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Aboard a Spider—A Complex Developmental Strategy Fossilized in Amber

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Naturwissenschaften (2011) 98:453–456 DOI 10.1007/s00114-011-0783-2 SHORT COMMUNICATION Aboard a spider—a complex developmental strategy fossilized in amber Michael Ohl Received: 3 February 2011 /Revised: 3 March 2011 /Accepted: 3 March 2011 /Published online: 23 March 2011 # Springer-Verlag 2011 Abstract Mantid flies (Mantispidae) are an unusual group Mantispidae are even more remarkable in their unusual of lacewings (Neuroptera). Adults markedly resemble larval developmental strategy. The larvae of most mantispids mantids in their general appearance and predatory behavior. exclusively feed on spider eggs. The first instar larva is highly The larvae of most mantispids exclusively prey on spider mobile and active; the other two larval stages immobile and eggs, whereby the first instar larva is highly mobile and maggot like. This kind of development shown by the active and the other two larval stages immobile and maggot mantispid larvae was first found by Brauer (1852) and has like. One of the larval strategies to pursue spider eggs is been called hypermetamorphosis (Aspöck 1996). spider-boarding. Here, I report on the first record of a fossil About 350 extant species of Mantispidae have been mantispid larva. It was found in Middle Eocene Baltic described to date (Ohl 2004). Although the raptorial amber, and it is the first record of Mantispidae from this forelegs of adult Mantispidae are distinctive structures, deposit. The larva is attached to a clubionoid spider in a their phylogenetic significance is controversial because position typical for most mantispid larvae, and, thus, it is similar leg morphologies are known to occur in other also the first fossil record of this complex larval behavior Neuroptera families too; particularly in the Afrotropical and development. Rhachiberothidae. Recent morphological (Aspöck and Mansell 1994) and molecular (Haring and Aspöck 2004) Keywords Neuroptera . Mantispidae . cladistic analyses have provided evidence for an inde- Hypermetamorphosis . Fossil . Spider . Parasitism pendent (parallel) evolution of raptorial forelegs at least twice within Neuroptera. An alternative morphological analysis suggested a sistergroup relationship between the Introduction Mantispidae and the Rhachiberothidae, with raptorial forelegs as one of their evolutionary novelties (Willmann Mantispidae, or mantid flies, is an unusual family of 1990). lacewings (Neuroptera), which is distinctive in having Although the majority of species in the Mantispidae with raptorial forelegs. At first sight, mantispids markedly known larval development are parasites of spider egg sacs, resemble praying mantids (Mantodea) in their general immature stages of at least some species in the New World appearance and predatory behavior. This striking similarity mantispid subfamily Symphrasinae are parasites in the nests of of two only remotely related groups of insects is an aculeate Hymenoptera (Redborg 1998). This is quite remark- excellent example of evolutionary convergence. able because the Symphrasinae are considered the morpho- logically most plesiomorphic, i.e., basal, lineage in Mantispidae (Lambkin 1986; Willmann 1990). However, M. Ohl (*) records of larval behavior in any mantispid lineage are Museum für Naturkunde, Leibniz-Institut für Evolutions- und fragmentary, thus the diversity of host specificity and parasitic Biodiversitätsforschung an der Humboldt-Universität zu Berlin, behavior in Mantispidae is poorly understood. As a result, the Invalidenstr. 43, 10115 Berlin, Germany phylogenetic significance of this specific larval strategy in the e-mail: [email protected] Mantispidae cannot be unambiguously evaluated at present. 454 Naturwissenschaften (2011) 98:453–456 Mantispidae are exceptionally rare in the fossil record, and all fossils hitherto known are adults, whose morphol- ogy provides no inference about larval behavior (Engel and Grimaldi 2007; Wedmann and Makarkin 2007). Further- more, fossil preservation of a mantispid larva is highly unlikely due to their soft body but also due to the highly specialized behavioral strategy. Thus, the discovery reported here of a fossil first instar larva of Mantispidae in Eocene Baltic amber attached to a clubionoid spider is a totally unexpected and a significant discovery. The fossil shows characteristics of the subfamily Mantispinae, which exclusively feed on spider eggs and which exhibit a complex larval development and behavior. This is the first fossil record of this mode of life and establishes that this complex of developmental and behavioral traits, unique for mantispines, was already present in the Eocene (44 Ma). Eocene spider biodiversity appears to have been of a similar magnitude to that seen today (Penney and Selden 2011), thus there was certainly a diverse araneofauna present at that time for mantispines to exploit. Materials and methods The specimens are preserved in a polished amber piece of about 37×16×6 mm and of exceptionally high quality. It originated from the personal collection of Jürgen Velten, Idstein, Germany, and will be finally deposited in the amber collection of the Museum für Naturkunde, Berlin, Germany. ThespecimenwasstudiedwithaLeica®M205C. Fig. 1 Clubionoid spider with a mantispid larva in Baltic amber. a Figure 1a, b is based on serial images taken with a digital Oblique dorsal view of the complete spider. b Close-up of the camera Leica® DFC 490 on a motorized dissecting scope mantispid larva. Blurred areas around the larva are due to the partly Leica® Z16Apo. The final multifocus images were cloudy fossil resin. Scale bars: a 1.0 and b 0.3 mm prepared with the Automontage software package by Syncroscopy®. active movement of the larva. Thus, it is clearly a first instar The spider was identified by Jörg Wunderlich. It is larva and belongs in the subfamily Mantispinae within probably a juvenile female and belongs in the superfamily Mantispidae because spider-boarding apparently only Clubionoidea. Since relevant diagnostic characters are not occurs in this subfamily. available, a more precise identification is impossible. The morphology of the fossil larva does not show This specimen was first figured by Janzen (2002: significant characters to provide evidence for a specific figs. 107–108), but it was incorrectly identified as a beetle systematic position. Total body length is 1.3 mm, which larva attached to an unidentified spider. It was again corresponds well to data in the literature (e.g., McKeown figured by Wunderlich (2004: photo 605), who assumed and Mincham 1948; Redborg 1998). However, with a total that it was an unidentified beetle larva, probably attacking body length of about 2.7 mm, the spider is unusually small or parasitizing an unidentified juvenile spider. However, compared with the larva. Mantispid larvae usually wrap he pointed out that phoresy was also a possibility. themselves around the pedicel, the stalked connection between the major body parts of the spider (Hoffman and Brushwein 1989), and even enter the spider’s booklungs at Results a certain point of their development. A prerequisite for such behaviors is a small body size of the mantispid larva The fossil mantispid larva (Fig. 1) is clearly of the relative to the spider, which is not the case in the fossil. The “campodeiform” type, with a flattened, elongate body and larva seems to have accidently boarded a juvenile female strong, markedly developed thoracic legs, which imply spider. Naturwissenschaften (2011) 98:453–456 455 Larvae of Mantispidae are apparently morphologically uniform. A complex system of chaetotaxy, a formal nomenclature of the setae, has been established for a few North American species (Hoffman and Brushwein 1992). Although the amber piece is remarkably well preserved, only a few major setae can be reliably identified. For example, all visible femora have two large, dorsal setae. The head shows a small group of minute, simple eyes (stemmata), with two primary setae (setae S4 and S9 according to the setal classification). On the abdomen, two distinct rows of major setae are present, which correspond to the subdorsal group setae 3 and the lateral group setae 2. Other setae could not be reliably identified. On the right fore and midlegs, the empodium, a large adhesive pad at the end of the tarsi, is visible. In total, all visible morphological characters of the fossil larva belong to the general set of features apparently common for all mantispid larvae studied so far (Hoffman and Brushwein 1992). Discussion Fig. 2 a Habitus of Mantispa styriaca (Poda), a living European The spider is a pre-adult female and cannot be identified member of the Mantispinae (used with permission from Heiko any further than to superfamily level. The Clubionoidea is a Bellmann, Germany). b First instar larva (setae omitted) and c third heterogeneous assemblage of several families, although the instar larva of the New World Leptomantispa pulchella (Banks) (taken from Hoffman and Brushwein (1992), with permission by the true sac spiders, the Clubionidae, is one of the most diverse American Entomological Society) and well-known families. To date, more than 25 species of clubionid spiders have been recorded as hosts of the North American Dicromantispa sayi (Banks) (Redborg and their tenure on the spider, the larvae feed on spider MacLeod 1985). haemolymph by penetrating body parts with thin cuticle. As far as is known, species of the subfamily Mantispinae Larvae which successfully climb onto a spider exhibit an develop exclusively in the egg sacs of a wide variety
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  • Figures in Italics Indicate the Prime Taxonomic Reference. Figures in Bold Type Indicate the Page on Which There Is a Figure. AB

    Figures in Italics Indicate the Prime Taxonomic Reference. Figures in Bold Type Indicate the Page on Which There Is a Figure. AB

    INDEX Figures in italics indicate the prime taxonomic reference. Figures in bold type indicate the page on which there is a figure. ABALOOS, 732, 748 Acerentomon, food, 455, 4.59; A. Acrocera, 1006; A. globulus, ABEL, 49I, 493 doderoi, 455 1006 abdomen, Coleoptera, adephagid Acerentulus, 4.59; head, mouth­ Acroceridae, 10o6; larvae par­ type, haplogastrous, hologa­ parts, 456; internal anatomy, asitic, 970; mesopleural sulcus strous, symphiogastrous, 825, 457 straight, 979 826, Diptera, 864; Achanthiptera rohrellijormis Acromantis, 6oi Hymenoptera, number of ex­ ( = inanis) in nests of Vespula, Acronycta, larval ecdyses, I094 posed segments, I I 87 I249 Acrotelsa, 44I ABDULLAH,884,89I,904 Acherontia atropos, I I39; sound­ acrotrophic ovarioles, in ABERNATHY,722,756 production, I I40; larva, alimen­ Coleoptera, 832 Abies excelsa, Physokermes piceae, tary canal, 1095; mandibular Acrydiidae, see Tetrigidae a pest on, 726 gland, 267 Actaletes, 470; tracheae present, ABRAHAMSON,903,904 Acheta domesticus, 546, .5 48; 467 Abraxas grossulariata auditory organ, I33 Actaletidae, 470 (Geometridae) wing-variation, Achilidae, 705 Actinoscytidae, 762 1133 Achilixiidae, 70.5 ACTON,684,688,748,767 Acalyptratae, I 020; larvae oc­ achrestogonimes, in Isoptera, 620 Actora, see Helcomyza casionally parasitic, 970; ner­ ACHTELIG,426,427,794,8I2 Actornithophilus, 665 vous system, 970; preapical Achroia, I 12 I Aculagnathidae, 884 tibial bristle, 967 acid gland, 1189 Aculeata, see Hymenoptera Acanaloniidae, 707 Acidia, see Philophylla Aculeata acanthae, in Mecoptera, 936; in ACKER, 794, 812 aculei, in Lepidoptera, I077 Siphonaptera, 946 Aclerda, 729 Acyrtosiphon, 7I7; A. pisum, Acanthaspis, puncture by, pain­ Aclerdidae, 7 29 photoperiod, temperature and ful, 732 Acleris (Tortricidae) venation, wing-development, 722 Acanthiidae, see Cimicidae or 1708 ACZEL, IOI6, I02J, IOJ7, I046 Saldidae Acletoxenus, I022 ADAIR, 599, 601 Acanthoceridae, 86o Aclypea, 854 Adalia, colour variation, 882; Acanthococcus devoniensis, 728 Acraea, I 126 development oflarva, 883; A.