Arthropod Structure & Development 47 (2018) 430e441

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Arthropod Structure & Development

journal homepage: www.elsevier.com/locate/asd

Comparative morphology of the thorax musculature of adult

Anisoptera (Insecta: Odonata): Functional aspects of the flight
apparatus
€umler, Stanislav N. Gorb, Sebastian Büsse*
Fabian Ba
Department of Functional Morphology and Biomechanics Institute of Zoology, Kiel University, Am Botanischen Garten 9, 24118, Kiel, Germany

a r t i c l e i n f o a b s t r a c t

Article history: Due to their unique flight mechanism including a direct flight musculature, Odonata show impressive
Received 5 December 2017 flight skills. Several publications addressed the details of this flight apparatus like: sclerites, wings,
Received in revised form musculature, and flight aerodynamics. However, 3D-analysis of the thorax musculature of adult drag-
10 April 2018
onflies was not studied before and this paper allows for a detailed insight. We, therefore, focused on the
Accepted 16 April 2018
thorax musculature of adult Anisoptera using micro-computed tomography. Herewith, we present a
Available online 2 May 2018
comparative morphological approach to identify differences within Anisoptera: Aeshnidae, Corduliidae,
Gomphidae, and Libellulidae. In total, 54 muscles were identified: 16 prothoracic, 19 mesothoracic,
Keywords:
Dragonflies
and 19 metathoracic. Recorded differences were for example, the reduction of muscle Idlm4 and an
Functional morphology additional muscle IIIdlm1 in Aeshna cyanea, previously described as rudimentary or missing. Muscle
Muscle setup Iscm1, which was previously reported missing in all Odonata, was found in all investigated species. The
Insect flight attachment of muscle IIpcm2 in Pantala flavescens is interpreted as a probable adaption to its long-
X-ray tomography (mCT) distance migration behaviour. Furthermore, we present a review of functions of the odonatan flight
muscles, considering previous publications. The data herein set a basis for functional and biomechanical
studies of the flight apparatus and will therefore lay the foundation for a better understanding of the
odonatan flight.
© 2018 Elsevier Ltd. All rights reserved.

1. Introduction mechanism of Odonata provides impressive flight skills: Odonata

The ability to fly has been an important evolutionary develop-
ment, greatly promoting the success of winged insects (Pterygota)
(Grimaldi and Engel, 2005). Within Pterygota, the Odonata
(damsel- and dragonflies) are aerial key predators with outstanding
flight skills enabled by their highly derived flight apparatus (Pfau,
1986; Corbet, 2004; Büsse et al., 2013).
This flight apparatus with corresponding muscles, which are
responsible for the wing movements, is developed differently
among Pterygota (e.g. Snodgrass, 1935). Within all Pterygota e
except Odonata e the mechanism supplying the main power for
driving the wings is indirect; here large dorsal longitudinal muscles
deform the winged thoracic segments, whereas in Odonata the
musculature is connected via cap tendons to the wing base sclerites
and, therefore, directly to the wings (Clark, 1940; Tannert, 1958;
Hatch, 1966; Pfau, 1986; Büsse et al., 2013). This direct flight
* Corresponding author.
E-mail address: sbuesse@zoologie.uni-kiel.de (S. Büsse).
can operate all 4 wings separately, allowing them to hover, glide
and in some species even fly backwards (Hatch, 1966; Corbet, 2004;
Grimaldi and Engel, 2005; Rüppell and Hilfert, 2013). The flight
apparatus itself is located within the pterothorax (Matsuda, 1970) e
fusion of the meso- and metathorax e which is tilted caudally by
45
; the prothorax is rather small (Hatch, 1966; Dathe, 2003).
Pleurites of the pterothorax are enlarged in dorso-ventral direction,
whereas tergites and sternites are small in comparison to other
pterygote insects (Hatch, 1966). Additionally, the tergum is
twistable along the longitudinal axis, supporting the ability of
Odonata to operate their wing pairs separately (Hatch, 1966; Pfau,
1986; Dudley, 2002; Corbet, 2004).
Several publications address various aspects of the flight appa-
ratus of Odonata: sclerites (Chao, 1953; Russenberger, 1960;
Willkommen and Ho €rnschemeyer, 2007; Willkommen, 2008;
Ninomiya and Yoshizawa, 2009), musculature (Maloeuf, 1935;
Clark, 1940; Asahina, 1954; Büsse et al., 2013, 2015; 2018; Büsse
and Ho € rnschemeyer, 2013), wings (Wootton, 1991; Gorb, 1999;
Wootton and Newman, 2008; Appel and Gorb, 2011; Rajabi et al.,

https://doi.org/10.1016/j.asd.2018.04.003
1467-8039/© 2018 Elsevier Ltd. All rights reserved.
 €umler et al. / Arthropod Structure & Development 47 (2018) 430e441
F. Ba
2016a; 2016b), aerodynamics of the odonatan flight (Pfau, 1986;
Dudley, 2002; Brodsky, 1994), as well as the functional aspects of
the flight musculature and sclerites (Clark, 1940; Hatch, 1966; Pfau,
1986). In total, the thoracic musculature of Odonata gained more
interest recently (Büsse et al., 2013, 2015; 2018; Büsse and
Ho€rnschemeyer, 2013), showing that using modern methodology
can increase the knowledge even of already investigated taxa. For
example, by using micro-CT technique Büsse and Ho €rnschemeyer
(2013) identified nine previously unknown muscles for An-
isoptera larvae, although the taxa were previously studied
(Maloeuf, 1935; Snodgrass, 1954). Furthermore, the importance of
consistent and high-resolution morphological data for phyloge-
netic analysis was shown in Büsse et al. (2018).
We, therefore, focus in this study on the thoracic musculature
of adult Anisoptera in a comparative morphological approach
studying species of the main groups: Aeshnidae, Corduliidae,
Gomphidae, and Libellulidae. We included different ecological as-
pects when selecting the species. Two different hunting styles are
represented: perchers (e.g. Sympetrum striolatum) glean from a
substrate, fly out to catch a spotted prey and ingest it while sitting
again, while fliers (e.g. Aeshna cyanea) search, detect, pursuit,
capture and ingest their prey in midflight (Clark, 1940; Corbet,
2004). One species among these, the flier Pantala flavescens, is a
Libellulidae (all known to be perchers) that hunts in flier stile and
travels over long distances (Hobson et al., 2012). Using modern
techniques (e.g. mCT) in combination with traditional techniques
(e.g. dissection), we aim to identify previously overlooked differ-
ences as well as confirm already known characters within An-
isoptera and between the main groups of Odonata. Understanding
the flight apparatus, as the functional main component of the insect
flight, is crucial to understand the evolution and origin of the flight
itself. Furthermore, we present an extensive review of functions of
the odonatan flight muscles, based on previous works of Clark
(1940), Hatch (1966) and the seminal work of Pfau (1986). The
combination of these two datasets e comprehensive morphological
re-investigation and review of flight muscles functionalities e sets
a basis for functional and biomechanical studies of the flight
apparatus and will, therefore, lay the foundation for a better un-
derstanding of the odonatan flight.
2. Material and methods
Adult specimens of the following Anisoptera species of the main
groups of Odonata were studied: A. cyanea (Müller, 1764) (Aesh-
nidae), Cordulia aenea (Linnaeus, 1758) (Corduliidae), Libellula
depressa Linnaeus, 1758 (Libellulidae), Onychogomphus forcipatus
(Linnaeus, 1758) (Gomphidae), P. flavescens (Fabricius, 1798)
(Libellulidae), and S. striolatum (Charpentier, 1840) (Libellulidae).
All regulations concerning the protection of free-living species
were followed. All necessary permits for collecting Odonata in
Germany were obtained from the “Untere Naturschutzbeho € rde”. No
endangered or especially protected species were collected.
Specimens for high resolution X-ray tomography (mCT) were
fixed in an alcoholic Bouin solution (¼ Duboscq-Brasil) (Romeis,
1987), stored in 70% ethanol, dehydrated in an ascending ethanol
series, and subsequently critical point dried (Balzers CPD030) prior
to scanning. The scans were carried out using a SkyScan 1172
desktop micro-CT scanner (Bruker micro-CT, Kontich, Belgium) at
40 kV and 250 mA with images taken every 0.25
at a total of 180
.
The generated data were reconstructed using Nrecon®, the seg-
mentation of the data was done with Amira 6.2 (FEI SAS, France,
www.vsg3d.com) and for the visualization, the open source 3D
creation suite Blender (Blender Foundation, Netherlands, www.
blender.org) and Illustrator CS6 (Adobe System Inc., www.adobe.
com) was used.
431
Additionally, specimens for dissections were collected, freshly
frozen and stored at 70
C and studied in a stereo microscope
using micro scissors and forceps.
In all following descriptions, the non-moving end of each
muscle will be called point of origin and its moving end will be
called point of insertion. All muscle names follow the nomenclature
introduced by Friedrich and Beutel (2008) and the homologization
for Odonata by Büsse et al. (2013). Anatomical structures are
described using the nomenclature of Beutel et al. (2013), if neces-
sary supplemented by Asahina (1954), Hatch (1966), Ninomiya and
Yoshizawa (2009) and Büsse et al. (2013) e all used abbreviations
are shown in Table A.1 in the supplementary materials. For an
overview of sclerites and cuticular structures, see Figure B.1eB.4 in
the supplementary materials.
3. Results
Generally, conditions of morphological characters in
S. striolatum (Figs. 1e5) are used as reference. For all other species,
only characters that differ from S. striolatum are mentioned.
In total, 54 muscles were found in the thorax of all studied
species; for C. aenea, L. depressa, O. forcipatus, P. flavescens and
S. striolatum: 16 in the prothorax, 19 in the mesothorax and 19 in
the metathorax. The total amount is the same for A. cyanea, except
that it is missing the prothoracic muscle Idlm4 and has an addi-
tional metathoracic muscle IIIdlm1. Furthermore, the muscle Iscm1
was unknown for Anisoptera, but is present in all investigated
species. For an overview of the points of origin/insertion of all
muscles, see Table C.1 in the supplementary materials. Additionally,
mCT images of the musculature of all specimens are provided in the
supplementary materials (see Figure DeH). Furthermore, a list of
muscles, found in other publications can be found in the supple-
mentary materials as well (Table I).
3.1. Musculature of the prothorax
dlm e dorsal longitudinal muscles (Fig. 1)
Idlm3 - M. prophragma-cervicalis
Origin: Tergal apophysis 1 (TA1); broader attachment area in
C. aenea.
Insertion: Base of TA2.
Characteristics: Runs from the prothorax to mesothorax.
Idlm4 - M. cervico-occipitalis dorsalis
Origin: Lateral region of the apex of TA1.
Insertion: Median at the postocciput (Büsse et al., 2013); absent
in A. cyanea.
dvm e dorso-ventral muscles (Fig. 2)
Idvm13 - M. pronoto-trochantinalis anterior
Origin: Dorso-lateral area of the tergite 1, anterior to Idvm18;
more median in C. aenea.
Insertion: Anterior procoxal rim, median to Idvm15.
Characteristics: Intersects with Idvm15.
Idvm15 - M. propleuro-coxalis superior
Origin: Dorso-lateral part of the tergite 1, anterior to Idvm13;
more median in C. aenea.
Insertion: Anterior area of the procoxal disk, lateral to Idvm13.
Characteristics: Intersects with Idvm13.
Idvm18 - M. pronto-coxalis lateralis
Origin: Dorso-lateral part of the tergite 1, posterior to Idvm13;
more median with a broader attachment area in C. aenea.
Insertion: Posterior part of the procoxal rim, at the base of the
mesothoracic preepisternal sclerite.
pcm e pleuro-coxal muscles (Fig. 3)
Ipcm8 - M. propleuro-trochanteralis
Origin: Dorso-posterior part of the episternum 1.
432 €umler et al. / Arthropod Structure & Development 47 (2018) 430e441
F. Ba

Fig. 1. Dorsal longitudinal and ventral longitudinal muscles of Sympetrum striolatum (A e inner layer, B e outer layer). Three-dimensional visualisation from mCT data, lateral view.
At certain areas, the cuticle is made transparent to get a better look at muscles behind it.

Insertion: Tendon of the protrochanter. Characteristics: Same ventral tendon as Ipcm8.

Characteristics: Same protrochanter tendon as Iscm6. tpm e tergo-pleural muscles (Fig. 5)
scm e sterno-coxal muscles (Fig. 4) Itpm3 - M. pronoto-pleuralis anterior
Iscm1 - M. profurca-coxalis anterior Origin: Dorso-lateral area of the tergite 1, lateral at an apophysis
Origin: Lateral side of the base of profurca, anterio-ventral of lateral to the TA1, anterior to Idvm15; lateral of Idvm13/15 in
Iscm6. O. forcipatus.
Insertion: Anterior procoxal rim, ventral of Idvm15 and lateral to Insertion: Anterior part of episternum 1.
Idvm13. Characteristics: Short muscle; comparably small in C. aenea.
Characteristics: Dichotomous. Itpm7 - M. protergo-cervicalis posterior
Iscm2 - M. profurca-coxalis posterior Origin: Lateral region of the tergite 1, posterior to Itpm8.
Origin: Most ventral part of the profurca. Insertion: Lateral of the cervix membrane (Büsse et al., 2015),
Insertion: Postero-lateral procoxal rim. median to Itpm8.
Iscm6 - M. profurca-trochanteralis Characteristics: Runs postero-median to Itpm8.
Origin: Lateral side of the profurca. Itpm8 - M. protergo-cervicalis anterior
Insertion: Tendon of the protrochanter. Origin: Antero-lateral region of the tergite 1, anterior to Itpm7.
Fig. 2. Dorso-ventral muscles of Sympetrum striolatum (A e inner layer, B e middle layer, C e outer layer). Three-dimensional visualisation from mCT data, lateral view. At certain
areas, the cuticle is made transparent to get a better look at muscles behind it.
434 €umler et al. / Arthropod Structure & Development 47 (2018) 430e441
F. Ba

Fig. 3. Pleuro-coxal muscles of Sympetrum striolatum (A e inner layer, B e outer layer). Three-dimensional visualisation from mCT data, lateral view. At certain areas, the cuticle is
made transparent to get a better look at muscles behind it.

Insertion: Lateral of the cervix membrane (Büsse et al., 2015), Origin: Apex of the profurca.
lateral to Itpm7. Insertion: Cranial at the tentorial bar (Büsse et al., 2015).
Characteristics: Runs antero-lateral to Itpm7. Characteristics: Runs into the head capsule (Büsse et al., 2015);
Itmp9 - M. protergo-preepisternalis thicker in P. flavescens and L. depressa.
Origin: Dorso-lateral area of the tergite 1, at the anterior part of Ivlm7 - M. profurca-mesofurcalis
an apophysis lateral to the TA1, anterior to Itpm3. Origin: Apex of the mesofurca.
Insertion: Base of the prothoracic preepisternal sclerite. Insertion: Posterior part of the profurca.
Itpm11 - M. prosterna-coxalis sinister Characteristics: Runs from the mesothorax in the prothorax,
Origin: Lateral rim of the right procoxa. posterior dichotomous.
Insertion: Ventral surface of the prothoracic intestine (Büsse
et al., 2015).
Characteristics: Thin muscle running from the right to left side 3.2. Musculature of the mesothorax
(Büsse et al., 2015); it connects more dorsal in C. aenea and
L. depressa. dlm e dorsal longitudinal muscles (Fig. 1)
vlm e ventro longitudinal muscles (Fig. 1) IIdlm1 - M. prophragma-mesophragmalis
Ivlm3 - M. profurca-tentorialis Origin: Apex of TA3.
 €umler et al. / Arthropod Structure & Development 47 (2018) 430e441
F. Ba 435

Fig. 4. Sterno-coxal muscles of Sympetrum striolatum (A e inner layer, B e outer layer). Three-dimensional visualisation from mCT data, lateral view. At certain areas, the cuticle is
made transparent to get a better look at muscles behind it.

Insertion: Anterior edge of the base of the semi-detached scutal Insertion: On the edge of the SDSP2 lateral to IIdvm3; median to
plate 3 (SDSP3). IIdvm6 and anterior of IIdvm1 in P. flavescens.
dvm e dorsoventral muscles (Fig. 2) IIdvm5 - M. mesonoto-coxalis posterior
IIdvm1 - M. mesonoto-sternalis Origin: At the base of the mesocoxal disk.
Origin: Close to the point of origin of IIdvm3. Insertion: At the posterior region of the proximal costal plate 2
Insertion: SDSP2, lateral of IIdvm3, postero-median to IIdvm4. (pCP2), anterior to IIdvm6.
Characteristics: Short muscle with a long cap tendon in the Characteristics: Dorsal cap tendon.
middle of the cap tendon of IIdvm3 (dissection only), runs IIdvm6 - M. mesocoxa-subalaris
lateral to IIdvm3. Origin: Posterior area of the mesocoxal disk, posterior of
IIdvm3 - M. mesonoto-trochantinalis posterior IIdvm4/5.
Origin: Antero-median of the mesocoxal rim at the base of the Insertion: Anterior region of the axillary plate 2 (AxP2), poste-
mesothoracic preepisternal apodeme. rior to IIdvm4/5; at SDSP2 lateral of IIdvm4 in P. flavescens.
Insertion: At SDSP2. Characteristics: Muscle gets dorsally thin and sharp with a small
Characteristics: Dorsal dichotomous prominent muscle with a insertion area, big ventral attachment area.
big ventral cap tendon; not dichotomous in P. flavescens. pcm e pleuro-coxal muscles (Fig. 3)
IIdvm4 - M. mesonoto-coxalis anterior IIpcm1 - M. mesanepisterno-trochantinalis
Origin: Antero-lateral edge of the mesocoxal rim.
436 €umler et al. / Arthropod Structure & Development 47 (2018) 430e441
F. Ba

Fig. 5. Tergo-pleural muscles of Sympetrum striolatum (A e inner layer, B e outer layer). Three-dimensional visualisation from mCT data, lateral view. At certain areas, the cuticle is
made transparent to get a better look at muscles behind it.

Origin: Mesothoracic preepisternal sclerite antero-lateral to Insertion: Anterior edge of the mesocoxa.
IIpcm2; longer muscle in C. aenea and L. depressa; anterior and Characteristics: Muscle runs close to the pleuron, dorsal
partly surrounded by IIpcm2 in O. forcipatus, P. flavescens and attachment side is bigger than the ventral one.
C. aenea. IIpcm6 - M. mesopleura-trochanteralis
Insertion: Inserted at the anterior region of pCP2. Origin: Ventral part of the interpleural ridge, between katepi-
Characteristics: Short thin muscle with the long dorsal cap sternum 2 and katepimeron 2 and posterior to IIpcm4; closer to
tendon, lateral to IIpcm2. IIpcm2 in O. forcipatus.
IIpcm2 - M. mesobasalare-trochantinalis Insertion: Tendon of the mesotrochanter.
Origin: Mesothoracic preepisternal sclerite, mediano-lateral to Characteristics: Ventral tendon is the same as for IIscm6.
IIpcm1. scm e sterno-coxal muscles (Fig. 4)
Insertion: Lateral to IIpcm1 at anterior region of pCP2; broader IIscm3 - M. mesofurca-coxalis medialis
point of origin in P. flavescens. Origin: Lateral side of the mesofurca, posterior to IIscm6;
Characteristics: Most prominent muscle in the mesothorax with median of IIscm6 in O. forcipatus.
short dorsal cap tendon. Insertion: Posterior edge of the mesocoxa, median to IIdvm6.
IIpcm4 - M. mesanepisterno-coxalis posterior Characteristics: Posterior origin to IIscm6.
Origin: In the posterior region of katepisternum 2, close to the IIscm6 - M. mesofurca-trochanteralis
interpleural ridge and anterior of IIpcm6; closer to IIpcm2 in Origin: Lateral side of the mesofurca, anterior to IIscm3; lateral
O. forcipatus. of IIscm3 in O. forcipatus.
 €umler et al. / Arthropod Structure & Development 47 (2018) 430e441
F. Ba
Insertion: Tendon of the mesotrochanter.
Characteristics: Tendon is the same as for IIpcm6.
tpm e tergo-pleural muscles (Fig. 5)
IItpm3 - M. mesonoto-basalaris
Origin: At the base of the apophysis of the border between
scutellum 2 and postnotum 2, dorsal of the attachment point of
IItpm4.
Insertion: At the base of an apophysis in the middle of AxP2,
dorsal of the attachment point of IItpm4.
Characteristics: Runs dorsal of IItpm4.
IItpm4 - M. mesonoto-pleuralis anterior
Origin: At the apex of the apophysis of the border between the
scutellum 2 and postnotum 2, ventral of the attachment area of
IItpm3.
Insertion: At the apex of an apophysis in the middle of AxP2,
ventral of the attachment point of IItpm3.
Characteristics: Runs ventral of IItpm3.
IItpm6 - M. mesonoto-pleuralis posterior
Origin: Uppermost edge of the interpleural ridge 2 on the
anepimeron 2 side.
Insertion: Lateral on the anterior region of the SDSP2.
Characteristics: Large point or origin area.
IItpm7 - M. mesanepisterno-axillaris
Origin: At the ventral region of the intersegmental ridge
between katepimeron 2 and katepisternum 3; more anterior in
O. forcipatus.
Insertion: At the very posterior edge of AxP2.
Characteristics: Dorsal cap tendon.
IItpm8 - M. mesepimero-axillaris secundus
Origin: At the ventral part of the katepimeron 2, between
the interpleural ridge and the intersegmental ridge; smaller
attachment area and more anterior in O. forcipatus.
Insertion: At the centre region of AxP2.
Characteristics: Large point of origin area, anterior of IItpm7/10,
big dorsal cap tendon.
IItpm10 - M. mesepimero-subalaris
Origin: The ventral region of the intersegmental ridge between
anepimeron 2 and anepisternum 3.
Insertion: Posterior area of AxP2.
Characteristics: Runs between IItpm7 (lateral) and IItpm8
(median).
vlm e ventral longitudinal muscles (Fig. 1)
IIvlm6 - M. mesospina-abdominosternalis
Origin: Posterior end of preepisternal apodeme 3.
Insertion: Very end of katepimeron 3, close to the bar between
katepimeron 3 and first abdominal sternite, latero-posterior to
IIIvlm2; no posterior tendon in L. depressa.
3.3. Musculature of the metathorax
dlm e dorsal longitudinal muscles (supplementary
material D.1)
IIIdlm1 - M. mesophragma-metaphragmalis
Origin: TA4.
Insertion: Dorso-lateral area of the ridge between the thorax
and abdomen.
Characteristics: Only present in A. cyanea.
dvm e dorsoventral muscles (Fig. 2)
IIIdvm1 - M. metanoto-sternalis
Origin: Via a long transparent tendon in the middle of the cap
tendon of IIdvm3 (Dissection only).
Insertion: SDSP3, lateral of IIIdvm3, postero-median to IIIdvm4.
Characteristics: Long tendon, short muscle.
IIIdvm3 - M. metanoto-trochantinalis posterior
437
Origin: Antero-median of the metacoxal rim at the base of the
metathoracic preepisternal apodeme.
Insertion: At SDSP3.
Characteristics: Very prominent dorsal dichotomous muscle,
ventral cap tendon.
IIIdvm4 - M. metanoto-coxalis anterior
Origin: Antero-lateral rim of the metacoxa.
Insertion: On the antero-lateral region of SDSP3.
Characteristics: Antero-lateral to IIIdvm3.
IIIdvm5 - M. metanoto-coxalis posterior
Origin: Antero-lateral part of the metacoxal disk.
Insertion: At the very posterior edge of pCP3, posterior to
IIIdvm4/5.
Characteristics: Dorsal cap tendon.
IIIdvm6 - M. metanoto-coxalis posterior
Origin: Median region of the mesocoxal disk.
Insertion: Anterior region of AxP3.
IIIdvm8 - M. metanoto-phragmalis
Origin: At the posterior edge of the thoracic abdominal
apodeme.
Insertion: At an apophysis at the anterior edge of the first
abdominal tergite.
Characteristics: Long ventral cap tendon.
pcm e pleuro-coxal muscles (Fig. 3)
IIIpcm1 - M. metanepisterno-trochantinalis
Origin: At intersegmental ridge between the katepimeron 2 and
katepisternum 3.
Insertion: At the anterior edge of the SDSP3.
Characteristics: Short muscle, long cap tendons on both sides,
lateral to IIIpcm2.
IIIpcm2 - M. metabasalare-trochantinalis
Origin: With big attachment side at the metathoracic
preepisternal apodeme.
Insertion: At the anterior region of pCP3.
Characteristics: Large dorsal cap tendon, most prominent
muscle in the metathorax.
IIIpcm4 - M. metanepisterno-coxalis posterior
Origin: In the posterior region of the katepisternum 3, close to
the intersegmental ridge 3 and anterior to IIIpcm6.
Insertion: Antero-external edge of the metacoxa.
IIIpcm6 - M. mesopleura-trochanteralis
Origin: Posterior part of the katepisternum 3, close to the
intersegmental ridge 3 and posterior to IIIpcm4.
Insertion: Tendon of the metatrochanter.
Characteristics: Metatrochanter tendon is the same as for
IIIscm6.
scm e sterno-coxal muscles (Fig. 4)
IIIscm3 - M. metafurca-coxalis medialis
Origin: Lateral side of metafurca, ventral of IIIscm6, broad
attachment side.
Insertion: Postero-internal edge of the metacoxa, median of
IIIdvm6.
Characteristics: Ventral origin of IIIscm6.
IIIscm6 - M. metafurca-trochanteralis
Origin: Lateral side of the apex of the metafurca, median of
IIIscm3, broad attachment side.
Insertion: Tendon of the metatrochanter.
Characteristics: Same metatrochanter tendon as for IIIpcm6.
tpm e tergo-pleural muscles (Fig. 5)
IIItpm3 - M. metanoto-basalaris
Origin: At the base of an apophysis of the border of the post-
notum 3 and the first abdominal tergite, dorsal of the attach-
ment side of IIItpm4.
Insertion: At the base of an apophysis in the middle of AxP3,
dorsal of the attachment side of IIItpm4.
438 €umler et al. / Arthropod Structure & Development 47 (2018) 430e441
F. Ba
Characteristics: Runs dorsal of IIItpm4.
IIItpm4 - M. metanoto-pleuralis anterior
Origin: At the apex of an apophysis of the border of the post-
notum 3 and the first abdominal tergite, ventral of the attach-
ment side of IIItpm3.
Insertion: At the apex of an apophysis in the middle of AxP3,
ventral of the attachment side of IIItpm3.
Characteristics: Runs ventral of IIItpm3.
IIItpm6 - M. metanoto-pleuralis posterior
Origin: Uppermost edge of the interpleural ridge 3 on the side of
anepimeron 3.
Insertion: Lateral on the anterior region of the SDSP3.
IIItpm7 - M. metanepisterno-axillaris
Origin: At the anterior region of the ventral carina, postero-
median of IIItpm8; more anterior (O. forcipatus).
Insertion: At the very posterior edge of AxP3, medio-lateral to
IIItpm10.
Characteristics: Slender muscle, dorsal cap tendon.
IIItpm8 - M. metapimero-axillaris secundus
Origin: With a big attachment side at the ventral part of the
katepimeron 3; smaller attachment area in O. forcipatus.
Insertion: With a short cap tendon at the centre region of the
AxP3.
Characteristics: Big muscle with the short dorsal cap tendon.
IIItpm10 - M. metepimero-subalaris
Origin: At an apodeme between the katepimeron 3 and
poststernum 3.
Insertion: At the posterior edge of AxP3.
Characteristics: Slender muscle, dorsal tendon.
vlm e ventral longitudinal muscles (Fig. 1)
IIIvlm2 - M. mesofurca-abdominalis
Origin: Poststernal apodeme.
Insertion: Bar at the first abdominal segment.
4. Discussion
4.1. Muscles
A total number of 54 muscles in the entire thorax could be
confirmed for all investigated species. In nearly all species the same
muscles are present, except for A. cyanea; here the prothoracic
muscle Idlm4 is missing, but an additional metathoracic muscle
IIIdlm1 is present. In all investigated species, we found muscle Iscm1
that was previously reported to be absent in Anisoptera (Maloeuf,
1935; Büsse and Ho € rnschemeyer, 2013; Büsse et al., 2018). The
muscle Iscm1 controls the leg movement and was probably over-
looked in earlier investigations, because of its small size and the
closeness to the muscle Iscm6. It has the same points of attachment
at the base of the profurca (origin) and the procoxal rim (insertion) as
the muscles described by Friedrich and Beutel (2008); therefore, they
are hypothesized to be homologous. It seems that this character state
is exclusive to Anisoptera and has not been described for Odonata
until now (Maloeuf, 1935; Clark, 1940; Asahina, 1954; Hatch, 1966;
Büsse et al., 2013, 2015; 2018; Büsse and Ho € rnschemeyer, 2013).
The muscle Idvm13 has been previously declared as absent in
Anisoptera larvae by Büsse and Ho € rnschemeyer (2013), though it
was present in all investigated adult specimens. Maloeuf (1935)
described a muscle in Anisoptera larvae (muscle 13) that may be
homologous to Idvm15 in Anisoptera larvae described by Büsse and
Ho € rnschemeyer (2013). In adult Anisoptera, the larval muscle
Idvm15 splits up, forming Maloeuf (1935) muscle 13A that can be
homologized with Idvm13 and 13B that can be homologized with
Idvm15 (Maloeuf, 1935; Büsse and Ho € rnschemeyer, 2013). The
muscle Idvm13 is described as absent in larvae and adult species of
Zygoptera and Epiophlebia (Asahina, 1954; Büsse et al., 2013, 2015;
2018), which makes it unique for adult Anisoptera. The muscle
Idvm15 can be found in both Epiophlebia and Zygoptera, and it
shows a dichotomy in the studied larvae (Büsse et al., 2018, Fig. 3).
Additionally, muscle II/IIItpm3 is present in all investigated An-
isoptera species, although it was previously described as exclu-
sively present in all odonatan larvae (Büsse and Ho €rnschemeyer,
2013; Büsse et al., 2015, 2018).
The attachment points among the studied species differ in 14
muscles within the pterothorax (Muscles: IIdvm3, IIdvm4, IIdvm6,
IIpcm1/2, IIpcm4/6, IIscm3/6, IItpm7/8, IIvlm6, IIItpm7/8). Muscle
IIdvm3 appears not to be dichotomous in P. flavescens.
Additionally, both muscle II/IIIdvm4 and II/IIIdvm6 have
different points of insertion in P. flavescens in comparison to the
other species. While the insertion of II/IIIdvm4 is only slightly
shifted in medial direction, inserting lateral to the muscle II/
IIIdvm3 and anterior to II/IIIdvm1, the insertion of the muscle II/
IIIdvm6 appears to be completely different. It inserts at the SDSP2/
3 lateral of the muscle II/IIIdvm4. Therefore, its function is pre-
sumably purely elevating rather than supinating elevating (as
discussed later). In this case, no other muscle is left to supinate and
elevate the wing at the same time (working together with II/
IIIdvm5).
The muscle IIpcm1 appears to be comparably larger in L. depressa
and C. aenea than in S. striolatum, which might indicate an addi-
tional need for a better protection (Clark, 1940) against downward
deflection (as discussed later) in both species; caused for example
in extreme situations like territorial fights (Corbet, 2004). Further-
more, the point of origin of muscle IIpcm1 is antero-lateral to
muscle IIpcm2 in S. striolatum, L. depressa and A. cyanea; in
O. forcipatus, P. flavescens and C. aenea, however, IIpcm1 is partly
surrounded by muscle IIpcm2 from the lateral and median side -
this should not have any significant consequences for the function
of muscle IIpcm1. In S. striolatum, both muscles (II/IIIpcm1 and II/
IIIpcm2) have the same points of origin and insertion as in larvae
and adult species of Epiophlebia and Zygoptera (Asahina, 1954;
Büsse et al., 2013, 2015; 2018). In P. flavescens, the point of origin
of the muscle IIpcm2 is comparably larger than in any other
investigated species, indicating that P. flavescens could probably
generate a greater force for the wing depression resulting in a faster
acceleration (and speed of flight). Additionally, P. flavescens is
known to migrate over great distances (e.g., from North India to the
Maldives or East Afrika) for breeding (Anderson, 2009; Hobson
et al., 2012), which might be the most reasonable explanation for
this particular muscle arrangement.
The point of origin of the muscle IIscm3/6 is slightly shifted
caudally in O. forcipatus compared to all other species. The muscle
IIscm3 is located median of muscle IIscm6 instead of running
posterior to it. In S. striolatum, both muscles have the same points of
origin and insertion as in larvae and adult species of Epiophlebia
and Zygoptera (Asahina, 1954; Büsse et al., 2013, 2015; 2018). In the
metathorax of O. forcipatus, two differences in comparison to all
other species could be observed. The origin of the muscle IIItpm7 is
located comparably further anterior and the point of origin of the
muscle IIItpm8 appears to be smaller. The muscle II/IIIdvm1 has
already been described in adult Anisoptera (Clark, 1940; Hatch,
1966; Pfau, 1986) and was found in all investigated specimens,
although it was in most cases not traceable in the mCT scans and
could only be found by dissection. The muscle could be found in
adult Zygoptera and Epiophlebia as well (Asahina, 1954; Büsse et al.,
2013). Finally, there is an additional metathoracic muscle found in
A. cyanea, IIIdlm1 (discussed later). It was described by Pfau (1986)
as absent or rudimentary in all adult Anisoptera and only present in
larvae and adult species of Epiophlebia and Zygoptera (Asahina,
1954; Büsse et al., 2013, 2015; 2018) e but is present in larvae
(Büsse and Ho € rnschemeyer, 2013).
 €umler et al. / Arthropod Structure & Development 47 (2018) 430e441
F. Ba
4.2. Sclerites
In Odonata, the wing base sclerites are formed to serve as
important attachment structures for muscles (cf. Ninomiya and
Yoshizawa, 2009). In general, all 4 tergal apophyses (pin shaped
structures, formed from everted cuticle) e located in the dorsal
area of the thorax, at the tergum e serve as attachment structure
for dorsal longitudinal muscles (supplementary material B). TA1 - 3
can be found in all specimens, whilst TA4 is only existing in
A. cyanea and rudimentary in all other specimens. Additionally, all
animals have two dorsal semi-detached scutal plates (plate-like
structures, formed from everted cuticle) in the pterothorax
(supplementary material B), connected to the notum. SDSP2 is
located in the mesothorax, is 8-shaped and flexibly connected to
the notum by a pin-like structure in the middle of the dorsal side of
the SDSP. It serves as attachment structure for various dorso-
ventral muscles and muscle tpm6. The SDSP3 is more strongly
connected to the tergum at the anterior and posterior part without
the pin like structure in the middle and is of plate-like shape. This
prevents it from being tilted, likely resulting in a better force
transmission. This is true for all specimens except A. cyanea, where
the SDSP3 is more flexibly connected and of similar shape as SDSP2.
Those two differences might be crucial for the functioning of
A. cyanea's additional muscle IIIdlm1, serving as a steering muscle
to swing the hindwing in anterior direction. The present TA4 serves
as an attachment point for muscle IIIdlm1, while the more flexible
SDSP3 provides enough flexibility to swing the hindwing in ante-
rior direction. Also, the katepisternum in O. forcipatus is compa-
rably smaller than in the other species (supplementary material B).
It is located ventral of the anepisternum and between the katepi-
meron (caudal) and the mesothoracic preepisternal sclerite
(cranial).
4.3. Review of the odonatan flight muscle function
The flight apparatus and its musculature are one of the unique
features of Odonata, making them aerial key predators among in-
sects (Corbet, 2004). The muscles can functionally be subdivided in
active phasic and supporting tonic muscles and further grouped in
terms of their function for the flight apparatus, serving one or
different purposes e depressors/elevators and or steering muscles
(Hatch, 1966; Pfau, 1986). In general, all tonic muscles (Muscles:
II/IIIpcm1, II/IIIdvm1, II/IIItpm6, II/IIItpm10; Fig. 6E) function as
supporters for phasic muscles and are very important for the wings
movement along its longitudinal axis (Clark, 1940; Hatch, 1966;
Pfau, 1986).
The muscle II/IIIpcm1 applies a steady downward force to the
anterior part of the pCP2/3, to prevent the wing from an upward
deflection (Hatch, 1966). The muscle II/IIIdvm1 applies a steady
downward force to the SDSP2/3 and prevents the wing from a
downward deflection (Clark, 1940; Hatch, 1966). Due to the size
difference between these two muscles and their associated phasic
muscles, the phasic contraction of muscles II/IIIpcm1 and II/IIIdvm1
is hypothesized to be ineffective for the elevation/depression of
the wing (Pfau, 1986). Therefore, their tonic contraction probably
provides a further antagonistic function e the muscle II/IIIpcm1
counteracts the elevating movement of the muscle II/IIIdvm3
and II/IIIdvm1 counteracts the depressing movement of the muscle
II/IIIpcm2 (Pfau, 1986). This could enable the separate control of
speed and amplitude of the wing (Pfau, 1986).
The tonic contracting muscle II/IIItpm6 is special because it
affects the wing movement in both the depression and elevating
phase. The tergal bridge keeps the wing bases of both sides at
the same distance and, additionally, the distance between the
connection points of the wing base with the tergal bridge (Fig. 7 A,
439
TB) and the pleura (Fig. 7A, P) remains constant as well. There is a
dorsal membranous gap between the episterna of the mesothorax
and, while elevating and depressing the wings through phasic
muscles, the pleura of the pterothorax is oscillating in an opposite
direction of the force direction of the muscle II/IIItpm6 (Pfau,
1986). By pulling the interpleural ridge and, therefore, the
pleura in median direction (Fig. 7B and C), the muscle II/IIItpm6
functions alternately as a synergist and antagonist, depending in
which position the wing is (Pfau, 1986). It serves as a spring with
an adjustable drag. At the first part of each movement phase
(elevation or depression), the phasic muscle has to overcome the
resistance of the muscle II/IIItpm6 (this antagonist effect is shown
in Fig. 7A) and after a certain point is exceeded, II/IIItpm6 be-
comes the synergist (Fig. 7B and C). Additionally, Hatch (1966)
described the muscle II/IIItpm10 to apply a steady downward
force to the posterior area of AxP2/3 to provide wing supination.
Pfau (1986) extended this assumption, that the muscle mainly
supinates the wing due to its low contracting power and move-
ment in opposite direction of the elevating musculature, poten-
tially decelerating the upward movement with the properties of
an adjustable spring.
We agree with Pfau (1986), that the muscle IIdlm1 most likely
helps to move the forewings in an anterior direction by pulling at
the TA3. The SDSP2 is thereby lifted caudally, while the forewing
is swinging anteriorly at the end of the downstroke. The muscle
IIIdlm1 in A. cyanea serves a similar purpose: it pulls at the TA4
to lower the SDSP3 anteriorly and move the hindwing in a
posterior direction (Pfau, 1986). The muscle IIIdlm1 is just rudi-
mentary or reduced in most Anisoptera (Pfau, 1986), but present
in Zygoptera and Epiophlebia (Asahina, 1954; Pfau, 1986; Büsse
et al., 2013, 2015; 2018). Therefore, in A. cyanea, the SDSP3 is
shaped like the SDSP2 and connected to the wing bases in the
same way, whilst the SDSP3 in all other investigated Anisoptera
is connected more strongly to the wing bases, in order to support
a better force transmission from muscles to the wings and to
make the metathorax a purely power segment for the wing beat
(Pfau, 1986). Additionally, there is another muscle in Zygoptera
and Epiophlebia, antagonizing the movement of II/IIIdlm1. The
muscle II/IIItpm2 might function as an antagonist, bringing the
SDSP2/3 back into its original position (Asahina, 1954; Pfau, 1986;
Büsse et al., 2013).
The following phasic muscles can be divided in elevators
(Muscle: II/IIIdvm3, II/IIIdvm4, II/IIIdvm5, II/IIIdvm6 and II/IIItpm3
and II/IIItpm4; Fig. 6A) and depressors (Muscle: II/IIIpcm2,
II/IIItpm7, II/IIItpm8; Fig. 6B) (Clark, 1940; Hatch, 1966; Pfau, 1986).
For the downstroke: The muscle II/IIItpm8 mainly depresses the
wing by pulling at the centre of AxP2/3 and supinating it at the
same time (Hatch, 1966; Pfau, 1986). Pfau (1986) describes muscle
II/IIIpcm2 as a pure depressing muscle by applying a force to the
anterior part of the pCP2/3, but the explanation by Hatch (1966),
that the muscle also pronates the wing, seems reasonable. The
muscle II/IIItpm7 depresses the posterior end of the AxP2/3, to
supinate the wing as a possible antagonist to the muscle II/IIIdvm5
(Hatch, 1966; Pfau, 1986), but helps depressing it in the downward
movement of the wing as well (Pfau, 1986). For the upstroke: The
muscle II/IIIdvm3 elevates the wing evenly by applying a
depressing force to the SDSP2/3 (Clark, 1940; Hatch, 1966; Pfau,
1986). The muscle II/IIIdvm5 applies force to the pCP 2/3, in order
to mainly pronate the wing as an antagonist to the muscle II/
IIItpm7 and elevate it in an upward movement of the wing as well.
The muscle II/IIIdvm6 is connected to the anterior region of AxP2/3,
supinating the wing (Hatch, 1966; Pfau, 1986) and elevating it at the
same time. It probably supports the function of II/IIIdlm1 by
decelerating and keeping the wing supinated at the end of the
downstroke (Pfau, 1986).
440 €umler et al. / Arthropod Structure & Development 47 (2018) 430e441
F. Ba

Fig. 6. Schematic of the function of different flight muscles, anterior view. A e wing elevation, B e wing depression, C e wing pronation, D e wing supination, E e tonic muscles.
Abbreviations: AxP e axillary plate, d e dorsal, dvm e dorso-ventral musculature, l e lateral, m e median, pcm e pleuro-coxal musculature, pCP e proximal costal plate, tpm e
tergo-pleural musculature, v e ventral.

4.4. Conclusion found in A. cyanea and P. flavescens in comparison to all other

In summary, besides many minor differences within the thorax
of the studied adult Anisoptera, some major characteristics could be
found. In all investigated species we could identify three muscles
(Iscm1 and II/IIItpm3) previously undescribed for adult Anisoptera.
Also, Idvm13 (recently misinterpreted as Idvm15 in larvae by Büsse
and Ho €rnschemeyer, 2013) could be confirmed to be present in all
species. Furthermore, one missing muscle (Idlm4) and one addi-
tional muscle (IIIdlm1) could be confirmed for A. cyanea, accom-
panied by a semi-detached scutal plate 3 of specialized shape. We
could show the value of a re-investigation using modern tech-
niques (e.g. mCT) with traditional techniques (e.g. dissection), for
identifying previously overlooked differences as well as for con-
firming already known characters. Although differences could be
species, no significant differences were discovered regarding
different hunting stiles (flier, percher).
Our results are confirmatory to all remarks regarding the
evolution and phylogeny of Odonata recently made by Büsse et al.
(2018). All 19 synapomorphies for the sister group relationship of
Odonata [Epiprocta þ Zygoptera] (cf. Misof et al., 2014), as well as
the 4 synapomorphies for Epiprocta [Epiophlebia þ Anisoptera]
(cf. Bybee et al., 2008; Blanke et al., 2012, 2015; Misof et al., 2014)
itself could be confirmed (Büsse et al., 2018). In more detail, the
synapomorphies for Anisoptera: absence of muscle Iscm4, pres-
ence of muscle IIscm2, absence of muscle IIscm4, position of
muscle IItpm8 anterior of muscle IItpm10, position of muscle
IIIpcm1 posterior of muscle IIIpcm2, insertion of muscle IIIpcm4 at
the antero-external edge of the metacoxa, origin of muscle IIIscm6

Fig. 7. Antagonistic and synergistic functions of the muscles II/IIItpm6. A e wing initial, B e wing depression, C e wing elevation. Black arrows show the direction of the force
produced by the muscles; white arrow shows the direction, in which the cuticle is deformed by flight musculature; grey arrows show the resulting movement direction of the wing.
Abbreviations: d e dorsal, dvm3 e dorso ventral muscle 3, l e lateral, m e median, P e pleura, SDSP e semi-detached-scutal plate, TB e tergal bridge, tpm6 e tergo pleural muscle 6,
tpm8 e tergo-pleural muscle 8, v e ventral.
 €umler et al. / Arthropod Structure & Development 47 (2018) 430e441
F. Ba
at the latero-external face of the metafurca, position of muscle
IIItpm7 median of muscle IIItpm10 (Büsse et al., 2018) could
be confirmed and the presence of muscle Iscm1, Idvm13 and
II/IIItpm3 could be added as new synapomorphies for Anisoptera.
The review of functions of the odonatan flight muscles, based on
previous works of Clark (1940), Hatch (1966) and the seminal work
of Pfau (1986) e latter only available in German e, will help to un-
derstand the functionality of this highly complex character system.
This all together will lay a basis for functional and biomechanical
studies of the flight apparatus, for example for muscular manipu-
lation experiments. Here our study can help considerably to detect
single muscles of interest and identify the functional effects of a
manipulation.
Acknowledgements
We are grateful for the support by the members of the Functional
Morphology and Biomechanics Group at Kiel University, especially
€ hnsen. SB is directly supported through the DFG
to E. Appel and A. Ko
grant BU3169/1-1. The project is partly financed through the DFG
“Forschungsgroßgera €te” grant INST 257/405-1 FUGG. Many thanks
to J. Ware (Rutgers University, Newark, USA), F. Suhling (Technische
Univesita€t Braunschweig, Braunschweig, Germany) and B. Kunz
(Langenburg, Germany) for providing specimens.
Appendix A. Supplementary data
Supplementary data related to this article can be found at
https://doi.org/10.1016/j.asd.2018.04.003.
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