ArticlePDF Available

Functional morphology of the mandibular apparatus in the cockroach Periplaneta americana (Blattodea: Blattidae)-A model species for omnivore insects

Authors:

Abstract and Figures

We examine the functional morphology of the mandibular apparatus, including its driving muscles, of the generalist insect Periplaneta americana using a combination of μ-computed tomography and geometrical modelling. Geometrical modelling was used to determine the changes of the mean fibre angle and length in the mandibular adductor muscle over the physiological range of mandible opening. The roughly scissor-like mandibles are aligned along the dorso-ventral axis of the head and are characterised by sharp interdigitating distal teeth, as well as a small proximal molar region. The mechanical advantage of the mandibles, i.e. the ratio between inner and outer levers, ranges between 0.37 to 0.47 depending on the considered incisivus. The mandibular abductor muscle is comprised of eight muscle fibre bundles, which are defined by distinct attachment positions on the sail-like apodeme protruding from the medio-lateral basis of the mandibles into the head lumen. Compared to carnivorous, herbivorous, or xylophagous insects, the relative volumes of the mandibular abductor and adductor muscle are small. Dependent on the mandible opening angle, the mean fibre angle of the adductor muscle ranges from 34° to 21°, while mean fibre length changes from 1.24 mm (closed mandible) to 1.93 mm at maximum mandible opening. Many of the specific morphological features found in the chewing apparatus of P. americana, such as the presence of a mola in combination with distal incisivi, small relative muscle size and the intermediate fibre angle can be understood as adaptations to its omnivorous life style.
Content may be subject to copyright.
477
ISSN 1863-7221 (print)
|
eISSN 1864-8312 (online)
© Senckenberg Gesellschaft für Naturforschung, 2015.
73
(3): 477 – 488
23.12 . 2 015
Functional morphology of the mandibular apparatus
in the cockroach Periplaneta americana (Blattodea:
Blattidae) – a model species for omnivore insects
T W *, 1, T K
2, S N. G
2 &
B W *, 3
1 Insect Biomechanics Group, Dept. of Zoology, University of Cambridge, Downing Street, Cambridge CB2 3EJ, UK; Tom Weihmann * [tw424
@cam.ac.uk] — 2 Functional Morphology and Biomechanics Group, Kiel University, Am Botanischen Garten 9, 24118 Kiel, Germany —
3 Entomology Group, Institut für Spezielle Zoologie und Evolutionsbiologie mit Phyletischem Museum, Friedrich-Schiller-Universität Jena,
Erbert Str. 1, 07743 Jena, Germany; Benjamin Wipfler * [benjamin.wipfler@uni-jena.de] — * Correspond ing author
Accepted 30.ix.2015.
Published online at www.senckenberg.de/arthropod-systematics on 14.xii.2015.
Editor in charge: Frank Wieland.
Abstract
We examine the functional morphology of the mandibular apparatus, including its driving muscles, of the generalist insect Periplaneta
americana using a combination of µ-computed tomography and geometrical modelling. Geometrical modelling was used to determine
the changes of the mean bre angle and length in the mandibular adductor muscle over the physiological range of mandible opening. The
roughly scissor-like mandibles are aligned along the dorso-ventral axis of the head and are characterised by sharp interdigitating distal
teeth, as well as a small proximal molar region. The mechanical advantage of the mandibles, i.e. the ratio between inner and outer levers,
ranges between 0.37 to 0.47 depending on the considered incisivus. The mandibular abductor muscle is comprised of eight muscle bre
bundles, which are dened by distinct attachment positions on the sail-like apodeme protruding from the medio-lateral basis of the mandi-
bles into the head lumen. Compared to carnivorous, herbivorous, or xylophagous insects, the relative volumes of the mandibular abductor
and adductor muscle are small. Dependent on the mandible opening angle, the mean bre angle of the adductor muscle ranges from 34° to
21°, while mean bre length changes from 1.24 mm (closed mandible) to 1.93 mm at maximum mandible opening. Many of the specic
morphological features found in the chewing apparatus of P. americana, such as the presence of a mola in combination with distal incisivi,
small relative muscle size and the intermediate bre angle can be understood as adaptations to its omnivorous life style.
Key words
Comparative morphology, insect, head, mouth parts, skeleton, muscles, mandibles, biting, chewing.
1. Introduction
Insects are the largest group of organisms in terms of
species number (Grimaldi & EnGEl 2005) and provide
a major part of the animal biomass. Although they are
in the focus of attention of many organismic biolo-
gists, there still remain many functional aspects that are
sparsely studied. One of these aspects is the physiology
of ingestion and food processing. With the dawn of the
µ-computed tomography (µ-CT) technique, internal mus-
cle architecture has become increasingly widely used for
phylogenetic analyses (e.g. FriEdrich et al. 2014; WipFlEr
et al. 2015). However, since most morphological studies
rely on individual specimens, they largely disregard in-
traspecic variation and specic ontogenetic adaptations.
Even if mean values and measures of dispersion were
W et al.: Cockroach chewing apparatus
478
provided, anatomical description alone does not provide
evidence to determine functional consequences of the
muscles and associated skeletal arrangements and struc-
ture (WEihmann et al. in press). In particular, this holds
for arthropods since physiological muscle properties are
much more variable than in vertebrates (Jahromi 1969;
Taylor 2000). Muscles, in turn, are the drivers of almost
all animal movements. Their arrangement in the skeletal
system, structure, and their physiological properties de-
termine the movement capabilities of an animal. Muscle
function and emerging capabilities of the powered limbs
have decisive impact on the development, behaviour,
interactions with the environment, and the evolution of
species.
Locomotion, mating and food acquisition are biolog-
ical functions that rely on muscle powered limbs, i.e.
the typical arthropod mouthparts in the case of feeding.
In many insects, specically those with biting-chewing
mouthparts, the paired mandibles are the strongest parts
responsible for biting and reducing larger food items into
smaller digestible pieces. Thus, they are indispensable for
food acquisition, grinding, and intake. Alongside these
key features, mandibles are also used for defence and ag-
gression, digging, feeding nest mates or offspring, cling-
ing, and transport (chapman 1995; clissold 2007).
The mechanics of neopteran insects’ mandibles is
relatively simple; they can be characterised as two class
3 levers working against each other (clissold 2007).
For each mandible, the driving forces are generated pre-
dominantly by a single adductor muscle and transmitted
to teeth edges or grinding ridges at its distal parts. The
adductor is attached to the median basis of the mandible
and is antagonised by a much weaker abductor muscle at-
taching at the lateral basis of the mandible. In neopteran
insects, the mandibles are connected to the head capsule
via simple hinge joints, whose rotational axes are dened
by anterior and posterior condyli (e.g. snodGrass 1944;
paul 2001; BlankE et al. 2012). Therefore, a mandible
can move only in a single plane. This makes the mechan-
ics of the biting process (schmiTT et al. 2014) much sim-
pler than for instance those of the ying or walking ap-
paratuses (maiEr et al. 1987; ahn & Full 2002; siEBErT
et al. 2010). Therefore, the experimental and analytic ef-
fort is reduced, which also reduces the effort of future
comparative studies leading to a better understanding of
interactions between single parts of a whole functional
unit.
Bite mechanics is largely underexplored in insects,
and detailed morphological data including physiological
examinations are notoriously rare. The largest body of
literature deals with the biting physiology of the chelae
of larger crustacean species, which comprise some of the
strongest biters in the animal kingdom (Taylor 2000).
Additionally, there are some papers about biting in some
orders of the chelicerates (van dEr mEiJdEn et al. 2012,
2013). However, in crustaceans, scorpions and solpugids,
the structures responsible for strong biting are chelae or
chelicerae. This is in stark contrast to insects where the
driving muscles are not situated in these limbs but rath-
er within the head capsule. Some papers deal with the
functional morphology and neuronal control of mandi-
ble movements in insects (GorB & BEuTEl 2000; paul &
GronEnBErG 2002; li et al. 2011), but only few studies
focused on the determination of bite forces. WhEaTEr &
Evans (1989) examined maximum bite forces and man-
dible closer size in several ground and rove beetles. Goy-
Ens et al. (2014) recently measured bite forces of stag
beetles. The carnivorous ground beetles exhibit special-
ized predatory mandibles while the stag beetles’ enlarged
mandibles are used primarily in male male ghts for
mating opportunities and not for food processing.
As a rst step to a more general understanding of in-
sect biting, we examine the structure of the mandibles
and associated muscles in the omnivore cockroach Peri-
planeta americana. A detailed examination of the head
morphology and anatomy of this species is provided by
WEissinG et al. (in press). schmiTT et al. (2014) studied
the movement of the mandible with in vivo X-ray radi-
ography. In conjunction with the exerted voluntary bite
forces of P. americana, which were studied by WEihmann
et al. (2015), here we provide a detailed study of insect
biting relying on anatomical and physiological data from
eight specimens. We analysed bre angles and lengths
of the major bre bundles of six mandibular adductor
muscles (m. craniomandibularis internus (0md1)) and
provide the relative sizes of adductor and abductor mus-
cles (m. craniomandibularis externus posterior (0md3))
of seven other hemimetabolous insect species from four
different insect orders. Moreover, the results for these
omnivore, xylophage, carnivore, and herbivore species
are compared with the conditions found in P. americana.
Finally, we draw inferences on the functioning of biting-
chewing mouthparts of insects in general, and compare it
with those of crustacean chelae and chelicerae of solpu-
gids.
2. Methods
The present study is based on eight adult specimens of
Periplaneta americana. They originated from a labora-
tory colony at the Institut für Spezielle Zoologie und
Evolutionsbiologie of the Friedrich-Schiller-Universität
Jena, Germany. The colony exists since 2012 and was
originally derived from professionally bred animals
(available at: www.schaben-spinnen.de). The animals
were kept at room temperature (23 25°C) in perspex
cages and fed twice a week with porridge oats; water
was provided ad libitum. The animals used in the present
study had a mean body mass of 1.12 ± 0.17 g. The same
animals were previously examined with respect to the
voluntary bite forces (WEihmann et al. 2015). With these
experiments we also determined the opening range of the
mandibles. Voluntary opening angles ranged from 46° to
about 100°, with the former meaning completely closed
mandibles, i.e. the condition used for µ-CT-examinations
479
ARTHROPOD SYSTEMATICS & PHYLOGENY — 73
(3) 2015
(see below). Despite the much larger range of voluntary
movements, signicant bite forces were obtained only
between 55° and 85° of mandible opening. At angles
smaller than 55° the interactions of the two mandibles
with the force sensor hampered further mandible closure
and therefore the measurement of reliable force values.
At angles larger than 85° passive forces of the joint
structure dominates mandible closing (see WEihmann et
al. 2015). After measuring the biting forces, the animals
were decapitated immediately and killed by freezing
(– 18°C) for several minutes. Afterward we transferred
them to 70% ethanol.
The opening angle of a mandible was dened as the
angle between the horizontal line, and the length axis of
a mandible (oa; Fig. 1E). The length axis of a mandible,
in turn, was dened as the line from the anterior condyle
of the mandible joint to the tip of the distal most tooth
(ma; Fig. 1E). Both measures, horizontal line and man-
dible axis, were acquired from video recordings, which
occurred synchronously with the force measurements.
During the process of lming, the labrum was folded up
and xed, to guarantee a clear view on the mandibles.
The system of coordinates was aligned individually.
Thus, the horizontal plane was spanned by the joint axes
of the left and right mandible joints with the connect-
ing line between the two anterior condyles dening the
horizontal axis of the head (Fig. 1A,D). The transverse
plane was dened by these condyles and was always per-
pendicular to the horizontal plane. The sagittal plane, in
turn, subtends the horizontal plane along the centreline
between the anterior condyles and is perpendicular to
both, the horizontal and the transverse plane. The inter-
section line of the horizontal and the sagittal planes also
denes the length axis of a cockroach’s head.
For µ-computed tomography (µ-CT), the heads of
the specimens were dried with hexamethyldisilazane and
mounted on a sample holder. The scans were performed
on a Skyscan 1172 (Bruker, Kontich, Belgium) that was
operated at an acceleration voltage of 40 kV and a current
of 250 µA. The exposure time for a single x-ray image
was 720 ms; x-ray projections were captured over a full
360° rotation of the specimen at steps of 0.130°. The x-
ray images were then converted into a volumetric data
set that consisted of isometric voxels with a voxel size of
3.07 µm. This volumetric µ-CT data (Fig. 1C) was ana-
lysed with Visage Imaging Amira 5.2.2 (Visageimaging,
San Diego, USA) using the length and volume measure-
ment tools. Illustrated volume renders were implemented
with VG Studiomax 2.2 (Volume Graphics GmbH, Hei-
delberg, Germany). The µ-CT scans are deposited in the
collection of the Phyletisches Museum in Jena, Germany
(scans 4 12 in Polyneoptera / Blattodea / Periplaneta ame-
ricana).
All morphological and anatomical measures were
taken from the 3D data provided by the µ-CT scans.
The general morphological terminology follows sEiFErT
(1995) and for the musculature WipFlEr et al. (2011). For
each specimen, we determined characteristic measures
of both mandibles. These measures were the positions of
the anterior and posterior condyles, the attachment po-
sition of the adductor tendon to the mandible base and
the positions of the mandible teeth. They were used to
determine the respective distances to the joint axis, i.e.
the lengths of the inner and outer levers, and to determine
the angles between them (Fig. 1E). Thereby, the lengths
of the inner and outer levers were dened as the distances
of the teeth, or the attachment of the adductor tendon,
perpendicular to the joint axis (Fig. 1E, Table 3). The ef-
fective inner lever, which is pivotal for the efciency of
the force transmission, was dened as the length of the
projection of the line between the joint axis and the ten-
don attachment point onto the horizontal line (Fig. 1E).
Despite immediate transfer to ethanol, only three speci-
mens (1.16 ± 0.1 g) had sufciently well preserved bres
of the adductor muscle for further examination. From
these three specimens we examined the left and the right
mandibular adductor and abductor muscles.
We distinguished eight distinct compartments in the
mandibular adductor muscle (m. craniomandibularis in-
ternus), which are dened by their origin on the tendon
(Fig. 2). The abductor muscle (m. craniomandibularis
externus posterior) is much smaller and does not divide
into different compartments. Fibre length and bre an-
gle of ve muscle bres that were evenly distributed in
the bundle were determined for each of the eight major
compartments of the adductor and for the abductor. We
selected one bre in the centre of the bundle and four
close to the end points of the dening axes of the roughly
elliptic cross section of the bre bundles. Additionally,
we measured the effective cross sectional area of the
eight compartments of the adductor and that of the ab-
ductor at their widest parts, i.e. we determined the area of
an elliptic envelope of virtual sections perpendicular to
the predominant bre orientation with the length measur-
ing tool of Visage Imaging Amira 5.2.2. The bre angles
were determined with respect to the major direction of
the muscle force (mf-fa; Fig. 1E,F), which was dened
as the direction from the attachment point of the tendon
at the mandible base to the centre point of a muscle’s
attachment area at the head capsule. The mean values of
bre length and angles were calculated individually for
each bre bundle and weighted according to the relative
contribution of the single bundles to the total cross sec-
tion area of a mandibular adductor. In this way, the mean
bre length and angle of the mandible adductor were
determined individually for the positional conditions
during µ-CT imaging at which mandibles were closed,
i.e. with maximally shortened adductor muscles. Muscle
length changes and angular changes, then, were calcu-
lated based on these weighted means averaged across all
examined specimens.
The position of the tendon attachment changes when
a mandible rotates around its pivot axis. Depending on
the length of the inner lever and the opening angles of
the mandibles, dorso-ventral and lateral displacements
were determined (see results), which led to correspond-
ing length changes and angular changes of the muscle
bres. Potential length changes of the tendon are negli-
W et al.: Cockroach chewing apparatus
480
gible as insect tendons usually are about 40 times stiffer
than those of vertebrates (BEnnET-clark 1975; kEr et al.
1988). Since lateral displacements were only about 0.3
mm and small compared to the total length of the muscle
tendon system of about 3.8 mm (see results), their im-
pact on the bre length and angle changes is negligible.
Thus, calculations of the mean bre length change and
mean angle change rely only on displacements in dorso-
ventral direction (see results section). By applying this
dorso-ventral displacement on the mean bre length and
angle, length and angular changes were calculated as
changes in a right-angled triangle with the lengthening
leg lying onto the major direction of the muscle force (cp;
Fig. 1E,F). For the calculation of the bre length chang-
es, i.e. those of the hypotenuse, the Pythagorean theorem
was applied. Angular changes were calculated accord-
ingly as changes in the angle between the leg of the right-
angled triangle in parallel with the main force direction
and the hypotenuse by using trigonometric functions. All
lengths, angles, changes, and statistics were calculated
with MATLAB R2010a (The MathWorks, Natick, MA,
USA). All variance in measurements is standard devia-
tion (mean ± s.d.).
Muscle and head capsule volumes of P. americana
were measured with the volume measure tool of Ami-
ra 5.2.2. The volume of the head capsule included the
mouthparts and eyes but not the antenna. The volume of
the muscles includes the respective tendon. These val-
Fig. 1. A: right mandible of Periplaneta americana in anterior view; B: left mandible of Periplaneta americana in anterior view; C: µ-com-
puted tomographical section of the head capsule; mandibular adductor muscle in blue, mandibular abductor muscle in red, pharynx in
green; D: coordinate system of the head capsule; E: distances, points and angles on the mandible; F: angles and directions on the man-
dibular tendon. — Abbreviations: I IV: incisivi; abm: mandibular abductor muscle; adm: mandibular adductor muscle; eil: effective inner
lever; fu: fulcrum; hp: horizontal plane; il: inner lever; il-ol: angle between outer and inner lever for the 2nd incisivi; mf: main direction of
muscle force; ma: mandibular axis or outer lever of the 1st incisivus; mf-fa: angle between the main direction of the muscle force and one
muscle bre; mr: mandibular molar region; oa: opening angle of the mandible; ol: outer lever of the 2nd incisivi; ph: pharynx; sp: sagittal
plane; tp: transverse plane. Scale bars: 0.5 mm.
481
ARTHROPOD SYSTEMATICS & PHYLOGENY — 73
(3) 2015
ues were also measured for other polyneopteran line-
ages with different diets, for which µ-CT scans of the
head were available in the collection of the Phyletisches
Museum, Jena, Germany: the xylophagous termite Mas-
totermes darwiniensis and cockroach Salganea sp., the
omnivorous roach Ergaula sp., the insectivorous mantid
Hymenopus coronatus (WipFlEr et al. 2012) and gryllo-
blattodean Galloisiana yuasai (WipFlEr et al. 2011) as
well as the herbivorous phasmatodeans Phyllium siccifo-
lium (FriEdEmann et al. 2012) and Timema sp. (one indi-
vidual studied respectively).
3. Results
3.1. Mandibular morphology
In the resting position, the mandibles of P. americana
are oriented along the dorso-ventral axis. Thus, compa-
rable to scissor blades, they act as a pair of sharp cutting
edges moving closely past each other, allowing shear-
ing of tough materials. In contrast to scissors, however,
each mandible has its own pivot and their axes are tilted
towards each other. On average the angles between the
joint axes and the sagittal plane were about 17 ± 2°, with
the posterior condyles positioned more laterally than the
anterior ones.
The teeth of the mandibles intercalate with each oth-
er, and thus left and right mandibles have to be slightly
unsymmetrical. The left mandible has four distal teeth
while the right has only three teeth. The distances of
the teeth towards the joint axes vary (Table 3), but the
distances from the distal-most teeth to the joint axes are
both about 2.52 mm (± 0.13 in the right and ± 0.10 in the
left mandible) and do not differ signicantly from each
other (t-test, p = 0.34). The distances from the joint axes
to the 3rd left and 2nd right teeth were 2.33 ± 0.11 mm and
2.32 ± 0.10 mm, respectively, which was also very simi-
lar (p = 0.95). The teeth have different shapes; particular-
ly the 3rd left and 2nd right teeth are characterised by sharp
proximal edges. With closed mandibles the length of the
muscle tendon complex of the mandibular adductor was
3.8 mm ± 0.16 mm (i.e. the length from the attachment of
the tendon at the mandible base to the centre point of the
muscle attachment area at the head capsule).
3.2. The morphology of the mandibular
adductor muscle and its tendon
In P. americana the mandibular adductor tendon is an
elongate structure with varying degrees of sclerotization.
It is attached on the mesal basal edge of the mandible.
This articulation zone is not sclerotized and therefore
highly exible. However, manual testing showed that in
alcohol preserved specimens the apodemes’ material is
denatured and conveys the impression of high resilience
to bending which is not the case in fresh specimens. From
this articulation, in the frontal view, the tendon continues
as a roughly triangular, sail-like, planar structure into the
lumen of the head capsule (Fig. 2). Close to the mandibu-
lar articulation the basal wing of the tendon is located
on the lateral side of the tendon. Both disto-mesal and
disto-lateral wings are attached distally (see also g. 11
in WEissinG et al. in press).
In both hemispheres of the head of all studied speci-
Fig. 2. Bundles of the right mandibular adductor muscle (m. craniomandibularis internus, 0md1) and abductor muscle (m. craniomandibu-
laris externus posterior, 0md3) of Periplaneta americana, 3D-reconstruction based on µ-computed tomography. A: frontal view; B: dorsal
view; C: posterior view. — Abbreviations: 0md3: M. craniomandibularis externus posterior; a – h: bundles of M. craniomandibularis
internus; as: antennal socket; atb: anterior tentorial bridge; ce: compound eye; ct: corpotentorium; fr: frons; md: mandible; mt: tendon of
M. craniomandibularis internus; pg: postgena; ve: vertex.
W et al.: Cockroach chewing apparatus
482
mens of P. americana the adductor can be divided into
eight distinct compartments. These muscle bre bundles
have dened areas of origin on the mandibular tendon
(Table 1; Fig. 2). In principle, the attachment of the
mandibular adductor on the head capsule is fan-shaped,
i.e. the attachment areas of the single bre bundles are
mostly oriented along the length axis and lined up along
medio-lateral directions (Fig. 2). Only the bundles b and
h deviate from this pattern and attach exclusively on the
posterior wall of the head capsule. Although all bundles
can be identied in both hemispheres, where they have
the same origin on the tendon, the structure of some bun-
dles differed consistently between the hemispheres. This
difference is reected by increased standard deviations
of the cross-section areas (e.g. bundle e in Table 2). In
two specimens, the right adductor seems to be somewhat
larger than the left one; in the third specimen, however,
it appears to be the opposite. Though the imbalances
might be a consequence of the asymmetric dentition of
right and left mandibles, deducing a general trend does
not seem to be reasonable at this stage due to the small
sample size. Therefore, we conned our analyses to the
averages of left and right muscles of all three specimens
(see below). Nevertheless, the issue with the mandibu-
lar asymmetry should be examined in more depth with
larger sample sizes in the future.
Bundle
Origin
Insertion
Comment
alaterally on the dist al part of the basal wing and
the entire lateral wing latero-posterior vertex the most lateral bundle
balong the entire ventral surface of the basal wing
of the mandibular tendonpostgena, laterad the foramen occipitale a broad bundle
c mesal side of the lateral wing of the tendonalong the entire antero-posterior vertex, mesal to
bundle a and laterally of d and e the biggest bundle
dposterior edge of the mesal wing of the tendon
anterior vertex, mesal to bundle c; in the right
hemisphere with two dinstinct subcomponents
while the left hemisphere has only one. The
additional mesal subcomponent of the right
bundle attaches in the midsagittal area, anterior
to bundle f of the left hemisphere.
forms a column with bundle e
ealong the entire lateral side of the mesal wing of
the tendon
posterior vertex, mesal to bundle c and lateral of
bundles g and f, directly posterad bundle d. In
the right hemisphere with two distinct
subcomponents, in the left one with only one.
forms a column with bundle d
fposterio-mesal edge of the mesal wing of the
tendonanterio-mesal vertex the most anterior bundle of
the mesal row
g mesal side of the mesal wing of the tendonmesally on the vertex, posterior to bundle f and
anterior to bundle h
the mesal bundle of the
mesal row
hventro-mesal edge of the mesal wing of the
mandibular tendon
mesally on the dorsal edge of the foramen
occipitale
the thinnest bundle of the
muscle
Bundle
Origin
I
nsertion
Comment
alaterally on the dist al part of the basal wing and
the entire lateral wing latero-posterior vertex the most lateral bundle
balong the entire ventral surface of the basal wing
of the mandibular tendonpostgena, laterad the foramen occipitale a broad bundle
c mesal side of the lateral wing of the tendonalong the entire antero-posterior vertex, mesal to
bundle a and laterally of d and e the biggest bundle
dposterior edge of the mesal wing of the tendon
anterior vertex, mesal to bundle c; in the right
hemisphere with two dinstinct subcomponents
while the left hemisphere has only one. The
additional mesal subcomponent of the right
bundle attaches in the midsagittal area, anterior
to bundle f of the left hemisphere.
forms a column with bundle e
ealong the entire lateral side of the mesal wing of
the tendon
posterior vertex, mesal to bundle c and lateral of
bundles g and f, directly posterad bundle d. In
the right hemisphere with two distinct
subcomponents, in the left one with only one.
forms a column with bundle d
fposterio-mesal edge of the mesal wing of the
tendonanterio-mesal vertex the most anterior bundle of
the mesal row
g mesal side of the mesal wing of the tendonmesally on the vertex, posterior to bundle f and
anterior to bundle h
the mesal bundle of the
mesal row
hventro-mesal edge of the mesal wing of the
mandibular tendon
mesally on the dorsal edge of the foramen
occipitale
the thinnest bundle of the
muscle
B
undle
Origin
Comment
alaterally on the dist al part of the basal wing and
the entire lateral wing latero-posterior vertex the most lateral bundle
balong the entire ventral surface of the basal wing
of the mandibular tendonpostgena, laterad the foramen occipitale a broad bundle
c mesal side of the lateral wing of the tendonalong the entire antero-posterior vertex, mesal to
bundle a and laterally of d and e the biggest bundle
dposterior edge of the mesal wing of the tendon
anterior vertex, mesal to bundle c; in the right
hemisphere with two dinstinct subcomponents
while the left hemisphere has only one. The
additional mesal subcomponent of the right
bundle attaches in the midsagittal area, anterior
to bundle f of the left hemisphere.
forms a column with bundle e
ealong the entire lateral side of the mesal wing of
the tendon
bundles g and f, directly posterad bundle d. In
the right hemisphere with two distinct
forms a column with bundle d
fposterio-mesal edge of the mesal wing of the
tendonanterio-mesal vertex the most anterior bundle of
the mesal row
g mesal side of the mesal wing of the tendonmesally on the vertex, posterior to bundle f and
anterior to bundle h
the mesal bundle of the
mesal row
hventro-mesal edge of the mesal wing of the
mandibular tendon
mesally on the dorsal edge of the foramen
occipitale
the thinnest bundle of the
muscle
Table 1. Origins at the mandible apodeme and insertions at the head capsule of the mandible closer bundles (M. craniomandibularis inter-
nus) in Periplaneta americana.
Table 2. Fibre lengths, bre angles, cross section areas (in mm2 and % of the entire muscle) and volume (in mm3 and % of the entire mus-
cle) of the eight muscle bre bundles of the mandibular adductor of Periplaneta americana.
bundle length
[mm]
angle
[°]
area
[mm2]
area
[%]
volume
[mm3]
volume
[%]
mean std mean std mean std mean std mean std mean std
a 1.17 ±0.18 30.30 ±6.0 0.53 ±0.05 23.90 ±2.6 0.78 ±0.09 24.78 ±2.53
b 1.17 ±0.19 39.70 ±5.9 0.50 ±0.08 22.50 ±2.3 0.62 ±0.11 19.39 ±1.46
c 1.52 ±0.25 41.90 ±15.3 0.33 ±0.05 14.70 ±2.4 0.60 ±0.15 18.62 ±3.18
d 1.00 ±0.05 59.80 ±5.7 0.21 ±0.06 9.30 ±2.1 0.23 ±0.10 6.93 ±2.31
e 1.34 ±0.23 11.00 ±7.6 0.38 ±0.14 17.20 ±6.5 0.60 ±0.25 18.59 ±5.06
f 1.11 ±0.1 41.60 ±14.1 0.13 ±0.05 5.70 ±2.2 0.16 ±0.04 5.03 ±1.44
g 1.25 ±0.08 26.40 ±11.1 0.12 ±0.04 5.20 ±1.9 0.14 ±0.05 4.79 ±2.02
h 1.29 ±0.15 30.60 ±6.5 0.03 ±0.01 1.50 ±0.6 0.06 ±0.02 1.87 ±0.55
483
ARTHROPOD SYSTEMATICS & PHYLOGENY — 73
(3) 2015
3.3. Characteristic lengths and angles
with closed and open mandibles
Subsequent to the straining physiological experiments
and the preparation for the µ-CT scans, the resting posi-
tion of the mandibles could be reliably identied only in
two right and four left mandibles. The resultant position
of the mandible base, i.e. the inner lever, was close to
the horizontal line when mandibles were closed (right:
4.6 ± 1.1°; left: 0.1 ± 1.2°). The inner levers were about
0.92 mm in both mandibles (right: 0.92 ± 0.06 mm;
left: 0.92 ± 0.09 mm). A rotation of this lever about the
joint axis results in positional changes of the mandibles.
Within the range of signicant bite forces (55° to 85° of
mandible opening), this change corresponds to a dorso-
ventral displacement of the tendon of about 0.45 mm.
Changes from closed to maximally opened mandibles
lead to a displacement of 0.7 mm. Since the orientation
of the muscle changes only marginally with increasing
mandible opening (see methods section) the effective le-
ver, i.e. the horizontal distance between the pivot and the
attachment of the tendon, reduces by about 30% when
considering the range from closed to maximally open
mandibles. If we consider those opening angles, where
considerable bite forces were measured, i.e. from about
55° to 85°, the effective lever decreased by only 18%.
Hence, the effective mechanical advantage (EMA), i.e.
the quotient of the effective inner lever to the outer le-
ver, changed too. The ratio of the distances between pivot
and tendon attachment on the one side and pivot and the
outer lever on the other side are constant and dene the
mechanical advantage (MA) of specic teeth. Depend-
ing on the tooth considered (Table 3), this ranged from
0.37 to 0.47. Here, the position of the 2nd right and 3rd left
teeth seems to be of particular signicance. Both teeth
are well developed and their proximal rims are cutting
edges; their MA is about 0.39.
Volumes and cross sectional areas of the eight bre
bundles differ strongly from each other, but their individ-
ual contributions to the cross sectional area of the whole
muscle are relatively constant among the measured spec-
imens (Table 2). On average the mandibular adductors
had a cross sectional area of about 2.23 ± 0.24 mm2. The
bundles a, b, c and e were the largest bre bundles mak-
ing up about 78% of the whole muscles’ cross sectional
area (Fig. 2; Table 2), which was calculated by summing
up the cross sectional areas of the single bundles. The
mean weighted bre angle is about 34° whereas single
bre bundles deviate markedly from this value (Table
2). The mean weighted bre length was about 1.24 mm
while the mean lengths of the single bre bundles ranged
from 1 to 1.52 mm.
When the cockroach mandibles open, the length of the
effective inner lever, the mean bre length, and the mean
bre angle change markedly (Fig. 1E,F). Starting from
closed mandibles the mean bre angle decreases from
about 34° to about 21° at maximally opened mandibles
(Fig. 3). At mandible opening from 55° to 85°, the mean
bre angle changes from about 31° to 23°. The mean -
bre length increases nearly linearly from 1.24 mm with
closed mandibles to 1.93 mm at 100° mandible opening.
In the range from 55° to 85°, the bre length changes from
about 1.36 mm to 1.76 mm; this corresponds to a relative
increase of 35% and 23%, respectively. Fibre length and
opening angle are almost linearly related. Thus, the as-
cending limb of the relationship of bite force and opening
angle, which occurs between 55° and 62° corresponds to a
mean muscle bre length range from 1.36 mm to 1.46 mm
(Fig. 3). The force plateau, between 62° and about 75°
(WEih mann et al. in press), corresponds to bre lengths
from 1.46 mm to 1.63 mm and the descending limb to -
bre length between 1.63 mm and about 1.76 mm (Fig. 3).
Muscle pennation results in muscle bre stresses
higher than whole muscle stresses (paul & GronEnBErG
1999). According to its dependency on the cosine of the
pennation angle, the differences are larger the higher the
muscle pennation angle. The pennation of mandibular
adductors is maximal when the mandibles are closed and
decreases with increasingly opened mandibles. Thus,
muscle bre stress is up to 20% higher than whole mus-
cle stress when mandibles are closed and the mean pen-
nation angle gains its maximum value of 34°. At maxi-
mally opened mandibles, the mean pennation angle is
only about 21° and the surplus in bre stress, thus, is
only about 7%. In the range from 55° to 85° mandible
opening, the pennation decreases from 31° to 23° which
results in bre stress values exceeding that of the whole
muscle by about 17% and 9% respectively.
Fig. 3. Changes of A: the mean bre length and B: the mean bre
angle of the mandibular adductor muscle of Periplaneta americana
for the mandible opening angles between 48° and 100°.
W et al.: Cockroach chewing apparatus
484
4. Discussion
The mouthparts of P. americana, especially the mandi-
ble, and its mechanics were the focus of recent studies
(schmiTT et al. 2014; WEihmann et al. 2015; WEissinG et
al. in press). Their mandibles are roughly triangular cut-
ting devices. In contrast to mechanical shears and scissors
their mechanics are characterized by two independent
joint axes such that there is usually no point of intersec-
tion if the animal grasps a piece of food. On the contrary,
the cutting edges of the two mandibles are typically di-
vided by a relatively wide spacing. While only the distal
parts of the mandibles are characterised by sharp edges
and teeth, the more proximal parts, i.e. those which could,
in principle, make up a point of contact between the op-
posed mandibles, are blunt and not suitable to generate
shear forces. Thus, the mechanism of cockroach mandi-
bles is rather analogous to staggered pairs of parrot beak
pruners. Initially, the tips of the mandible teeth perforate
the outer surface of a food item and then the proximal
edges of the teeth cut apart the material (see Figs. 1, 2)
cut apart the material. Only when the opening angles of
the mandibles are small, the cutting edges of some teeth
can interact like scissor blades and may generate signi-
cant shear forces. Here, particularly the second right and
the third left teeth seem to have the capacity to form a
structure similar to the carnassial structure of carnivore
mammals enabling P. americana to cut up stringy matter
such as brous plant and animal materials.
P. americana, as many other roaches, is an omnivo-
rous insect (BEll et al. 2007). This diet is also reected
in their mandibular apparatus. Each mandible has distal
incisivi as well as a proximal grinding area, the mola
(Fig. 1A,B; WEissinG et al. in press). Carnivorous in-
sects such as dragonies or mantids lack the mola and
therefore have a mesal cutting edge (BlankE et al. 2012;
WipFlEr et al. 2012) while the mesal side of the mandible
of herbivorous insects contains a sole grinding area (e.g.
FriEdEmann et al. 2012).
Adaptations towards the generalized lifestyle can
also be found in the mean bre angle of the mandibu-
lar adductor. For adductors with elongated apodemes
and only little horizontal width, paul & GronEnBErG
(1999) proposed a geometrical model. It predicts that for
maximum bite force generation the optimum bre angle
is 45° whereas maximum closing velocities are reached
with bres aligned along the force direction. Thus, most
insect species should adopt muscles with intermediate -
bre angles. With 34° at closed mandibles, the mean bre
angle in P. americana is similar to many non-specialized
ants (paul & GronEnBErG 1999). In contrast, the bre
angles are as small as 15° in fast predatory ants while
muscle bres in herbivorous, leaf-cutter and seed eating
ants attach at angles steeper than 40° (paul & GronEn-
BErG 1999). Although most literature refer to measure-
ments with closed mandibles, from a functional point of
view, bre angles should be obtained at the force plateau
of a mandibular adductor. In P. americana this plateau is
reached at mandible opening angles between 62° and 75°
(WEihmann et al. 2015). Here, the mean bre angles are
smaller and reach angles between 25° and 28°.
A small mechanical advantage (MA), i.e. the quotient
of the inner lever to the outer lever results in a smaller
force output in the mandible. However, the potential max-
imum velocity of the mandible tip increases and the time
necessary to close the mandibles decreases. Accordingly,
the detritivore larva of the beetle Liocola exhibits a rather
high MA of 0.54 (GorB & BEuTEl 2000). The mandibles
of predatory aquatic beetle larvae of the species Hydro-
philus and Cybister, which in turn rely on fast attacks
on rather soft-bodied prey are comparatively slender and
have MA values of 0.28 and 0.26 respectively (GorB &
BEuTEl 2000). Additionally, the mandibles of Hydrophi-
lus larvae have a prominent cutting ridge (retinaculum)
at their median central part, which allows the cracking
of snail shells by taking advantage of the much higher
mechanical advantage (GorB & BEuTEl 2000). Male stag
beetles (GoyEns et al. 2014), which use their elongated
mandibles in their notorious ghts for mating opportuni-
ties have also the need for fast actions. Thus, depending
on the bite positon, MA values of male mandibles range
Table 3. Distances in the mandibles of Periplaneta americana. —
Abbreviations: il = inner lever i.e. distance between joint axis and
tendon attachment; ol1 ol4 = outer lever i.e. distances between
joint axis and the mandible teeth 1 to 4 (distal to proximal).
Table 4. Angles between the inner lever (il) and outer levers (ol) for
all incisivi of Periplaneta americana.
485
ARTHROPOD SYSTEMATICS & PHYLOGENY — 73
(3) 2015
from 0.13 to 0.28, while the MA of female mandibles is
about 0.34. In carnivorous ground and rove beetles MA
values range between 0.35 and 0.59 (WhEaTEr & Evans
1989) and 0.18 and 0.46 (li et al. 2011) respectively.
Both examinations present the MA of the distal most
teeth of the mostly single-toothed predatory mandibles.
Similar values are measured in Periplaneta americana.
They range from 0.37 to 0.47 from the distal most to the
proximal incisivi with 0.39 in the second right and third
left which are the strongest teeth. Thus the omnivorous
lifestyle of Periplaneta americana is not reected in the
mechanical advantage.
With closed mandibles, the position of the inner lever
almost coincides with the horizontal line, i.e. the line be-
tween the two anterior condyles. Therefore, the force of
the adductor muscle is optimally transmitted to the man-
dibles’ teeth and edges in this condition. However, the
orientation of the single muscle bres may deviate sig-
nicantly from the current direction of the main muscle
force. In the transverse plane the bre angles of the bun-
dles f and a deviate up to 60° from each other (Figs. 1,
2). Therefore, depending on the opening angle of the
mandibles, differential or sequential activation patterns
are conceivable, i.e. lateral bundles are active primarily
when opening angles are small and medial bre bundles
show highest activity when opening angles are high.
However, it has been previously found in ants (paul &
GronEnBErG 2002) that posterior and lateral bres are
probably not recruited differentially, although fast mus-
cle bres, lumped together in specic muscle subunits,
can be activated independently.
Most of the bre bundles gain attachment area and
therefore effective cross-sectional area by spreading out
in anterio-posterior direction at the curved dorsal wall
of the head capsule (Fig. 2B). In this way, the attach-
ment areas largely match the effective cross-sectional
areas. Only bundle b and h attach almost exclusively at
the posterior wall of the head capsule. Their attachment
areas are signicantly larger than the cross-sectional ar-
eas. Accordingly, the forces generated by these muscle
bundles are distributed over a relatively larger area and
this decreases the tensile loading of the comparatively
at posterior wall of the head capsule, which probably is
not optimised to withstand high tensile forces.
The maximum bite force of P. americana is about
0.5 N (WEihmann et al. 2015). However, this study used
a 2D-force sensor which allowed only for the discrimina-
tion of medio-lateral and dorso-ventral bite forces. An-
terio-posterior force components could not be resolved.
Though the movability of the mandibles is largely re-
stricted to the transverse plane, the joint axes of the man-
dibles are tilted with regard to the length axis of the head
by about 17°. Consequently, and according to trigono-
metric functions, absolute mandible forces were up to 6%
higher than the measured resulting forces. Thus, muscle
forces and stresses might also be higher. In contrast to
the tilted joint axes, the blades and cutting edges of the
mandibles are almost aligned in parallel to the transverse
plane. The anterio-posterior force components, therefore,
primarily seem to facilitate shovelling of the reduced
food towards the oesophagus and do not contribute to the
biting forces themselves.
If applying the log10 transformation of the bite force
quotient (BFQ), i.e. maximum bite force/body weight0.66
as suggested by van dEr mEiJdEn et al. (2012), the re-
sulting logBFQ is 0.99 for P. americana. This quotient
should be independent of body mass and therefore allow
comparisons between different sized animals (van dEr
mEiJdEn et al. 2012). Male stag beetles of the species
Cyclommatus metallifer can generate bite forces of up
to 9 N with a body mass of about 1.36 g (GoyEns et
al. 2014) which results in logBFQ of 2.19. Even higher
values can be expected for leaf-cutter ants. With an es-
timated bite force of more than 1 N (WEihmann et al.
2015, supporting information: S1 Text) and a body mass
of about 20 mg, the ants’ logBFQ exceeds 2.45. Thus,
insects with specialized mandibular apparatus that al-
low them to clutch opponents or cut tough leaves exhibit
much higher values than omnivorous P. americana. For
chelate crustaceans, scorpions and solpugids the values
range from 0.98 to 2.96, where the highest values were
attained in crustaceans (Taylor 2000; van dEr mEiJdEn
et al. 2012). Apparently insects, arachnids and crusta-
ceans include species with moderate to very distinct
biting abilities. However, a comparison between insects
and crustaceans is difcult since all crustaceans stud-
ied so far use their chelae rather than their mandibles to
crush prey. Moreover available literature mostly refers
to species specialised for slow and hard-shelled prey.
Thus their bite forces are expected to be above non-
specialist species (van dEr mEiJdEn et al. 2012; Taylor
2000). Crustaceans are arguably the most morphologi-
cally diverse group of arthropods, but the species stud-
ied so far do not reect this actual biodiversity. From
a phylogenetic point of view, insects are in fact a ter-
restrial group of crustaceans (e.g. misoF et al. 2014). In
contrast to chelae, mandibles are independently driven
and work against each other. However, according to
Newton’s 3rd law, one moveable lever with only one ad-
ductor acting against a rigid counterpart, in principle,
can apply the same biting force as mandibles of the same
size with equally sized adductors. The advantages of
two independently driven blades seems not to primarily
be to increase bite force but rather reduce length changes
of the adductors when the animals encompass and cut
food pieces of a certain size. That is because the working
ranges of both sides add up, and high opening angles can
be achieved with only half the muscular length change.
As a consequence, the adductors can act closer to their
optimum length of 1.46 mm to 1.63 mm in P. americana
(WEihmann et al. 2015), which results in increased ef-
ciency. More over, the effective closing velocity is high-
er for a given mean sarcomere and bre length because
the velocities of both sides also add up. If no particularly
fast actions are needed, the muscles can still act closer to
isometric conditions, which increases the maximum bit-
ing force or efciency again (hill 1938; WEndT & GiBBs
1974; croW & kushmErick 1982).
W et al.: Cockroach chewing apparatus
486
The rather low maximum bite forces exerted by P.
americana are also reected by the relative small vol-
ume of the adductor muscles relative to the head cap-
sule (Table 5; Fig. 4). In the three studied specimens of
P. americana, the mandible adductors represented about
14.6% ± 3.8% of the entire volume of the head capsule.
The only lower value (11.9%) was observed in the like-
wise omnivorous cockroach Ergaula sp. With the excep-
tion of the mantid Hymenopus coronatus (16.5%), all
other species studied here have distinctly higher values.
In Hymenopus this low value might be a result of the
large dorsal fastigium and the cone-like compound eyes
which strongly increase the volume of the head capsule
(WipFlEr et al. 2012). In our study, the highest values
were found in the wood-feeding cockroach Salganea sp.
(29.9%) and the herbivorous phasmatodean Phyllium
siccifolium (28.8%). However, quite similar values were
documented for carnivorous rove beetles (li et al. 2011).
They seem to also have relatively big mandibular adduc-
tor muscles making up about 26% to 33% of the head
capsule’s volume. Even larger muscles were found in ant
workers (paul 2001), where the adductors can occupy up
to 66% of the head capsule volume.
The ratios between the volumes of the adductor and
the abductor muscle varied considerably between differ-
ently adapted species. Higher ratios seem to be reserved
for species specialised in tough food. We observed the
highest ratio in the herbivorous phasmatodeans (23.2 in
Phyllium and 20.4 in Timema) followed by the xylopha-
gous roach Salganea (18.1). Relatively low ratios of 8.4
were found in P. americana (Fig. 3) and 8.7 in the in-
sectivorous mantid. Since lower ratios and accordingly
relatively stronger mandible abductor muscles might fa-
cilitate higher rates when repeated biting is required, or
faster reopening when a predatory strike missed, this fea-
ture is probably particularly useful in species with a diet
comprising a signicant part of elusive animal source
food. In the omnivorous roach Ergaula as well as the xy-
lophagous and herbivours species the adductor is at least
11 times bigger than the abductor. li et al. (2011) found
Fig. 4. Relative volume of the mandibular muscles for selected species of insects. A: relative volume of M. craniomandibularis internus
(0md1) compared to the volume of the head capsule; B: relative volume of M. craniomandibularis externus posterior (0md3) compared to
the volume of the head capsule; C: ratio between M. craniomandibularis internus (0md1) and M. craniomandibularis externus posterior
(0md3).
Table 5. Volume of the head capsule (in mm3), and the bres and tendon of the mandible adductor (M. craniomandibularis internus, 0md1)
and abductor muscles (M. craniomandibularis externus, 0md3) of selected species. The muscle volumes are provided in absolute values
(mm3) and as percentage of the volume of the head capsule.
487
ARTHROPOD SYSTEMATICS & PHYLOGENY — 73
(3) 2015
volume ratios between 6.3 and 12.2 in three species of
predatory rove beetles with distinctly differing mandible
morphologies.
It should be kept in mind that the specimens of P.
americana used in this study were bred for several gen-
erations and fed with uniform diet. However, the same
applies to the cockroach Ergaula sp., the mantid Hy-
menopus coronatus and the phasmatodean Phyllium sic-
cifolium, while the other species were taken from the
wild. The effects of uniform diet and constant inbreed-
ing on the development of the chewing apparatus and
other organs have to be claried by future analysis but
we assume that they are detrimental for normal develop-
ment.
The chewing apparatus of insects is a complex struc-
ture allowing for both, hard biting, shredding tough food
items, and grinding up smaller pieces. In P. americana
like in other dicondylic insects, chewing is largely driven
by the structurally complex mandibular adductor muscle.
In P. americana it consist of eight distinct muscle bre
bundles. These bundles, in turn, consist of muscle bres
with variable lengths and bre angles. Additionally, they
are most likely composed of different bre types (paul
& GronEnBErG 1999, 2002). The small relative muscle
size and intermediate bre angle both reect these cock-
roaches’ omnivorous life style while the mechanical ad-
vantage seems not a good predictor.
5. Acknowledgments
We thank Tobias Siebert (Stuttgart) for interesting discussions of
the specic muscle structure. We thank Hans Pohl (Jena) for creat-
ing the outstanding illustration of the coordinate system (Fig. 1D)
and Aleksandra Birn-Jeffery (Cambridge) for proof-reading the
draft. This work was nancially supported by the German Research
Foundation (DFG) [We 4664/2-1 to TW, WI 4324/1-1 to BW, and
KL 2707/2-1 to TK] and by a PostDoc stipend of the Daimler und
Benz Stiftung (32-10/12 to BW).
6. References
Ahn A.N., Full R.J. 2002. A motor and a brake: two leg extensor
muscles acting at the same joint manage energy differently in
a running insect. – Journal of Experimental Biology 205(Pt 3):
379 – 389.
BEll W.J., roTh L.M., nalEpa C.A. 2007. Cockroaches: ecology
behaviour, and natural history. – The Johns Hopkins University
Press: Baltimore. 230 pp.
BEnnET-Clark H.C. 1975. The energetics of the jump of the lo-
cust Schistocerca gregaria. – Journal of Experimental Biology
63(1): 53 – 83.
BlankE A., WipFlEr B., LETsch h., Koch h., BEckmann F., BEuTEl
r., MisoF B. 2012. Revival of Palaeoptera head characters
support a monophyletic origin of Odonata and Ephemeroptera
(Insecta). – Cladistics 28(6): 560 – 581.
Chapman R.F., dE BoEr G. 1995. Regulatory Mechanisms in Insect
Feeding. – Springer: Heidelberg.
Clissold F.J. 2007. The biomechanics of chewing and plant frac-
ture: mechanisms and implications. – Advances in Insect Phys-
iology 34: 317 – 372.
CroW M.T., KushmErick M.J. 1982. Chemical energetics of slow-
and fast-twitch muscles of the mouse. – The Journal of General
Physiology 79(1): 147 – 166.
FriEdEmann K., WipFlEr B., BradlEr S., BEuTEl R.G. 2012. On the
head morphology of Phyllium and the phylogenetic rela tion-
ships of Phasmatodea (Insecta). – Acta Zoologica 93: 184 – 199.
FriEdrich F., MaTsumura Y., Pohl H., Bai M., HörnschEmEyEr T.,
BEuTEl R.G. 2014. Insect morphology in the age of phyloge-
nomics: innovative techniques and its future role in systemat-
ics. – Entomological Science 17: 1 – 24.
GorB S.N., BEuTEl R.G. 2000. Head-capsule design and mandible
control in beetle larvae: A three-dimensional approach. – Jour-
nal of Morphology 244: 1 – 14.
GoyEns J., Dirckx J., DiErick M., Van HoorEBEkE L., AErTs P. 2014.
Biomechanical determinants of bite force dimorphism in Cy cl-
om matus metallifer stag beetles. – Journal of Experimental Bio -
logy 217(Pt 7): 1065 – 1071.
Grimaldi D., EnGEl M.S. 2005. Evolution of the Insects. – Cam-
bridge University Press: New York.
Hill A.V. 1938. The heat of shortening and the dynamic constants
of muscle. – Proceedings of the Royal Society of London B:
Biological Sciences 126(843): 136 – 195.
Jahromi S., ATWood H. 1969. Correlation of structure, speed of
con traction, and total tension in fast and slow abdominal mus-
cle bers of the lobster (Homarus americanus). – Journal of
Ex perimental Zoology 171(1): 25 – 37.
KEr R.F., AlExandEr R.M., BEnnETT M.B. 1988. Why are mamma-
lian tendons so thick? – Journal of Zoology 216(2): 309 – 324.
Li D., ZhanG K., Zhu P., Wu Z., Zhou H. 2011. 3D conguration
of mandibles and controlling muscles in rove beetles based on
micro-CT technique. – Analytical and Bioanalytical Chemistry
401(3): 817 – 825.
MaiEr L., RooT T.M., SEyFarTh E.A. 1987. Heterogeneity of spider
leg muscle: Histochemistry and electrophysiology of identied
bers in the claw levator. – Journal of Comparative Physio-
logy B: Biochemical, Systemic, and Environmental Physio logy
(Histo rical Archive) 157(3): 285 – 294.
misoF B., liu sh., mEusEmann k., pETErs r.s., donaTh a., mayEr
c., FrandsEn p.B., WarE J., Flouri T., BEuTEl r.G., niEhuis
o., pETErsEn m., izquiErdo-carrasco F., WapplEr T., rusT
J., aBErEr a.J., aspöck u., aspöck h., BarTEl d., BlankE
a., BErGEr s., Böhm a., BucklEy T., calcoTT B., chEn J.,
FriEdrich F., Fukui m., FuJiTa m., GrEvE c., GroBE G., Gu
sh., huanG y., JErmiin l.s., kaWahara a.y., kroGmann l.,
kuBiak m., lanFEar r., lETsch h., li y., li zh., li J., lu h.,
machida r., mashimo y., kapli p., mckEnna d.d., mEnG G.,
nakaGaki y., navarrETE-hErEdia J.l., oTT m., ou y., pass
G., podsiadloWski l., pohl h., rEumonT B.m. v., schüTTE
k., sEkiya k., shimizu sh., slipinski a., sTamaTakis a., sonG
W., su x., szucsich n.u., Tan m., Tan x., TanG m., TanG J.,
TimElThalEr G., Tomizuka sh., TrauTWEin m., TonG x., uchi-
FunE T., Walzl m.G., WiEGmann B.m., WilBrandT J., WipFlEr
W et al.: Cockroach chewing apparatus
488
B., WonG T.k.F., Wu q., Wu G., xiE y., yanG sh., yanG q.,
yEaTEs d.k., yoshizaWa k., zhanG q., zhanG r., zhanG W.,
zhanG y., zhao J., zhou ch., zhou l., ziEsmann T., zou sh.,
li y., xu x., zhanG y., yanG h., WanG J., WanG J., kJEr k.m.,
zhou x. 2014. Phylogenomics resolves the timing and pattern
of insect evolution. – Science 346: 763 – 767.
Paul J. 2001. Mandible movements in ants. – Comparative Bioche-
mistry and Physiology Part A: Molecular & Integrative Physio-
logy 131(1): 7 – 20.
Paul J., GronEnBErG W. 1999. Optimizing force and velocity: man-
dible muscle bre attachments in ants. – Journal of Experimen-
tal Biology 202(7): 797 – 808.
Paul J., GronEnBErG W. 2002. Motor control of the mandible closer
muscle in ants. – Journal of Insect Physiology 48(2): 255 267.
SchmiTT C., Rack A., BETz O. 2014. Analyses of the mouthpart ki-
ne matics in Periplaneta americana (Blattodea, Blattidae) using
synchrotron-based X-ray cineradiography. – Journal of Ex pe-
rimental Biology 217(17): 3095 – 3107.
SEiFErT G. 1995. Entomologisches Praktikum. – Georg Thieme Ver-
lag: Stuttgart, New York.
SiEBErT T., WEihmann T., RodE C., Blickhan R. 2010. Cupiennius
salei: biomechanical properties of the tibia-metatarsus joint
and its exing muscles. Journal of Comparative Physiolgy
B 180(2): 199 – 209.
SnodGrass R.E. 1944. The feeding apparatus of biting and sucking
insects affecting man and animals. – Smithsonian Institution.
Taylor G.M. 2000. Maximum force production: why are crabs so
strong? – Proceedings of Biological Science 267(1451): 1475
1480.
van dEr mEiJdEn A., CoElho P.L., Sousa P., HErrEl A. 2013. Choose
your weapon: defensive behavior is associated with morpho-
logy and performance in scorpions. – PloS one 8(11): e78955.
van dEr mEiJdEn A., LanGEr F., BoisTEl R., VaGovic P., HEEThoFF
M. 2012. Functional morphology and bite performance of rap-
torial chelicerae of camel spiders (Solifugae). – Journal of Ex-
perimental Biology 215(Pt 19): 3411 3418.
WEihmann T., REinhardT L., WEissinG K., SiEBErT T., WipFlEr B.
2015. Fast and powerful: Biomechanics and bite forces of the
mandibles in the American cockroach Periplaneta america-
na. – PlosOne.10(11): e0141226.
WEihmann T., GoETzkE h.h., GünThEr M. in press. Requirements
and limits of anatomy-based predictions of locomotion in ter-
restrial arthropods with emphasis on arachnids. – Journal of
Paleontology.
WEissinG K., Klass K.-D., WEihmann T., WipFlEr B. in press. The
cephalic morphology of the American roach Periplaneta amer-
icana (Blattodea). – Arthropod Systematics & Phylogeny.
WEndT I.R., GiBBs C.L. 1974. Energy production of mammalian
fast- and slow-twitch muscles during development. – American
Journal of Physiology 226: 642 – 647.
WhEaTEr C.P., Evans M.E.G. 1989. The mandibular forces and pres-
sures of some predacious Coleoptera. – Journal of Insect Phy-
sio logy 35(11): 815 – 820.
WipFlEr B., machida R., müllEr B., BEuTEl r.G. 2011. On the
head morphology of Grylloblattodea (Insecta) and the system-
atic position of the order, with a new nomenclature for the head
muscles of Dicondylia. – Systematic Entomology 36: 241
266.
WipFlEr B., WiEland F., DEcarlo F., HörnschEmEyEr T. 2012. Ce-
phalic morphology of Hymenopus coronatus (Insecta: Manto-
dea) and its phylogenetic implications. – Arthropod Structure
& Development 41(1): 87 – 100.
WipFlEr B., KluG r., GE s.-q., Bai m., GöBBEls J., YanG x.-k.,
HörnschEmEyEr T. 2015. The thorax of Mantophasmatodea,
the morphology of ightlessness, and the evolution of the neo-
pteran insects. – Cladistics 31: 50 – 70.
... Additionally several studies compared the morphology of the head capsule or specific mouthparts for several cockroach species (Buder & Klass, 2013;Klass & Eulitz, 2007;Mangan, 1908;Zhuzhikov, 2007). The mechanical and functional aspects of the mouthparts of Periplaneta americana were addressed by Popham (1961), Roberts (1972), Schmitt, Rack & Betz (2014) and Weihmann et al. (2015aWeihmann et al. ( , 2015b. ...
... craniomandibularis internus). Details concerning these factors and their specific measurements are provided in Weihmann et al. (2015a). For comparison, we also measured the effective cross section area and volume of the mandibular adductor for the cockroaches Blattella germanica, Periplaneta americana, and Salganea rossi. ...
... However, the most proximal ones show distinct differences (0.45 to 0.52), which is correlated to the fact that the left one is distinctly more proximal than the right. Similar values (ranging between 0.37 and 0.47) have been measured for Periplaneta americana (Weihmann et al., 2015a) but also for carnivorous beetles (0.35-0.59); (Wheater & Evans, 1989). Seemingly, there is no direct correlation between diet and mechanical advantage (Weihmann et al., 2015a). ...
Article
Full-text available
Background Cockroaches are usually typical omnivorous detritivores and their cephalic morphology is considered to be ancestral in various aspects. Thus, several studies addressed the morphology and function of the blattodean head, and the cockroach usually serves as a model for standard mouthparts in text books. However, so far only two of the three major lineages of Blattodea have been studied and no detailed information for the head of any Corydioidea was available. The present study closes this gap by providing a detailed morphological description of the head of Ergaula capucina , studying some important functional parameters of the mandible and discussing it in a phylogenetic framework. Methods The cephalic morphology of Ergaula studied in detail using a broad set of different techniques including digital microscopy, µ-computed tomography, and 3-dimensional reconstructions. Concerning the functional morphology of the mandible, we compared the volume and effective cross sections of the eight compartments of the primary mandibular adductor muscle for Ergaula , Blattella germanica , and Salganea rossi and measured the mechanical advantage, i.e. , the force transmission ratio for all teeth of the mandible of Ergaula . Results The head capsule of Ergaula is characterized by a strong sexual dimorphism and typical orthopteran mouthparts. It resembles the head capsule of other roaches in several respects and confirms oesotendons, the reduction of the mesal occelus, and bipartite M. verticopharyngealis and M. hypopharyngosalivaris as blattodean apomorphies. But it also shows some unique adaptations. It is the first described cockroach that lacks the dorsal tentorial arms which has various consequences for the cephalic musculature. On the maxillary lacinia, Ergaula is the first described blattodean to show strong and blunt setae instead of a lacinula, which might be homologues to the dentisetae of dragonflies and mayflies. Like other corydiid roaches that inhabit xeric areas, Ergaula has an atmospheric water-vapor absorption mechanism that includes a gland and a ductus on the epipharnyx and bladders on the hypopharynx. The mandibular adductor is in cockroaches asymmetric, a pattern not found in termites, mantids, or other closely related insects.
... In all insects with chewing mouthparts, bite forces are generated by large muscles located in the head capsule, and transmitted to the cutting edge of the mandible via an apodeme and a mandibular joint [26][27][28]. Because this musculoskeletal bite system is both of behavioural, ecological and evolutionary relevance and can be analysed with first principles, it has received increasing attention from biomechanists [29][30][31][32][33], evolutionary biologists [34][35][36][37][38][39], functional morphologists [32,[40][41][42][43][44][45][46][47][48] and (behavioural) ecologists alike [28,[49][50][51][52][53][54][55][56]. Concretely, for an isometric contraction at zero fibre stretch, the force exerted at any point of the mandible, F b , may be written as the product between the ratio of muscle volume V m and the average fibre length L f (the physiological cross-sectional area of the muscle, A phys = V m /L f ), the muscle stress σ m , the cosine of the pennation angle ϕ, and the mechanical advantage MA [28,40,49,51]: ...
... In all insects with chewing mouthparts, bite forces are generated by large muscles located in the head capsule, and transmitted to the cutting edge of the mandible via an apodeme and a mandibular joint [26][27][28]. Because this musculoskeletal bite system is both of behavioural, ecological and evolutionary relevance and can be analysed with first principles, it has received increasing attention from biomechanists [29][30][31][32][33], evolutionary biologists [34][35][36][37][38][39], functional morphologists [32,[40][41][42][43][44][45][46][47][48] and (behavioural) ecologists alike [28,[49][50][51][52][53][54][55][56]. Concretely, for an isometric contraction at zero fibre stretch, the force exerted at any point of the mandible, F b , may be written as the product between the ratio of muscle volume V m and the average fibre length L f (the physiological cross-sectional area of the muscle, A phys = V m /L f ), the muscle stress σ m , the cosine of the pennation angle ϕ, and the mechanical advantage MA [28,40,49,51]: ...
... Implicit in this definition is the assumption that muscle contraction moves the apodeme along its main axis. This assumption is supported by the fact that the main axis approximately coincides with the resulting muscle force vector, which has been used as an alternative reference axis for the calculation of pennation angles in previous studies [29,32]. Pennation angles, averaged for each muscle tissue, were about two degrees smaller using this definition, but this difference was independent of worker size [Analysis of covariance (ANCOVA): F 1,56 = 0.10, P = 0.75], within the accuracy of the angle estimation (see below), and thus does not affect conclusions on the scaling of the average pennation angle. ...
Preprint
Full-text available
The extraordinary success of social insects is partially based on "division of labour", i. e. individuals exclusively or preferentially perform specific tasks. Task-preference may correlate with morphological adaptations so implying task-specialisation, but the extent of such specialisation can be difficult to determine. Here, we demonstrate how the physical foundation of some tasks can be leveraged to quantitatively link morphology and performance. We study the allometry of bite force capacity in Atta vollenweideri leaf-cutter ants, polymorphic insects in which the mechanical processing of plant material is a key aspect of the behavioural portfolio. Through a morphometric analysis of tomographic scans, we show that the bite force capacity of the heaviest colony workers is twice as large as predicted by isometry. This disproportionate "boost" is predominantly achieved through increased investment in muscle volume; geometrical parameters such as mechanical advantage, fibre length or pennation angle are likely constrained by the need to maintain a constant mandibular opening range. We analyse this preference for an increase in size-specific muscle volume and the adaptations in internal and external head anatomy required to accommodate it with simple geometric and physical models, so providing a quantitative understanding of the functional anatomy of the musculoskeletal bite apparatus in insects.
... In all insects with chewing mouthparts, bite forces are generated by large muscles located in the head capsule, and transmitted to the cutting edge of the mandible via an apodeme and a mandibular joint [20,21]. Because this musculoskeletal bite system is of behavioural, ecological and evolutionary relevance and can be analysed with first principles, it has received increasing attention from biomechanists [22][23][24][25], evolutionary biologists [26][27][28][29][30], functional morphologists [24,[31][32][33][34][35][36][37][38] and (behavioural) ecologists alike [21,[39][40][41][42][43][44]. Concretely, for an isometric contraction at zero fibre stretch, the force exerted at any point of the mandible, F b , may be written as the product between the ratio of muscle volume V m and the average fibre length L f (the physiological cross-sectional area of the muscle, A phys = V m /L f ), the muscle stress σ m , the cosine of the average pennation angle w, and the mechanical advantage MA [21,31,39,41]: ...
... In all insects with chewing mouthparts, bite forces are generated by large muscles located in the head capsule, and transmitted to the cutting edge of the mandible via an apodeme and a mandibular joint [20,21]. Because this musculoskeletal bite system is of behavioural, ecological and evolutionary relevance and can be analysed with first principles, it has received increasing attention from biomechanists [22][23][24][25], evolutionary biologists [26][27][28][29][30], functional morphologists [24,[31][32][33][34][35][36][37][38] and (behavioural) ecologists alike [21,[39][40][41][42][43][44]. Concretely, for an isometric contraction at zero fibre stretch, the force exerted at any point of the mandible, F b , may be written as the product between the ratio of muscle volume V m and the average fibre length L f (the physiological cross-sectional area of the muscle, A phys = V m /L f ), the muscle stress σ m , the cosine of the average pennation angle w, and the mechanical advantage MA [21,31,39,41]: ...
Article
The extraordinary success of social insects is partially based on division of labour, i.e. individuals exclusively or preferentially perform specific tasks. Task preference may correlate with morphological adaptations so implying task specialization, but the extent of such specialization can be difficult to determine. Here, we demonstrate how the physical foundation of some tasks can be leveraged to quantitatively link morphology and performance. We study the allometry of bite force capacity in Atta vollenweideri leaf-cutter ants, polymorphic insects in which the mechanical processing of plant material is a key aspect of the behavioural portfolio. Through a morphometric analysis of tomographic scans, we show that the bite force capacity of the heaviest colony workers is twice as large as predicted by isometry. This disproportionate 'boost' is predominantly achieved through increased investment in muscle volume; geometrical parameters such as mechanical advantage, fibre length or pennation angle are likely constrained by the need to maintain a constant mandibular opening range. We analyse this preference for an increase in size-specific muscle volume and the adaptations in internal and external head anatomy required to accommodate it with simple geometric and physical models, so providing a quantitative understanding of the functional anatomy of the musculoskeletal bite apparatus in insects.
... But even though insects provide an overwhelming morphological diversity, they are notoriously underexplored with respect to maximum bite forces and their dependency on mandible opening. Except for functional inferences from morphological data (65) and one earlier experimental work on ground beetles (66), all other functional knowledge has been gained only recently (8)(9)(10)(67)(68)(69). ...
... However, in the opening range where passive forces become significant, the mandible adductors are far on the descending limb of the force-length relation with only a small potential for force generation. Moreover, the effective in-lever is by about 30% shorter than in closed mandibles reducing the effective mechanical advantage of the mandible (8). Thus, here, the passive forces antagonize the abductors, which can open the mandibles up to 100° and are most likely the stronger of the two antagonistic muscles at large gape angles ...
Thesis
Full-text available
Although, major aspects of organismal movements can only be explained by biomechanical arguing, in biology the discipline is still often regarded as a somehow exotic, peripheral research area. Nevertheless, for scientific fields like behavioural biology, ecology, evolution history, but also for zoology in general it is of particular importance. Built on basic physical and biochemical laws it is inherently interdisciplinary. Given its integrative potential, biomechanics could provide a crucial connecting point for many, so far often incompatible research fields. Biomechanical analyses also offer important starting points for biomimetic approaches and biologically inspired robotics. Arthropods are the most diverse taxonomic group on earth and make up major proportions of animal biomass in both aquatic and terrestrial habitats. Accordingly, they are hardly overestimated key agents in a wide range of ecological contexts. Their immense diversity yielded a wealth of different body plans and hugely varying movable appendages. Movement systems are directly related to the fitness of an organism, and their mechanistic understanding therefore provides intellectual access to behavioural, ecological and phylogenetical contexts. Major mechanisms in these contexts are muscle contraction, transmission of forces to substrates, joint design and functioning, material properties (strength, stiffness, damping), physical contact with substrates (attachment) and scaling laws affecting a wide range of force and metabolic limits. The present work deals with all these mechanisms and classifies them in terms of ecology, behaviour and phylogeny of different species and body plans.
... However, the weight of an animal scales with its volume, i.e. to the third power of the length measure (Schmidt-Nielsen, 1975;Biewener, 2005). Accordingly, it is much simpler for small animals to adapt their morphology to high force requirements (Scholz et al., 2006), as is often seen in insects (Dirks and Federle, 2011;Weihmann et al., 2015b), other terrestrial arthropods (e.g. Evans and Forsythe, 1984;Manton, 1954;Robinson and Valerio, 1977;van der Meijden et al., 2012;Nyffeler et al., 2017) and those of the soil mesofauna (Heethoff and Koerner, 2007). ...
Article
Arthropods are the most diverse clade on earth with regard to both species number and variability of body plans. Their general body plan is characterised by variable numbers of legs, and many-legged locomotion is an essential aspect of many aquatic and terrestrial arthropod species. Moreover, arthro-pods belong to the first groups of animals to colonise subaerial habitats, and they did so repeatedly and independently in a couple of clades. Those arthropod clades that colonised land habitats were equipped with highly variable body plans and locomotor apparatuses. Proceeding from their respective specific anatomies, they were challenged with strongly changing environmental conditions as well as altered physical and physiological constraints. This review explores the transitions from aquatic to terrestrial habitats across the different arthropod body plans and explains the major mechanisms and principles that constrain design and function of a range of locomotor apparatuses. Important aspects of movement physiology addressed here include the effects of different numbers of legs, different body sizes, minia-turisation and simplification of body plans and different ratios of inertial and damping forces. The ar-ticle's focus is on continuous legged locomotion, but related ecological and behavioural aspects are also taken into account.
... Due to the small size of most insect species (Chown and Gaston 2010), even simple biomechanical assessments such as bite force measurements involve complex experimental setups which are currently limited by the size of the force-sensing element which can be introduced between the mandibles. Weihmann et al. (2015a) used a bespoke strain gauge-based 2D force transducer with a tip element of 0.8 mm diameter; David et al. (2016a) used a piezoelectric 1D force sensor with 0.63 mm diameter. Therefore, insects with a gape no less than approximately 5 mm should be measured with currently available setups in order to ensure that the adductor muscles operate near their maximum force outputs ( Blümel et al. 2012b, c). ...
Chapter
Full-text available
Insects show a plethora of different mandible shapes. It was advocated that these mandible shapes are mainly a function of different feeding habits. This hypothesis was tested on a larger sampling of non-holometabolan biting–chewing insects with additional tests to understand the interplay of mandible function, feeding guild, and phylogeny. The results show that at the studied systematic level, variation in mandible biting–chewing effectivity is regulated to a large extent by phylogenetic history and the configuration of the mandible joints rather than the food preference of a given taxon. Additionally, lineages with multiple mandibular joints such as primary wingless hexapods show a wider functional space occupation of mandibular effectivity than dicondylic insects (= silverfish + winged insects) at significantly different evolutionary rates. The evolution and occupation of a comparably narrow functional performance space of dicondylic insects is surprising given the low effectivity values of this food uptake solution. Possible reasons for this relative evolutionary “stasis” are discussed.
... The spines at the distal ends of the mandibles (Figure 4) may pierce and rasp into the soft tergite (the anterior tergites of mysids are less sclerotised than the following tergites) and then into the heart of the host. A similar function of the mandibles has been proposed for several parasitic insects (Ma, Huang, & Hua, 2013;Mehlhorn, 2016;Rasnitsyn, Poinar, & Brown, 2017;Weihmann, Kleinteich, Gorb, & Wipfler, 2015). Due to the visible insertion hole in the first tergite of the host (Figure 3b), penetration by the mandibles of the dajiid is likely. ...
Article
Parasitic isopods have become specialised to many different host species and therefore show a wide variety of attachment and feeding specialisations. Often such structures are difficult to examine due to their small sizes which makes a more complete understanding of their functional morphology difficult. Here we present a new report and a first time high‐resolution, non‐SEM documentation of a parasitic epicaridean isopod, a female of the dajiid Arthrophryxus sp. from the Sea of Okhotsk. It was found during the SokhoBio 2015 on its host, a mysid shrimp (Holmsiella sp.). Arthrophryxus has only one formally described species, Arthrophryxus beringanus Richardson, 1908. With high‐resolution documentation methods, we reveal new details of the morphological structures of mouthparts and thoracopods of this dajiid. Furthermore, we discuss the functional morphology of attachment to the host and feeding according to our new findings. We suggest that the thoracopods are involved in the attachment process even more than formerly assumed for different dajiids. The piercing‐sucking mouthparts and the additional attachment mechanisms strongly indicate a permanent parasitism of the dajiid isopod. Permanent parasites affect the fitness of their hosts; therefore, deep‐sea forms of dajiid isopods have direct impact on the deep‐sea crustacean communities.
Article
We report fluid feeding with a sucking pump in the arthropod class Diplopoda, using a combination of synchrotron tomography, histology, electron microscopy, and three-dimensional reconstructions. Within the head of nine species of the enigmatic Colobognatha, we found a pumping chamber, which acts as positive displacement pump and is notably similar to that of insects, showing even fine structural convergences. The sucking pump of these millipedes works together with protractible mouthparts and externally secreted saliva for the acquisition of liquid food. Fluid feeding is one of the great evolutionary innovations of terrestrial arthropods, and our study suggests that it evolved with similar biomechanical solutions convergent across all major arthropod taxa. While fluid-feeding insects are megadiverse today, it remains unclear why other lineages, such as Colobognatha, are comparably species poor.
Chapter
The morphology, musculature, and function of the feeding apparatus of cockroaches is described in detail and compared with other insects with biting and chewing mouthparts. The mouthparts of cockroaches represent, in most cases, the ancestral condition for winged and neopteran insects. Their head capsule is flattened in a posterior-anterior direction and very similar among the studied species. The right mandible is very constant in shape, while the number of distal incisivi in left mandibles varies among species. With the exception of Tivia sp. (Corydiidae), primary mandibular adductor of the mandible has eight distinct compartments in all studied roaches, for which functional cross section and volume are provided. In all these specimens, the left adductor is smaller than the right one. Bite forces and muscle properties are discussed for Periplaneta americana. The maxilla, labium, and hypopharynx are also highly similar among cockroaches and close to the pterygotan ground plan. The same also applies to the associated musculature for which we also provide functional and kinematic considerations. Cockroaches salivate food outside the mouth cavity before cutting it with the mandibles. The maxillae transport food into the cibarium where the hypopharynx is involved in transporting it between the grinding mandibular molae. The crushed food is sucked into the pharynx via dilation. During the feeding process, most mouthparts exhibit highly concerted activities. This process generally follows the ground pattern for insects with biting and chewing mouthparts, although some salivation processes may differ.
Chapter
Insect mouthparts are modified appendages of head segments that are adapted to exploit different food sources. This chapter describes the general mouthpart morphology of Hexapoda, introduces basic feeding types in insects, and illustrates mouthpart function. Insect mouthparts include three appendages, the paired mandibles, the paired maxillae, and the unpaired labium as well as additional head structures, the labrum, and the hypopharynx. The noninsect lineages of Hexapoda possess entognathous mouthparts, which are concealed inside the head, while ectognathous mouthparts of Insecta articulate externally on the head capsule. Especially in winged insects, characteristic adaptations of mouthparts evolved in context with various food sources resulting in feeding specialization and enhanced functional performance. Insect mouthparts can be categorized in three principal functional types: (1) mandibulate biting and chewing mouthparts, (2) haustellate mouthparts forming variously composed proboscises, and (3) filter-feeding mouthparts of aquatic immature stages. The diversity of functional types and remarkable modifications are presented in various examples; characteristic patterns of mouthpart evolution are discussed. The composition of mouthparts in the various hexapod orders is summarized in a table. Additional functions, like defense, brood care, and male-male competition, modified the mouthparts in some insects. Rudimentary mouthparts are found in some nonfeeding adults of various insect taxa.
Article
Full-text available
The skeleto-muscular system of the head of the American cockroach Periplaneta americana is described in detail. The results are compared with previous partial descriptions of the cephalic morphology of this species and other dictyopterans. The head of Periplaneta is, as in other cockroaches, mostly characterized by plesiomorphies such as the typical orthopteroid mouthparts, the lateral position of the compound eyes, 5-segmented maxillary palps and 3-segmented labial palps, as well as long antennae. Periplaneta shows sexual dimorphism with the compound eyes of the males reaching further ventrally. The epistomal ridge is medially interrupted so that the frons and the clypeus are confluent. The cephalic musculature is typical for a polyneopteran insect and includes 59 muscles. Potential apomorphies for Blat-todea in the cephalic area include the absence of the median ocellus, the bipartite condition of M. verticopharyngealis (0ph1) and of M. hypopharyngosalivaris (0hy12), and the presence of oesotendons. The lacinula, a subapical lobelet on the lacinia, is present in almost all studied blattodeans but its potential homology to the dentisetae of Palaeoptera or the lamellae of apterygotes cannot be addressed at the moment. A " perforate " tentorium, a membranous postmola, and a lacinia that fits into the concave mesal wall of the galea are confirmed as autapomorphies of Dictyoptera.
Article
Full-text available
Knowing the functionality and capabilities of masticatory apparatuses is essential for the ecological classification of jawed organisms. Nevertheless insects, especially with their outstanding high species number providing an overwhelming morphological diversity, are notoriously underexplored with respect to maximum bite forces and their dependency on the mandible opening angles. Aiming for a general understanding of insect biting, we examined the generalist feeding cockroach Periplaneta americana, characterized by its primitive chewing mouth parts. We measured active isometric bite forces and passive forces caused by joint resistance over the entire mandibular range with a custom-built 2D force transducer. The opening angle of the mandibles was quantified by using a video system. With respect to the effective mechanical advantage of the mandibles and the cross-section areas, we calculated the forces exerted by the mandible closer muscles and the corresponding muscle stress values. Comparisons with the scarce data available revealed close similarities of the cockroaches’ mandible closer stress values (58 N/cm2) to that of smaller specialist carnivorous ground beetles, but strikingly higher values than in larger stag beetles. In contrast to available datasets our results imply the activity of faster and slower muscle fibres, with the latter becoming active only when the animals chew on tough material which requires repetitive, hard biting. Under such circumstances the coactivity of fast and slow fibres provides a force boost which is not available during short-term activities, since long latencies prevent a specific effective employment of the slow fibres in this case.
Article
Full-text available
Insects are the most speciose group of animals, but the phylogenetic relationships of many major lineages remain unresolved. We inferred the phylogeny of insects from 1478 protein-coding genes. Phylogenomic analyses of nucleotide and amino acid sequences, with site-specific nucleotide or domain-specific amino acid substitution models, produced statistically robust and congruent results resolving previously controversial phylogenetic relations hips. We dated the origin of insects to the Early Ordovician [~479 million years ago (Ma)], of insect flight to the Early Devonian (~406 Ma), of major extant lineages to the Mississippian (~345 Ma), and the major diversification of holometabolous insects to the Early Cretaceous. Our phylogenomic study provides a comprehensive reliable scaffold for future comparative analyses of evolutionary innovations among insects.
Article
Full-text available
The kinematics of the biting and chewing mouthparts of insects is a complex interaction of various components forming multiple jointed chains. The novel technique of in vivo cineradiography by means of Synchrotron radiation was used to elucidate the motion cycles in the cockroach Periplaneta americana. Digital X-ray footage sequences were used in order to calculate pre-defined angles and distances, each representing characteristic aspects of the movement pattern. We were able to analyze the interactions of the mouthpart components and to generate a functional model of maxillary movement by integrating kinematic results, morphological dissections, and fluorescence microscopy. During the opening and closing cycles that take 450-500 ms on average, we found strong correlations between the measured maxillary and mandibular angles, indicating a strong neural coordination of these movements, as manifested by strong antiphasic courses of the maxillae and the mandibles and antiphasic patterns of the rotation of the cardo about its basic articulation at the head and by the deflection between the cardo and stipes. In our functional model of the maxilla, its movement pattern is explained by the antagonistic activity of five adductor / promotor muscles and one adductor / remotor muscle. However, beyond the observed intersegmental and bilateral stereotypy, certain amounts of variation across subsequent cycles within a sequence were observed with respect to the degree of correlation between the various mouthparts and the maximum, minimum, and time course of the angular movements. Although generally correlated with the movement pattern of the mandibles and the maxillary cardo-stipes complex, such plastic behavior was especially observed in the maxillary palpi and the labium.
Article
Full-text available
In the stag beetle family (Lucanidae), males have diverged from females by sexual selection. The males fight each other for mating opportunities with their enlarged mandibles. It is known that owners of larger fighting apparatuses are favoured to win the male-male fights, but it was unclear whether male stag beetles also need to produce high bite forces while grabbing and lifting opponents in fights. We show that male Cyclommatus metallifer stag beetles bite three times as forcefully as females. This is not entirely unexpected given the spectacular nature of the fights, but all the more impressive given the difficulty of achieving this with their long mandibles (long levers). Our results suggest no increase in male intrinsic muscle strength to accomplish this. However, morphological analyses show that the long mandibular output levers in males are compensated by elongated input levers (and thus a wider anterior side of the head). The surplus of male bite force capability is realized by enlargement of the closer muscles of the mandibles, while overall muscle force direction remained optimal. To enable the forceful bites required to ensure male reproductive success, male head size and shape are adapted for long input levers and large muscles. Therefore, the entire head should be regarded as an integral part of male armature.
Book
The only book to deal comprehensively with insect feeding was published by C. T. Brues in 1946. His Insect Dietary was an account of insect feeding habits. Since that time there has been a revolution in biology, and almost all aspects of our understanding of insect feeding have expanded to an extent and into areas that would have been unthinkable in Brues' day. Yet, our book does not replace Insect Dietary but, instead, complements it, because our aim is to bring together information on the mechanisms by which food quality and quantity are regulated. We deliberately focus attention on the feeding process; to include food-finding would have required a much larger book and would have moved the focus away from more proximate mechanisms. This book is dedicated to the late Vincent G. Dethier. As a pioneer in studying the physiological basis of animal behavior, he focused on regulation of feeding in flies and caterpillars. His work on the blowfly, together with that by his many students and co-workers, still provides the most completely described mechanism of insect feeding. The citation of his work in almost every chapter in this book illustrates the importance of his findings and ideas to our current understanding of regulation of insect feeding. The authors in this book provide many innovative and stimulating ideas typifying Dethier's approach to the study of feeding be­ havior.
Article
Modern computer-aided techniques foster the availability and quality of 3D visualization and reconstruction of extinct and extant species. Moreover, animated sequences of locomotion and other movements find their way into motion pictures and documentary films, but also gain attraction in science. While movement analysis is well advanced in vertebrates, particularly in mammals and birds, analyses in arthropods, with their much higher variability regarding general anatomy and size, are still in their infancies and restricted to a few laboratory species. These restrictions and deficient understanding of terrestrial arthropod locomotion in general impedes sensible reconstruction of movements in those species that are not directly observable (e.g., extinct and cryptic species). Since shortcomings like over-simplified approaches to simulate arthropod locomotion became obvious recently, in this review we provide insight into physical, morphological, physiological, behavioral, and ecological constraints, which are essential for sensible reconstructions of terrestrial arthropod locomotion. Such concerted consideration along with sensible evaluations of stability and efficiency requirements can pave the way to realistic assessment of leg coordination and body dynamics.
Book
The cockroach is truly an evolutionary wonder. This definitive volume provides a complete overview of suborder Blattaria, highlighting the diversity of these amazing insects in their natural environments. Beginning with a foreword by E. O. Wilson, the book explores the fascinating natural history and behavior of cockroaches, describing their various colors, sizes, and shapes, as well as how they move on land, in water, and through the air. In addition to habitat use, diet, reproduction, and behavior, Cockroaches covers aspects of cockroach biology, such as the relationship between cockroaches and microbes, termites as social cockroaches, and the ecological impact of the suborder. With over 100 illustrations, an expanded glossary, and an invaluable set of references, this work is destined to become the classic book on the Blattaria. Students and research entomologists can mine each chapter for new ideas, new perspectives, and new directions for future study. © 2007 by The Johns Hopkins University Press. All rights reserved.