Insecta: Neuroptera: Coniopterygidae)

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Insecta: Neuroptera: Coniopterygidae) Arthropod Structure & Development 50 (2019) 1e14 Contents lists available at ScienceDirect Arthropod Structure & Development journal homepage: www.elsevier.com/locate/asd Small, but oh my! Head morphology of adult Aleuropteryx spp. and effects of miniaturization (Insecta: Neuroptera: Coniopterygidae) * Susanne Randolf , Dominique Zimmermann Natural History Museum Vienna, 2nd Zoological Department, Burgring 7, 1010, Vienna, Austria article info abstract Article history: We present the first morphological study of the internal head structures of adults of the coniopterygid Received 15 October 2018 genus Aleuropteryx, which belong to the smallest known lacewings. The head is ventrally closed with a Accepted 1 February 2019 gula, which is unique in adult Neuroptera and otherwise developed in Megaloptera, the sister group of Neuroptera. The dorsal tentorial arms are directed posteriorly and fused, forming an arch that fulfills functions otherwise taken by the tentorial bridge. A newly found maxillary gland is present in both sexes. Keywords: Several structural modifications correlated with miniaturization are recognized: a relative increase in Miniaturization the size of the brain, a reduction in the number of ommatidia and diameter of the facets, a countersunken Brain fi Musculature cone-shaped ocular ridge, and a simpli cation of the tracheal system. The structure of the head differs Maxillary gland strikingly from that of the previously studied species Coniopteryx pygmaea, indicating a greater vari- Tentorium ability in the family Coniopterygidae, which might be another effect of miniaturization. Gula © 2019 Elsevier Ltd. All rights reserved. 1. Introduction With nearly 560 described species, Coniopterygidae are one of the four most speciose neuropteran families, inhabiting all Miniaturization is a common phenomenon in many groups of zoogeographical regions with the exception of extremely cold animals and has major effects not only on the morphology but also areas (Sziraki, 2011). Three subfamilies are recognized: Conio- on the physiology, ecology and life history of the miniaturized or- pteryginae, Aleuropteryginae, and the highly unusual neotropical ganism (Hanken and Wake, 1993). Very small organisms are not Brucheiserinae with only four known species (Sziraki, 2011). simply reduced in size; they must develop solutions to cope with Several authors even proposed to elevate the subfamilies to family size-related constraints (Schmidt-Nielsen, 1984). This leads to a rank (Tillyard, 1926; Carpentier and Lestage, 1928; Riek, 1975), range of considerable reorganizations of structures, affecting because the differences between them are substantial: They differ almost all organs and tissues that are forced to fit within tiny vol- in the venation of fore- and hindwings, in Coniopteryginae the umes (Polilov, 2015a, b; 2016c). last abdominal spiracles are reduced, and in Aleuropteryginae the Neuroptera are highly variable with respect to their body size, galea is divided and plicatures are present on the abdomen. having forewing lengths from 2 mm to over 70 mm (New, 1989). Coniopterygidae are free-living and have a lifespan of several Singular species with a small body size are present in different weeks (Muma, 1967; Henry, 1976). Niven and Farris (2012) sug- neuropteran families. The Coniopterygidae, or “dustywings”, gested that miniaturized species have severe behavioral deficits. however, are the only family with a small body size throughout all This does not seem to be the case for Coniopterygidae, which species, and can thus be regarded as the midgets of Neuroptera perform a variety of more or less complex behaviors, similar to their (New, 1989). Their body and wings are usually covered with the larger relatives: Being mainly carnivorous, they detect and over- eponymous whitish or brownish dust of waxy particles (Enderlein, power their prey, including soft-bodied arthropods in Conio- 1906) secreted by hypodermal wax glands (Withycombe, 1925). pteryginae and scale insects in Aleuropteryx (Gepp, 1967; Henry, 1976). Their mating is preceded by a rather intricate precopula- tory behavior of both sexes (Johnson and Morrison, 1979), and when disturbed, they can be observed to “play possum” or escape in a fluttery flight followed by landing on the underside of vege- * Corresponding author. tation (Johnson, 1980). E-mail addresses: [email protected] (S. Randolf), dominique. [email protected] (D. Zimmermann). https://doi.org/10.1016/j.asd.2019.02.001 1467-8039/© 2019 Elsevier Ltd. All rights reserved. 2 S. Randolf, D. Zimmermann / Arthropod Structure & Development 50 (2019) 1e14 Data on the head morphology of Coniopterygidae are sparse: 2.4. Micro-computered tomography Only recently, the head anatomy of Coniopteryx pygmaea, a species representing the subfamily Coniopteryginae, was investigated and One specimen of Aleuropteryx was dehydrated and stained for described in detail (Randolf et al., 2017). Otherwise, only few data 24 h with a 1% (w/v) solution of elemental iodine (I2) in absolute are available on the general external morphology of the head ethanol. After staining, the sample was rinsed for several hours in (Shepard, 1967; Meinander, 1972), and one scanning electron absolute ethanol and mounted in a plastic pipette tip again in ab- microscopic study comparing the surface structures and sensilla of solute ethanol. It was scanned using an XRadia MicroXCT-400 (Carl Aleuropteryx and Semidalis as representatives of the two sub- Zeiss X-ray Microscopy, Pleasanton, CA, USA) at 40 kVp/50 mA using families Aleuropteryginae and Coniopteryginae (Zimmermann the 20X detector assembly. Projections were recorded with 120s et al., 2009). In the present study, we describe the head exposure time (camera binning 2) and an angular increment of 0.2 morphology of Aleuropteryx juniperi and Aleuropteryx loewii. With a between projections. Tomographic slices were reconstructed with a body length of only 2 mm in both sexes, Aleuropteryx Low,1885€ (Fig. voxel resolution of 0.95 mm using the software provided with the 1) is one of the smallest Coniopterygidae and the eponymous genus microCT system. The reconstructed volume image was exported as for the subfamily Aleuropteryginae. We aim to a) recognize effects DICOM sequence. of miniaturization by comparing it to the head morphology of larger neuropteran representatives, and b) assess the degree of 2.5. 3D-reconstruction intrafamiliar variability by comparing it with the similarly sized species C. pygmaea (Randolf et al., 2017). Reconstructions were made using the software Amira 6.3.0. We computed new volume datasets from the original data and the la- bels data object by using the arithmetic function in Amira 6.3.0 2. Material and methods (Kleinteich et al., 2008). Volumes were calculated from the labels with the Material statistics function in Amira 6.3.0. Isosurfaces of 2.1. Taxa examined the segmented volumes were created and extracted. Since the resolution of the microCT images was insufficient for reconstruc- Male specimens of A. juniperi Ohm (1968), were examined by tion of detailed anatomy, histological sections were photographed microCT scans and histological cross sections, one specimen of with a Nikon DS-Fi1 camera (2/3 inch sensor), mounted on a Nikon A. loewii Klapalek (1894), was examined by histological longitudinal Eclipse 80i microscope with a 0,7x C-Mount Adapter in the trin- sections. Additionally cross and longitudinal sections of female ocular tube. The resolution was 2560 Â 1920 pixel. To be able to Aleuropteryx sp. were studied. Specimens were collected in front of open a larger amount of images in Amira, the images were con- the Museum of Natural History Vienna, Maria-Theresien-Platz in verted to greyscale. Every single section was imaged, imported and 2018 at Thuja sp., the specimen for the microCT was collected in aligned in Amira 6.3.0. Scheibbs, Lower Austria in 1995 at Juniperus communis. For Based on these reconstructions, the schematic drawing in Fig. 5 comparative purposes, microCT scans and histological sections of were made with Adobe Illustrator CC 2018. MicroCT image stacks the following specimens were studied: Chrysoperla carnea (Ste- are deposited in the Natural History Museum Vienna and the phens, 1836) (Chrysopidae), Chrysopa dorsalis Burmeister, 1839 University of Veterinary Medicine Vienna. Histological sections are (Chrysopidae), Podallea vasseana (Navas, 1910) (Berothidae), housed in the Natural History Museum Vienna, 2nd Zoological Mucroberotha vesicaria Tjeder, 1968 (Rhachiberothidae), Poly- Department. stoechotes punctata (Fabricius, 1793) (Ithonidae sensu Winterton and Makarkin, 2010), Micromus variegatus (Fabricius, 1793) (Hem- 2.6. Terminology erobiidae), Myrmeleon hyalinus distinguendus Rambur, 1842 (Myrmeleontidae). The classification of cephalic musculature follows Wipfler et al. (2011), of musculature of the circulatory system Wipfler and Pass (2014) and Friedrich and Beutel (2008) for thoracic musculature 2.2. Semithin-sections (Ivlm1, Fig. 6A; Ivlm3, Fig. 6A and B). In addition, the classification by von Keler (1963) is provided in brackets in the results section. Specimens were put to death with 96% alcohol and embedded in The terminology of the external head capsule follows Shepard Hard-Plus Resin. Semithin histological sections, 1 mm thick, were (1967) and the terminology of the mouthparts follows Meinander made with a diamond knife on a Leica EM UC7 (Ludwig Boltzmann (1972). Institute for Experimental and Clinical Traumatology) and stained
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