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Comparative Study of Sensilla and Other Tegumentary Structures of Myrmeleontidae Larvae (Insecta, Neuroptera)

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Comparative Study of Sensilla and Other Tegumentary Structures of Myrmeleontidae Larvae (Insecta, Neuroptera) Received: 30 April 2020 Revised: 17 June 2020 Accepted: 11 July 2020 DOI: 10.1002/jmor.21240 RESEARCH ARTICLE Comparative study of sensilla and other tegumentary structures of Myrmeleontidae larvae (Insecta, Neuroptera) Fernando Acevedo Ramos1,2 | Víctor J. Monserrat1 | Atilano Contreras-Ramos2 | Sergio Pérez-González1 1Departamento de Biodiversidad, Ecología y Evolución, Unidad Docente de Zoología y Abstract Antropología Física, Facultad de Ciencias Antlion larvae have a complex tegumentary sensorial equipment. The sensilla and Biológicas, Universidad Complutense de Madrid, Madrid, Spain other kinds of larval tegumentary structures have been studied in 29 species of 2Departamento de Zoología, Instituto de 18 genera within family Myrmeleontidae, all of them with certain degree of Biología- Universidad Nacional Autónoma de psammophilous lifestyle. The adaptations for such lifestyle are probably related to México, Mexico City, Mexico the evolutionary success of this lineage within Neuroptera. We identified eight types Correspondence of sensory structures, six types of sensilla (excluding typical long bristles) and two Fernando Acevedo Ramos, Departamento de Biodiversidad, Ecología y Evolución, Unidad other specialized tegumentary structures. Both sensilla and other types of structures Docente de Zoología y Antropología Física, that have been observed using scanning electron microscopy show similar patterns in Facultad de Ciencias Biológicas, Universidad Complutense de Madrid, Madrid, Spain. terms of occurrence and density in all the studied species (with few exceptions). The Email: [email protected] sensilla identified are: coeloconica, placoidea, basiconica, trichodea type I, trichodea Funding information type II, and campaniformia. All these sensilla have mechano- or chemosensorial func- Instituto de Biología, Universidad Nacional tions. Some regions of the larval body have been studied using SEM for the first time, Autónoma de Mexico, Grant/Award Number: CT53/16-CT54/16; Programa de Apoyo a such as the surface of the food canal, which bears sensilla coeloconica, and the Proyectos de Investigación e Innovación abdominal segment X, that bears three types of sensilla: coeloconica, basiconica, and Tecnológica, UNAM, Grant/Award Number: IN207517; Spanish Ministry of Sciences and campaniformia. Sensilla placodea are newly reported on antlion larvae, being present Innovation, Grant/Award Number: on the mandibular base, pronotum, mentum, and cardum. Also, new locations of sen- CGL2010-22267-C07-05; Universidad Nacional Autónoma de México silla coeloconica (e.g., on rastra) and sensilla campaniformia (e.g., on odontoid pro- cesses) are noted. A novel porous texture with chemoreceptor function has been Peer Review The peer review history for this article is identified in the base of mandibles. A mechanism of dentate-notched surfaces that available at https://publons.com/publon/10. anchor maxillae and mandible, reinforcing the food canal, is detailed. All these senso- 1002/jmor.21240. rial structures, in addition to ocular tubercles for light caption and their great muscu- lar system, confer to these larvae an extraordinary predation capacity to success hunting and living in such harsh environments. KEYWORDS antlion, chemoreceptor, mechanoreceptor, morphology, SEM 1 | INTRODUCTION Aspöck, & Cerretti, 2017; Badano, Aspöck, Aspöck, & Haring, 2017; Jones, 2019; Michel et al. 2017), trying to understand the relation The family Myrmeleontidae, commonly known as antlions, is the between antlions and owlflies, the lastest phylogenomic analyses most diverse family within the order Neuroptera. Although many (Machado et al., 2019; Winterton et al., 2018) finally include owlflies recent studies have focused on the phylogeny of this group (formerly Ascalaphidae) in Myrmeleontidae (Machado et al., 2019; employing different sources of information (e.g., Badano, Aspöck, Winterton et al., 2018). With this inclusion, the family Journal of Morphology. 2020;281:1191–1209. wileyonlinelibrary.com/journal/jmor © 2020 Wiley Periodicals LLC 1191 1192 ACEVEDO RAMOS ET AL. Myrmeleontidae comprise 2,090 extant species (Oswald, 2020; Myrmeleontidae, like many other arthropods, usually present vari- Oswald & Machado, 2018). ous types of cuticular sensilla. Until now, six types of sensilla have This success is probably due to the specialization of larval stages, been reported for antlion larvae: sensillum trichodeum, sensillum especially in those groups, which succeed in colonizing the inhospita- chaeticum, sensillum basiconicum, sensillum campaniformium, ble sandy environment and becoming true psammophilous (Badano & digitiform sensillum, and sensillum coeloconicum (Eisenbeis & Pantaleoni, 2014; Mansell, 1999). Wichard, 1987; Lipovšek Delakorda et al., 2009; Devetak et al., 2013). The phylogenetic relevance of larvae in the evolution of this Sensilla chaetica/trichodea are complex and difficult to interpret group has been highlighted, and recent works related to this issue just because they cover a wide array of different types with subtle varia- corroborate it (Badano, Aspöck, Aspöck, & Cerretti, 2017; Badano, tions (Beutel et al., 2014; Chapman, 1998; Zacharuk, 1985), including Engel, Basso, Wang, & Cerretti, 2018; Winterton et al., 2018). those commonly referred as “seta” or “bristle.” In this work, we have Antlion larvae are well-known due to the fact that some species focused on the other types of sensilla, excluding such “bristles.” make pitfall traps in the sand (Badano, Aspöck, Aspöck, & Among the Myrmeleontidae species whose larvae have been Cerretti, 2017; Stange, 2004). This behavior, however, occurs in only studied using SEM (see Table 1), sensilla (apart from the different a few of the genera, and most of them are ambush predators that forms of “bristles”) have been registered for Distoleon tetragrammicus remain completely still waiting for their preys. (Fabricius, 1798) (Satar et al., 2006), Neuroleon microstenus Indeed, they can be found in many different habitats: tree cavi- (McLachlan, 1898) (Devetak et al., 2010a; Lipovšek Delakorda ties, caves, burrows, between stones, and so forth. Considering et al., 2009), Myrmecaelurus trigrammus (Pallas, 1771) (Devetak Myrmeleontidae sensu stricto, the majority of species live buried, or et al., 2013), Solter ledereri Navás, 1912 (Satar, Tusun, & Aykut, 2014), partly buried (keeping mandibles, ocular tubercles and sometimes also Gepus gibbosus Hölzel, 1968 (Satar, Tusun, & Bozdogan, 2014), a part of the pronotum unburied), in substrates such as organic matter, Myrmeleon formicarius Linnaeus, 1767 (Eisenbeis & Wichard, 1987; debris, sand, and so forth (Badano & Pantaleoni, 2014; Mansell, 1999; Lipovšek Delakorda et al., 2009), M. yemenicus Hölzel, 2002 (Devetak Stange, 2004). As has already been commented, some groups et al., 2010b), Euroleon nostras (Geoffroy in Fourcroy, 1785) (Lipovšek have succeeded in becoming psammophilous by living completely Delakorda et al., 2009) and Cueta lineosa (Rambur 1842) buried in the sand. Therefore, it is not surprising that the body (Tusun, 2020). It is noteworthy that all these papers report about Old surface of Myrmeleontidae larvae is completely covered by setae World species, and in most of these papers, only a few of the present which perform a mechanosensory function, among others (Badano & sensilla are noted. Pantaleoni, 2014; Devetak, Klokocˇovnik, Lipovšek, Bock, & The work of Devetak et al. (2013) stands out: it elaborates on Leitinger, 2013; Lipovšek Delakorda, Pabst, & Devetak, 2009). How- these sensorial structures in Myrmecaelurus trigrammus, also indicating ever, they also present other types of sensilla and cuticular sensorial the functions in which each type of sensilla are likely involved. How- structures that can only be observed by means of scanning electronic ever, we are far from understanding these questions, and further stud- microscopy (SEM). ies are needed to fully assess the role of sensilla in these animals. Cuticular sensilla are basically modified setae with sensorial func- Here, the sensilla and other types of tegumentary structures iden- tions (Chapman, 1998; Römer, 2003; Zacharuk, 1985). Each sensillum tified using SEM in several larvae of 29 species in 18 genera of has a cuticular component (seta), and one or more sensory neurons; Myrmeleontidae, all of them inhabitants of environments with sand, apart from these there are always some structures and/or cavities friable stones, dust and/or loose dirt, are described, and their probable produced by other associated cells that are also part of the sensilla or potential functions are specified. (Beutel, Friedrich, Yang, & Ge, 2014; Chapman, 1998; Glendinning, 2008). The role of each sensillum depends on its compo- sition, and can be mechano-, chemo-, thermo-, and even hygro- 2 | MATERIALS AND METHODS receptors (Altner & Loftus, 1985; Altner & Prillinger, 1980; Giglio, Ferrero, Perrotta, Talarico, & Zetto Brandmayr, 2010; Keil, 1997; 2.1 | Scanning electron microscopy Zacharuk & Shields, 1991). Mechanosensorial sensilla have no pores on its surface (Beutel 2.1.1 | Sample preparation et al., 2014; Chapman, 1998; Römer, 2003; Zacharuk, 1985). The simplest type is sensillum trichodeum. Chemoreceptor sensilla We use scanning electron microscopy (SEM) at the National Elec- (i.e., olfactory), have micropores on the surface of its cuticular com- tronic Microscopy Center of the Universidad Complutense de Madrid ponent (Beutel et al., 2014; Chapman, 1998; Galizia, 2008; (CNME-UCM) and at the
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