Research Article |
Corresponding author: Thies H. Büscher ( stu101562@mail.uni-kiel.de ) Academic editor: Benjamin Wipfler
© 2017 Thies H. Büscher, Stanislav N. Gorb.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Büscher TH, Gorb SN (2017) Subdivision of the neotropical Prisopodinae Brunner von Wattenwyl, 1893 based on features of tarsal attachment pads (Insecta, Phasmatodea). ZooKeys 645: 1-11. https://doi.org/10.3897/zookeys.645.10783
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The euplantulae of species from all five genera of the Prisopodinae Brunner von Wattenwyl, 1893 were examined using scanning electron microscopy with the aim to reveal the significance of attachment pads regarding their phylogenetic relationships. The split into the conventional two sister groups is supported by the two-lobed structure of the euplantulae with a smooth surface in the Prisopodini and a nubby surface microstructure in the Paraprisopodini. The two lineages are well distinguishable by this feature, as well as by the shape of the euplantulae themselves. The functional importance of the attachment pad surface features is discussed.
Phasmatodea , tarsus, euplantulae, Neotropis, scanning electron microscopy
The Prisopodinae Brunner von Wattenwyl, 1893, which occur exclusively in Central and South America, were erected by
Various attachment devices have evolved on the tarsi and pretarsi of hexapods (
One species per genus has been examined from dried specimens using scanning electron microscopy (SEM). Living animals were anaesthetised with CO2 and then decapitated. The right metatarsi were dissected at the level of the tibia and fixated in 2.5% glutaraldehyde in PBS buffer on ice on a shaker for 24 h. To soften and reactivate the attachment pads from the tarsi of dried insects, the legs were cut off, rehydrated in a relaxing chamber for 24 h, and then stored in a 10% solution of lactic acid (
The tarsi of M. antillarum consist of very broad tarsomeres bearing large, roundish euplantulae. The arolium is smaller than the euplantulae. The euplantulae form two separated lobes diverging in lateral direction of the tarsus (Fig.
Scanning electron micrographs of the tarsal morphology of different Prisopodinae species. From left to right: Overview; Fourth euplantula; Adhesive microstructure. Scale bars: 1 mm; 300 μm; 5 μm. Melophasma antillarum, female (A–C). Paraprisopus merismus, female (D–F). Prisopus horstokkii, female (G–I). Dinelytron grylloides, female (J–L). Damasippus sp., female (M–O).
Similar to M. antillarum, the euplantulae of P. merismus cover a proportionally significant area of the ventral side of tarsomeres, but form hemispherical attachment pads. The arolium is likewise reduced in size (Fig.
The representatives of the Prisopodini are also distributed in Central and South America (
In general the tarsus of Pr. horstokkii has a similar appearance to other Prisopodini, but in detail the tarsal morphology of Prisopus reveals unique characters in comparison to the other Prisopodinae. The tarsus is not symmetrical as in the other species, but broadened apically. Additionally, the tarsal setae on the dorsal side of the tarsomeres are much longer in comparison to the other examined genera. The euplantulae of this species are similar to the other Prisopodini, with euplantulae consisting of two bars (Fig.
In comparison to the tarsi of the Paraprisopodini, the tarsus and the euplantulae of D. grylloides are more slender. Except the first tarsomere, the euplantulae consist of two thin bars traversing the tarsomere and dividing it centrally. The euplantula on the long basitarsus is limited to a small bilobed pad (Fig.
The examined specimens are captive-bred from individuals which have been found in Monteverde, Costa Rica and which do not belong to any described species. Similar to D. grylloides, the tarsi of this Damasippus sp. individual are slender with a long basitarsus. The euplantulae consist of two bars as well (Fig.
In
Due to the shortening of the basitarsus observed in the Paraprisopodini the entire tarsal chain looks shorter than in the Prisopodini. With such geometry, the adhesive force is generated nearer to the body of the insect, which might provide some advantage for controlling attachment and detachment. The Paraprisopodini are camouflaged well in resting position with their legs pulled towards their body. Longer legs on the contrary may be useful for taking longer strides and therefore run faster (
All species of the Prisopodinae bear a euplantula on the tarsomere V, which is not the case in all species of the Phasmatodea (
The two lineages can be distinguished by the morphological features of the tarsi. The Paraprisopodini bear round, bilobed attachment pads with a nubby adhesive ultrastructure, which correspond to the shape found in many other species of the Phasmatodea (cf.
The Prisopodini’s euplantulae on the contrary consist of two thin bars, which are interpreted as an apomorphy of this lineage and support the monophyly of it. Additionally the lack of nubs on the euplantulae is not part of the ground plan in the Euphasmatodea (
The examined species of Damasippus is found in Costa Rica in dampy and windy habitats. The flying adults are in need of effective attachment organs in order to adhere securely on different substrates when landing, since a fall to the ground would cause troubles to the large animals living up in the tree canopies. The flight of the examined species is not sufficiently effective to return to the foliage without high efforts, but their specialisation to the food plants necessitates a distribution close to them. Considering the slightly concave shape of the euplantulae in this lineage, they may function as a suction cup, generating strong attachment force on rather smooth substrates. It is plausible to assume that, if the bars meet together, they form an ellipse and seal the surrounded volume. The generation of the suction effect can be presumably performed by haemolymph pressure control within the euplantulae (cf.
Additionally, both lineages differ significantly in their surface microstructure. So far the nubby surface of the Paraprisopodini is exclusively found in other species with reduced wings. The apterous species Neohirasea maerens (Brunner von Wattenwyl, 1907), Aretaon asperrimus (Redtenbacher, 1906) (
From the functional point of view, smooth phasmid attachment pads demonstrate strong adhesive and frictional performance on smooth substrates, whilst the nubby pad surface seems to be the adaption to a broader range of substrate textures (
The species M. antillarum bears euplantulae, which are known to mainly generate friction, but possesses a reduced arolium, which generates adhesion (
Within the Prisopodinae two types of attachment pads are found coherently for the two previously suggested lineages (Paraprisopodini and Prisopodini). It is shown here that characters of attachment pads are useful for distinguishing these lineages. The Paraprisopodini bear big and roundish bilobed euplantulae, as most other known Euphasmatodea, whilst the Prisopodini bear two-bared euplantulae with a groove intersecting the entire tarsomere as an apomorphy. Additionally, the two lineages can be distinguished by the micromorphology of the pad surface. Whilst the Paraprisopodini bear nubby euplantulae with specific densities of nubs, the Prisopodini’s euplantulae are smooth without any micromorphological features. Both macroscopical and microscopical characters contribute to the differentiation of the two lineages, which formerly were distinguished by the tegmina only. The use of the pad surface microstructure for the phylogeny of these groups is suggested in this study for the first time. To validate the monophyly of the former Prisopodinae and their location within the Pseudophasmatinae a more comprehensive study of the attachment ultrastructures of the Phasmatodea in combination with upcoming transcriptome analyses are suggested.
We thank Alexander Kovalev and Esther Appel (Department of Functional Morphology and Biomechanics, Kiel University, Germany) for providing help in the preparation of the samples for SEM. Harald Bruckner (NHM Vienna, Austria) is thanked for supplying detailed images of the tarsi of type specimen housed in the phasmid collection in the Natural History Museum Vienna, Austria. We thank Marco Gottardo (Department of Life Sciences, University of Siena, Italy), Sven Bradler (Department of Morphology, Systematics, and Evolutionary Biology, Georg-August-Universität Göttingen, Germany) and Rolf Beutel (Institute of Systematic Zoology and Evolutionary Biology, Friedrich Schiller University Jena, Germany) for helpful comments on the manuscript. Amoret Spooner (OUMNH Oxford, UK) and Judith Marshall (
Coll. TB Private collection of Thies Büscher, Kiel, Germany
OUMNH University Museum of Natural History Oxford, UK
HT Holotype
ST Syntype
PT Paratype
SEM Scanning electron microscope
Damasippus sp.; coll. TB: 2♂♂, 2♀♀; one female examined via SEM
Damasippus sp.;
Damasippus batesianus (Westwood, 1859); OUMNH, HT: 1♂
Damasippus discoidalis Redtenbacher, 1906;
Damasippus fuscipes Redtenbacher, 1906; NHW, ST: 2♂♂, 1♀
Damasippus fuscipes Redtenbacher, 1906;
Damasippus striatus Redtenbacher, 1906; OUMNH: 1♀
Damasippus zymbraeus (Westwood, 1859); OUMNH, ST: 2♂♂, 1♀
Damasippus zymbraeus (Westwood, 1859); OUMNH: 1 nymph
Dinelytron agrion Westwood, 1859;
Dinelytron agrion Westwood, 1859; OUMNH: 1♂
Dinelytron grylloides Gray, 1835; coll. TB: 1♀; examined via SEM
Melophasma antillarum coll. TB: 6♂♂, 6♀♀; one female examined via SEM
Melophasma vermiculare Redtenbacher, 1906; NHW, ST: 2♀♀
Paraprisopus sp.;
Paraprisopus merismus (Westwood, 1859); coll. TB; 1♀; examined via SEM
Paraprisopus merismus (Westwood, 1859);
Paraprisopus foliculatus Redtenbacher, 1906; NHW, ST: 1♀
Prisopus ariadne Hebard, 1923;
Prisopus berosus Westwood, 1859;
Prisopus berosus Westwood, 1859; OUMNH: 1♂
Prisopus cepus Westwood, 1859; OUMNH, HT: 1♂
Prisopus cepus Westwood, 1859; OUMNH: 2♀♀, 1 nymph
Prisopus cornutus Gray, 1835; OUMNH: 1♂
Prisopus cornutus Gray, 1835;
Prisopus horridus (Gray, 1835); OUMNH: 1♀
Prisopus horstokkii (Haan, 1842); coll. TB: 3♂♂, 1♀; one female examined via SEM
Prisopus horstokkii (Haan, 1842);
Prisopus phacellus Westwood, 1859;
Prisopus phacellus Westwood, 1859;
Prisopus phacellus Westwood, 1859; OUMNH: 2♀♀
Prisopus sacratus (Olivier, 1792); OUMNH: 3♂♂, 2♀♀, 2 nymphs
Prisopus sacratus (Olivier, 1792);
Prisopus sacratus (Olivier, 1792);
Prisopus spiniceps Burmeister, 1838; OUMNH: 1♀