceous Research 86 (2018) 24e32 25

Frenelopsis, and ginkgoales such as Eretmophyllum and Pseudotor- Group (sensu Rodríguez-Lopez et al., 2009; Barron et al., 2015), ellia (see Delclos et al., 2016). The deposit is situated in the Utrillas Lower Cretaceous, middleeupper Albian (sensu Villanueva- Group (sensu Rodríguez-Lopez et al., 2009), which corresponds in Amadoz et al., 2010), upper Albian (E. Barron, pers. com. 2015; this area to a fluvial delta swamp deposit (Querol et al., 1992), or based on an accurate palynological study), which corresponds to a wet areas in a fore-erg system (Rodríguez-Lopez et al., 2009). San deposit of a fluvial deltaic swamp. The outcrop of San Just (Penalver~ Just amber was discovered recently, in 2003 (Penalver~ et al., 2007; et al., 2007; Penalver~ and Delclos, 2010) is located in the munici- Penalver~ and Delclos, 2010), thus the current arthropod collection pality of Utrillas (, Autonomous Com- from this deposit is moderate. Up to now, several and munity, eastern of Spain). species, including diverse mites, have been described Etymology. The species epithet is dedicated to Dr. David Grimaldi, from this deposit. Only some Diptera families have been recog- American Museum of Natural History, , to acknowledge nized: Limoniidae, , , , his contribution to the study of the ancient and extant dipterans. , , , , Chimer- Diagnosis. Male. Basal 7 flagellomeres partially fused in a thick omyiidae, and (e.g., Arillo et al., 2008a, cone-shaped structure. Intermediate 6 flagellomeres moniliform, 2009; Szadziewski et al., 2016). more or less cylindrical. Aristate apical flagellomere, approximately The two archizelmirid specimens from San Just amber (specimen as long as the pedicel and the rest of the flagellum together. Female numbers CPT-3342 and CPT-4166; CPT-4167 for the mite specimen) unknown. are housed at the Fundacion Conjunto Paleontologico de Teruel- Holotype. Specimen CPT-3342 (complementary number SJ-07-9), a Dinopolis (Province of Teruel, Spain). The specimens were embedded virtually complete male specimen, preserved in a clear-orange in epoxy resin (EPO-TEK 301) as described in Corral et al. (1999) and turbid piece of amber trimmed to 5 3 2 mm (in an Epoxy Nascimbene and Silverstein (2000), which allowed physical protec- resin trapezoid 23 15 2 mm). This specimen has been selected tion and optimal study in ventral, lateral and dorsal views. as holotype due to the good preservation of the antennae, wing, Camera lucida drawings were made using an Olympus U-DA legs and genitalia. The holotype was discovered during the 2007 drawing tube attached to a microscope Olympus BX51. Micropho- paleontological excavation in a piece from the rich level of the tography was done by a digital camera ColorView IIIu Soft Imaging outcrop. Housed at the Fundacion Conjunto Paleontologico de Teruel- System attached to the same microscope. Habitus photographs Dinopolis (Province of Teruel, Spain). were taken with a digital camera Canon EOS 650D using the soft- Paratype. Specimen CPT-4166 (complementary number SJ-07-113), ware “Macrofotografía”, version 1.1.0.5. Most of the photographs a virtually complete male specimen, preserved in a clear-orange are reconstructions of extended depth of field based on consecutive turbid piece of amber trimmed to 5 3 1 mm (in an Epoxy pictures taken at successive focal planes. resin trapezoid 20 13 1 mm), and accompanied by a Leptus mite (CPT-4167; complementary acronym SJ-07-114). The paratype was discovered during the 2007 paleontological excavation in an amber 3. Systematic paleontology piece from the slagheap originated during the construction of the road that exposed the amber-bearing level. Housed at the same Class Insecta Linnaeus, 1758 institution that the holotype. Order Diptera Linnaeus, 1758 Description (following Grimaldi et al. (2003) description of Superfamily Sciaroidea Billberg, 1820 B. aristica). Male. Body gracile (Figs. 1 and 2), 1.9 mm long measured Family Archizelmiridae Rhodendorf, 1962 from the paratype. Head: Eyes large, occupying entire lateral sur- face of head; dichoptic (Fig. 1), without dorso-ventral differentia- Remarks. The extinct family Archizelmiridae was proposed by tion of facets (diameter of facet ¼ 18.5 mm and 20 mm; measured Rhodendorf (1962) to include a rather incomplete specimen of a from the holotype and paratype, respectively), with scarce inter- new genus and species (Archizelmira kazachstanica) from the Upper facetal setulae and a row of setae close the margins. Three ocelli Konservat-Lagerstatte€ of Karatau (Kazakhstan). Later, present (visible on the holotype; diameter ¼ ca. 40 mm), not on a Grimaldi et al. (2003) emended the diagnosis of the family to prominent mound; there is at least one strong ocellar seta between include a new compression fossil species (Archizelmira baissa)from ocelli. Mouthparts with labellum well developed, reaching the apex the Lower Cretaceous outcrop of Baissa (Transbaikal, Russian of the second palpomere; palpus well developed, 0.16 mm long Federation) and three new genera and species from Cretaceous (measured from the paratype), with three segments not cylindrical, ambers: Zelmiarcha lebanensis (Lebanon, Barremian), Burmazelmira but slightly flattened; proximal palpomere the longest and the aristica (, , see Shi et al., 2012) and Archi- widest, second palpomere the shortest, apical palpomere with a melzira americana (, Turonian). Hippa and Vilkamaa strong apical seta (Figs. 1 and 3). (Figs. 1e3), total length (2005) redefined and included Archizelmiridae in the 0.65 mm, with long, narrow scape (length ca. 2.5 times the width), latter family as a subfamily (Archizelmirinae), together with several with row of short, stiff setae on distal rim and transversal, other groups, a proposal not followed in the present study. Archi- discontinuous rows of setulae (less number of rows than in the zelmiridae is undoubtedly a monophyletic group. It has been sug- pedicel); pedicel large, scoop-shaped, with row of short, stiff setae gested to be a sister group of Sciaridae (Grimaldi et al., 2003; Hippa on distal rim and ca. 25 transversal, discontinuous rows of setulae. and Vilkamaa, 2005) although this relationship is unclear (Amorim Flagellomeres highly differentiated: basal 7 flagellomeres greatly and Rindal, 2007). fused into a thick cone-shaped structure (faint annuli discernible Genus Burmazelmira Grimaldi, Amorim and Blagoderov, 2003 under high magnification). Base of partially fused basal flag- Type species: Burmazelmira aristica Grimaldi, Amorim and ellomeres with a long, narrow condyle inserted into the apex of the Blagoderov, 2003, by original designation. pedicel (Figs. 1 and 3). Intermediate 6 flagellomeres moniliform, more or less cylindrical. Apical flagellomere long (length ca. Burmazelmira grimaldii sp. nov. 0.3 mm), whip-like (conforming an arista), with dense pubescence. LSID: 12FEB8A0-B035-4F5A-8BC7-F5F36EE47B76 Cervix elongate. Thorax: Pleura: not well visible. Legs: Long, Figs. 1e3 slender. Coxae relatively long. Fore:mid:hind tibial spurs 1:2:2 Type locality and horizon. The specimens were found in amber from (Figs. 1 and 3); tibial spurs finely pilose. Posterior margin of the fore gray-black claystones with abundant plant remains in the Utrillas femur showing a row of ca. 12 sparse, fine setae (Figs. 2 and 4), 26 A. Arillo et al. / Cretaceous Research 86 (2018) 24e32

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 right antennae 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. posterior margin of the hind tibia showing a row of ca. 25 dense, Abdomen: Genitalia: Male with gonocoxite short; gonostylus and sharp setae (Fig. 3) and anterior margin of the hind basitarsomere gonocoxite approximately equal in thickness and not gracile; gon- with a row of ca. 15 similar setae. Fore tibiae apparently without ostylus with apical pair of tooth-like spines pointing mediad. 9th apical comb of fine setae, unlike in B. aristica from , tergite transverse, wide and short, roughly trapezoid and slightly but present in distal mesotibiae (Fig. 1). Well-developed empodia rounded (Figs. 1 and 3). and pulvilli (Fig. 3). Wing: wing rounded (Figs. 1 and 2), 1.8 mm Discussion. The new species belongs to the genus Burmazelmira long measured from the holotype; C and R veins dark; others light. mainly having well-developed CuP and A1 veins and Sc reaching Sc fairly long, abruptly ended just proximal to level of Rs crossvein. nearly to Rs, eyes with short interfacetal setulae and with basal C ends slightly beyond the apex of R4þ5 and distant from apex flagellomeres packed into a conical structure and apical flag- of M1. R vein field narrow. R1 and R4þ5 with row of evenly-spaced ellomere aristate, approximately as long as the pedicel and the rest setulae along most of its length. Bases of M1þ2, CuA1, and CuA2 of the flagellum together, but it is notably longer in B. aristica. nearly parallel, attached to posterior wall of large basal cell partially Grimaldi et al. (2003) indicate in the diagnosis of the genus Bur- formed by vein composed of r-m and m-cu. CuA2 slightly sinuous, mazelmira that possibly the arista is constituted by the two distal nearly straight. CuP and A1 well developed, but abruptly incom- flagellomeres. The two specimens of the new species have only one plete, lengths more than half the distance from wing base to complete antenna each. One antenna shows a straight, long distal margin. Anal lobe large, slightly projecting; alula inconspicuous. flagellomere (Fig. 1), but the other looks like it is composed by two A. Arillo et al. / Cretaceous Research 86 (2018) 24e32 27

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 genus Leptus (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 the posterior margin of the femur).

flagellomeres (Figs. 1 and 2). We interpreted the latter as bent dense setulae) and a male genitalia with gonocoxite and gonostylus during the process of inclusion of the specimen into the resin, but less gracile and 9th tergite short and wide. we cannot discard a possibility of two-segmented structure. Apart of the diagnostic characters, Burmazelmira grimaldii differs from The absence of Burmazelmira in Alava and El Soplao ambers is B. aristica, from the Cenomanian of Myanmar, the only species of remarkable considering the large collections of bioinclusions from the genus know up to now, having scarce interfacetal setulae (vs. these deposits and the fact that they are dated as late Albian as is 28 A. Arillo et al. / Cretaceous Research 86 (2018) 24e32

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) (the same 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 showing well-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.

San Just amber (E. Barron, com. pers.), constituting these three the less fusion of the flagellomeres, according to the sequence most important amber deposits in the Iberian Peninsula. A com- described by Grimaldi et al. (2003) for the four genera of Archi- parison of the three collections shows a few shared taxa between zelmiridae. These authors indicated that the antennal changes two deposits as the species Archaeromma hispanicum (Hymenop- observed along the time for the four genera is exactly as hypothe- tera, ) in Alava and El Soplao (Ortega-Blanco sized by Stuckenberg (1999) for the evolution of the flagellum in et al., 2011), and Protoculicoides skalskii and Leptoconops zherikhini brachyceran Diptera. (Diptera, Ceratopogonidae) in Alava and San Just (Arillo et al., The Mesozoic family Archizelmiridae is extremely rare in the 2008a), but also unique taxa in each deposit. For example the fossil record but new discoveries have increased the known pale- of families Melanthripidae, Stenurothripidae and odiversity; currently, the family has 6 species in 4 genera. Each of were only found in Alava, San Just and El Soplao ambers, respec- these 6 species are known from a different deposit (Jurassic- tively, which, however, could be due to sampling bias. Cretaceous) suggesting that more specimens are present in the The present discovery extends the paleographic distribution and paleoentomological collections but there is a bias in the study of the age interval (late AlbianeCenomanian) of the genus, but the com- fossil record of Diptera, favoring other families. ments by Grimaldi et al. (2003) about the phylogenetic relation- ships among the four genera of Archizelmiridae correlated with Class Arachnida Cuvier, 1812 stratigraphic occurrence (see page 380 of that article) remain valid. Subclass Acari Leach, 1817 The new species is ca. 6 myr older than B. aristica and shows a clear Superorder Zakhvatkin, 1952 A. Arillo et al. / Cretaceous Research 86 (2018) 24e32 29

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

Order Reuter, 1909 Family 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 the mouthparts to the posterior part of the idiosoma). Idiosoma 390 mm length and 228 mm width, with elongated oval outline (probably Fig. 5. Photomicrographs of an isolated larval Leptus sp., SJNB-2012-33-02, from San fi Just amber. Lower photomicrograph made with consecutive pictures taken at succes- engorged) (Fig. 4). Dorsally covered by a milky coat, obscuring ne sive focal planes. details of the integument, but some setae visible. Gnathosoma attached to the fore femur of the host's leg. Basal part of chelicers and palpi visible, but distal parts obscured by the host. Legs well- preserved, including setae (right leg I not visible in dorsal view). foreleg of the paratype of an archizelmirid dipteran corresponds to Ventral side is not visible due to the position among the legs of the an unknown host-parasitic relationship; despite Leptus-Diptera host. interactions are relatively common in the amber fossil record since Discussion. The family Erythraeidae is characterized by the pres- the Lower Cretaceous, namely the Barremian of the Lebanon amber ence of a larval stage that frequently are ectoparasites of other (Table 1). The fine preservation in San Just amber includes some . The observed morphological characters fit well in muscle fascicles in the foreleg with the mite and other legs as the genus Leptus and the new fossil mite is as other larval mites of showed in Fig. 2. That fine preservation in this amber deposit the genus Leptus known from Spanish Cretaceous amber (see allowed the detailed description of other minute mites as Ame- Fig. 5 and Delclos et al., 2007); however some features, such as troproctus valeriae by Arillo et al. (2008b), Cretaceobodes martinezae the chaetotaxy, are not visible in this specimen, mainly due to the by Arillo et al. (2010), Trhypochthonius lopezvallei by Arillo et al. milky coat. (2012) and Tenuelamellarea estefaniae and Hypovertex hispanicus by Arillo et al. (2016). Additional isolated larvae of Leptus sp. have been found in San Just amber (Fig. 5) and in the rest of the 4. Parasitic relationship and taphonomical notes important Cretaceous Spanish ambers. As evident in Table 1, Baltic and Dominican ambers contain the Parasitism and parasitoidism are the most abundant source of main record of such as interactions, but the Mesozoic amber record interspecific interactions preserved in amber (Labandeira, 2014). In (Cretaceous) contains interesting examples all involving the mite fact, the manner in which resins captured terrestrial arthropods family Erythraeidae (possibly all of them belonging to the genus that became engulfed by the subsequent resin flows and then Leptus), except to the case of a dolichopodid fly parasitized by preserved them in fine fidelity immobilizing them and avoiding Microthrombidiidae in Canadian amber (Poinar et al., disarticulation and deformation explains why the ancient resins 1993). The Mesozoic records have been reported in Canadian, (amber and copal) virtually constitute the only geological material Raritan (New Jersey), Lebanon and Spanish ambers affecting the that contains direct evidence of parasitism. The described presence dipteran families Ceratopogonidae, , Chironomidae, of a parasitic Leptus sp. (Acari, Erythraeidae) attached to a Dolichopodidae, and now Archizelmiridae as well (see Table 1). The 30 A. Arillo et al. / Cretaceous Research 86 (2018) 24e32

Table 1 Known 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?) 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 Glockner€ (1978) (Hydracarina) Canadian amber (Campanian); Poinar et al. (1997) (Erythraeidae) (attached to ) Spanish amber (upper Albian); Alonso et al. (2000); fig. 9.4 (Leptus, Erythraeidae) Lebanese amber (Barremian); Azar et al. (2010); fig. 37B (Erythraeidae) 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 Gdansk) Baltic amber (middle Eocene): Szwedo and Sontag (2009); fig. 5 (Leptus, Erythraeidae) (coll. Museum of Amber Inclusions, University of Gdansk) 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.)

relative scarcity of records of parasitism in Cretaceous ambers, in arthropods ( and ) as hosts, while nymphs and comparison to Cenozoic ones, most likely is a consequence of a adults are free living. Insects as potential hosts of these mites have sampling bias, linked with a research bias, due to that historically received little attention, but this interspecific interaction could be the bioinclusions in Cenozoic ambers has been intensively studied, very frequent; for example, 102 heteropterans were captured in a mainly in Baltic amber, in comparison to Mesozoic ambers. How- secondary forest in Brazil, from which a total of 12 Leptus mites of ever, this circumstance has changed during the last two decades, an undescribed species were sampled in 11 specimens of bugs due to the intensification of the study of the Cretaceous Burmese observed as hosts (Pereira et al., 2012). Parasitic erythraeid larvae amber and the discovery of new Cretaceous amber outcrops very attach to their hosts on areas of soft cuticle above pockets of rich in bioinclusions in diverse parts of the world. For that reason, is circulating hemolymph (Åbro, 1988). Diptera was a diverse and surprising the absence of these records in Burmese amber, also abundant order in the resiniferous forests, and well recorded in considering that this amber has yielded one of the most diverse amber, having in general a soft cuticle and active behaviors visiting biotas from the Cretaceous period, mainly arthropods, in remark- diverse areas of the ecosystems, multiplying the opportunities for able abundance. Most likely, this kind of interspecific interaction in parasitic mites. Burmese amber has not received attention for now. It is not surprising that both the Mesozoic and Cenozoic amber 5. Conclusions records of arthropods parasitized by mites mainly involve larvae of the genus Leptus. The life cycle of parasitic larval stages of this The new discovery corroborates proposed progressive cosmopolitan genus in the Recent biota includes a wide range of morphological 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 deposits Barron, E., Peyrot, D., Rodríguez-Lopez, J.P., Melendez, N., Lopez del Valle, R., than a species from Burmese amber, B. grimaldii has antennae less Najarro, M., Rosales, I., Comas-Rengifo, M.J., 2015. Palynology of Aptian and upper Albian (Lower Cretaceous) amber-bearing outcrops of the southern consolidated, with moniliform flagellomeres 8e13 not fused to a margin of the Basque-Cantabrian Basin (northern Spain). Cretaceous Research bulbous base. Modification of antennae along the diversification of 52, 292e312. Boucot, A.J., Poinar, G.O., 2010. Fossil behavior compendium. CRC Press, 363 pp. Archizelmiridae during the Cretaceous took slightly different Corral, J.C., Lopez del Valle, R., Alonso, J., 1999. El ambar cretacico de Alava (Cuenca routes, with the appearance of an arista in Burmazelmira and the Vasco-Cantabrica, norte de Espana).~ Su colecta y preparacion. Estudios del reduction of the number of flagellomeres in Archimelzira. However, Museo de Ciencias Naturales de Alava 14 (Special Publication, number 2), in both cases antenna became more mobile according to functional 7e21. Delclos, X., Arillo, A., Penalver,~ E., Barron, E., Soriano, C., Lopez del Valle, R., morphology inferred from the , which most likely led to Bernardez, E., Corral, C., Ortuno,~ V.M., 2007. Fossiliferous amber deposits from improvement of communication and olfactory functions. the Cretaceous (Albian) of Spain. Comptes Rendus Palevol 6, 135e149. Discovery of a new archizelmirid in the Lower Cretaceous of Delclos, X., Penalver,~ E., Arillo, A., Engel, M.S., Nel, A., Azar, D., Ross, A., 2016. New fi (Insecta: Mantodea) in Cretaceous ambers from Lebanon, Spain and Spain con rms that the group, though scarce in fossil record, was Myanmar. Cretaceous Research 60, 91e108. widely distributed through Upper Jurassic-Cretaceous at least in Geirnaert, E., 2002. L’ambre. Miel de fortune et memoire de vie. Editions du Piat,176 pp. Northern hemisphere warm temperate zone. Their rarity in fossil Grimaldi, D.A., Engel, M.S., 2005. Evolution of the Insects. Cambridge University record might be due to unusual biology and/or their study is biased Press, New York, 755 pp. Grimaldi, D., Shedrinsky, A., Wampler, T.P., 2000. A remarkable deposit of fossilif- respect to other dipteran families. erous amber from the Upper Cretaceous (Turonian) of New Jersey. In: One of the new specimens of archizelmirids provided new evi- Grimaldi, D. (Ed.), Studies on fossils in amber, with particular reference to the e dence of parasitism involving the mite family Erythraeidae for the Cretaceous of New Jersey. Backhuys Publishers, Leiden, pp. 1 76. Grimaldi, D., Amorim, D.S., Blagoderov, V., 2003. The Mesozoic family Archi- scarce Mesozoic record of interspecific interactions between ar- zelmiridae (Diptera: Insecta). Journal of Paleontology 77 (2), 368e381. thropods, increasing the known number of dipteran families Hippa, H., Vilkamaa, P., 2005. The genus Sciarotricha gen. n. (Sciaridae) and the & parasitized by mites in the past. phylogeny of recent and fossil Sciaroidea (Diptera). Insect Systematics Evo- lution 36, 121e144. Janzen, J.W., 2002. Arthropods in Baltic amber. Halle (Saale). Ampyx-Verlag, 167 pp. Acknowledgements Kobbert, M.J., 2005. Bernstein e Fenser in die Urzeit. Gottingen.€ Planet Poster Editions, 227 pp. Labandeira, C.C., 2014. Amber. In: Laflamme, M., Schiffbauer, J.D., Darroch, S.A.F. We thank the staff of the Fundacion Conjunto Paleontologico de (Eds.), Reading and Writing of the Fossil Record: Preservational Pathways to Teruel-Dinopolis, in particular Dr. Luis Alcala and Mr. Eduardo Exceptional Fossilization (pp. 163e217). The Paleontological Society Papers, vol. Espílez, for curation and access to specimens. Authors wish also to 20. The Paleontological Society Short Course. Martínez-Delclos, X., Briggs, D.E.G., Penalver,~ E., 2004. Taphonomy of insects in express their gratitude to the two anonymous reviewers and to the carbonates and amber. Palaeogeography, Palaeoclimatology, Palaeoecology 203, Editor Dr. E. Koutsoukos for their helpful comments and input, 19e64. Najarro, M., Penalver,~ E., Rosales, I., Perez-de la Fuente, R., Daviero-Gomez, V., which improved the manuscript. Paleontological excavation was Gomez, B., Delclos, X., 2009. Unusual concentration of Early Albian arthropod- sponsored by Diputacion General de Aragon (Direccion General de bearing amber in the Basque-Cantabrian Basin (El Soplao, Cantabria, Northern Patrimonio Cultural) and Caja Rural de Teruel. This study is sup- Spain): Palaeoenvironmental and palaeobiological implications. Geologica Acta ported by the Spanish Ministry of Economy and Competitiveness 7 (3), 363e387. “ Nascimbene, P., Silverstein, H., 2000. The preparation of fragile Cretaceous ambers project CGL2014-52163 Iberian amber: An exceptional record of for conservation and study of organismal inclusions. In: Grimaldi, D. (Ed.), Cretaceous forests at the rise of modern terrestrial ecosystems”. Studies on fossils in amber, with particular reference to the Cretaceous of New Jersey. Backhuys Publishers, Leiden, pp. 93e102. Ortega-Blanco, J., Penalver,~ E., Delclos, X., Engel, M.S., 2011. False fairy wasps in Early References Cretaceous amber from Spain (: Mymarommatoidea). Palae- ontology 54 (3), 511e523. Åbro, A., 1988. The mode of attachment of mite larvae (Leptus spp.) to harvestment Penney, D., Green, D.I., 2011. Fossils in amber. Remarkable snapshots of prehistoric (). Journal of Natural History 22, 123e130. forest life. Siri Scientific Press, Manchester, 225 pp. Alonso, J., Arillo, A., Barron, E., Corral, J.C., Grimalt, J., Lopez, J.F., Lopez, R., Martínez- Penney, D., Jepson, J.E., 2014. Fossil Insects: An introduction to palaeoentomology. Delclos, X., Ortuno,~ V., Penalver,~ E., Trincao,~ P.R., 2000. A new fossil resin with Siri Scientific Press, Manchester, 224 pp. ~ biological inclusions in Lower Cretaceous deposits from Alava (Northern Spain, Penalver, E., Delclos, X., 2010. Spanish Amber. In: Penney, D. (Ed.), of Basque-Cantabrian Basin). Journal of Paleontology 74 (1), 158e178. fossils in amber from the major world deposits. Siri Scientific Press, Manchester, Amorim, D.S., Rindal, E., 2007. Phylogeny of the Mycetophiliformia, with proposal of pp. 236e270. ~ the subfamilies Heterotrichinae, Ohakuneinae, and Chiletrichinae for the Ran- Penalver, E., Delclos, X., Soriano, C., 2007. A new rich amber outcrop with palae- gomaramidae (Diptera, ). Zootaxa 1535, 1e92. obiological inclusions in the Lower Cretaceous of Spain. Cretaceous Research 28, Arillo, A., 2007. Paleoethology: fossilized behaviours in amber. Geologica Acta 5 (2), 791e802. ~ 159e166. Pereira, A.I.A., Fadini, M.A.M., Pikart, T.G., Zanuncio, J.C., Serrao, J.E., 2012. New hosts Arillo, A., Penalver,~ E., Delclos, X., 2008a. Microphorites (Diptera: Dolichopodidae) and parasitism notes for the mite Leptus (Acari: Erythraeidae) in fragments of from the Lower Cretaceous amber of San Just (Spain), and the co-occurrence of the Atlantic Forest, Brazil. Brazilian Journal of Biology 72 (3), 611e616. two ceratopogonid species in Spanish amber deposits. Zootaxa 1920, 29e40. Poinar Jr., G.O., 1985. Fossil evidence of insect parasitism by mites. International Arillo, A., Subías, L.S., Shtanchaeva, U., 2008b. A new fossil species of oribatid mite, Journal of Acarology 11 (1), 37e38. Ametroproctus valeriae sp. nov. (Acariformes, , Ametroproctidae), from Poinar Jr., G.O., 2003. Amber. In: Resh, V., Carde, R.T. (Eds.), Encyclopedia of Insects. the Lower Cretaceous amber of San Just, Teruel Province, Spain. Cretaceous Academic Press, San Diego, CA, pp. 9e12. Research 30 (2), 322e324. Poinar Jr., G.O., Milki, R., 2001. Lebanese amber. The oldest insect ecosystem in Arillo, A., Penalver,~ E., García-Gimeno, V., 2009. First fossil (Diptera: fossilized amber. Oregon State University Press, 96 pp. Spaniidae) from the Lower Cretaceous amber of San Just (Teruel Province, Poinar, G.O., Poinar, R., 1999. The amber forest. A reconstruction of a vanished Spain). Zootaxa 2026, 33e39. world. Princeton University Press, Princeton, 239 pp. Arillo, A., Subías, L.S., Shtanchaeva, U., 2010. A new genus and species of oribatid Poinar, G.O., Pike, E.M., Krantz, G.W., 1993. -animal parasitism. Nature 361, mite, Cretaceobodes martinezae gen. et sp. nov., from the Lower Cretaceous 307e308. amber of San Just (Teruel Province, Spain) (Acariformes, Oribatida, Otocephei- Poinar Jr., G.O., Acra, A., Acra, F., 1994. Animal-animal parasitism in Lebanese amber. dae). Paleontological Journal 44, 287e290. Medical Science Research 22, p. 159. Arillo, A., Subías, L.S., Shtanchaeva, U., 2012. A new species of fossil oribatid mite Poinar Jr., G.O., Krantz, G.W., Boucot, A.J., Pike, T.M., 1997. A unique Mesozoic (Acariformes, Oribatida, Trhypochthoniidae) from the Lower Cretaceous amber parasitic association. Naturwissenschaften 84, 321e322. of San Just (Teruel Province, Spain). Systematic & Applied Acarology 17, Querol, X., Salas, R., Pardo, G., Ardevol, L., 1992. Albian -bearing deposits of the 106e112. Iberian Range in northeastern Spain. In: McCabe, P.J., Parrisch, J.T. (Eds.), Con- Arillo, A., Subías, L.S., Sanchez-García, A., 2016. New species of fossil oribatid mites trols on the distribution and quality of Cretaceous , pp. 193e208. (Acariformes, Oribatida), from the Lower Cretaceous amber of Spain. Cretaceous Geological Society of America Special Paper 267. Research 63, 68e76. Rhodendorf, B.B., 1962. Order Diptera. In: Rhodendorf, B.B. (Ed.), Fundamentals of Azar, D., Geze, R., Acra, F., 2010. Lebanese Amber. In: Penney, D. (Ed.), Biodiversity of paleontology, volume 9, Arthropoda, Tracheata, Chelicerata. Smithsonian fossils in amber from the major world deposits. Siri Scientific Press, Manchester, Institution Libraries and National Science Foundation, Washington, D.C., pp. 271e298. pp. 444e502 [In Russian] English translation 1991. 32 A. Arillo et al. / Cretaceous Research 86 (2018) 24e32

Rodríguez-Lopez, J.P., Melendez, N., Soria, A.R., de Boer, P.L., 2009. Reinterpretacion and new synonymy in recently described fossil genera (Diptera: Ceratopogo- estratigrafica y sedimentologica de las formaciones Escucha y Utrillas de la nidae). Cretaceous Research 58, 1e9. Cordillera Iberica. Revista de la Sociedad Geologica de Espana~ 22, 163e219. Szwedo, J., Sontag, E., 2009. The traps of the “amber trap”. How inclusions could Ross, A., 1998. Amber. The Natural time capsule. The Natural History Museum trap scientists with enigmas. Denisia 26, 155e169. Publishing, London, 73 pp. Villanueva-Amadoz, U., Pons, D., Diez, J.B., Ferrer, J., Sender, L.M., 2010. Angiosperm Schlee, D., Glockner,€ W., 1978. Bernstein. Stuttgarter Beitrage€ zur Naturkunde (Ser. pollen grains of San Just site () from the Albian of the Iberian C) 8, pp. 1e72. Range (north-eastern Spain). Review of Palaeobotany and Palynology 162, Shi, G., Grimaldi, D.A., Harlowb, G.E., Wang, J., Wang, J., Yang, M., Lei, W., Li, Q., Li, X., 362e381. 2012. Age constraint on Burmese amber based on UePb dating of . Weitschat, W., 2009. Jager,€ Gejagte, Parasiten und Blinde Passagiere e Momen- Cretaceous Research 37, 155e163. taufnahmen aus dem Bernsteinwald. Denisia 26, 243e256. Stuckenberg, B.R., 1999. Antennal evolution in the (Diptera), with a Weitschat, W., 2012. Snapshots of life from Baltic amber forest. 7th Session of the reassessment of terminology relating to the flagellum. Studia Dipterologica 6, World Amber Council, 18e19 May, 2012. City Council in Gdansk, pp. 75e79. 33e48. Weitschat, W., Wichard, W., 1998. Atlas der Pflanzen und Tiere im Baltischen Szadziewski, R., Arillo, A., Urbanek, A., Sontag, E., 2016. Biting of the extinct Bernstein. Verlag Dr. Friedrich Pfeil, München, 256 pp. genus Protoculicoides Boesel from Lower Cretaceous amber of San Just, Spain