JOURNAL OF MORPHOLOGY 238:157–178 (1998)
An Exaggerated Trait in Insects: The Prothoracic Skeleton
of Stictocephala bisonia (Homoptera: Membracidae)
ULRICH E. STEGMANN*
Institut für Ökologie und Evolutionsbiologie, Universität Bremen,
Bremen, Germany
ABSTRACT The prothoracic skeleton of Stictocephala bisonia was investigated in adults and fifth-instar nymphs on a gross morphological (SEM,
maceration) and light microscopic level. In both nymphs and adults, the
prothoracic skeleton consists of the pronotum, episternum, epimeron, precoxale, sternum, trochantin, and two endoskeletal characters (furcal arms and
pleural apophyses). In nymphs, the entire pronotum is a single-layered
outgrowth of the integument communicating with the body cavity and filled
with hemolymph and fat body cells (‘‘spine’’); the dorsal and ventral processes
and the suprahumeral bud are extensions of this single-layered integument.
In adults, the pronotum is composed of (1) a proximal, single-layered part, and
(2) a larger, distal, double-layered part (‘‘posterior reduplication’’) with two
cuticular layers separated by a thin lumen. The posterior reduplication is
elevated above the body and forms hollow (air-filled) extensions (e.g., suprahumeral horns). Its two cuticular layers are connected through cuticular
columns that appear on the external surface as pits. The lumen between these
layers communicates with the body cavity and contains nerves and tracheae.
In the lumen of newly eclosed adults, intercellular space, epidermal cells with
long processes, and hemocytes with nonlipid granules are present. In the
lumen of sclerotized adult pronota, the intercellular space has disappeared,
together with definite cell boundaries. Several structures are associated with
the external cuticle: two types of innervated sensilla trichodea that articulate
in the center of external pits, sensilla campaniformia, sensilla coeloconica,
and cuticular canals with exterior openings. The morphogenetic implications
of pronotal construction, various aspects of adult prothoracic anatomy, and
the value of glands and sensilla for an adaptive interpretation of the pronotum are discussed. J. Morphol. 238:157–178, 1998. r 1998 Wiley-Liss, Inc.
KEY WORDS: Stictocephala bisonia; prothorax; pronotum; lobe; double-layer; morphogenesis; function
In many treehoppers (Membracidae), the
dorsal sclerite of the prothorax is extraordinarily enlarged, assuming an array of bizarre shapes across the family—a fact that
has attracted an equally diverse community
of adaptive and nonadaptive hypotheses over
the decades and still awaits satisfactory evolutionary explanations (e.g., Wood, ’93). In
dealing with the Membracidae, the taxonomists of the eighteenth and nineteenth centuries (e.g., Linnaeus, 1758; De Geer, 1773;
Stoll, 1788; Latreille, 1802; Fabricius, 1803;
Germar, 1835; Burmeister, 1839; Amyot and
Serville, 1843; Fairmaire, 1846; Stål, 1859,
1866; Fowler, 1894) based their work largely
on the external appearance of this sclerite
r 1998 WILEY-LISS, INC.
(the pronotum). These investigators introduced terms describing its commonly found
external characters: the lateral horn (‘‘cornus’’: Linnaeus, 1758), humeral angle
(‘‘angles humeraux’’: Amyot and Serville,
1843), posterior process (‘‘cornu postico’’: Stål,
1859), and the frontal and dorsal parts of the
sclerite (‘‘metopidium’’ and ‘‘dorsum,’’ respectively; Fowler, 1894).
The first achievement toward an understanding of pronotal anatomy of the Membra-
Contract grant sponsor: Studienstiftung des deutschen Volkes.
*Correspondence to: Ulrich Stegmann, Biozentrum,
Zoologie III, Am Hubland, 97074 Würzburg, Germany.
E-mail: [email protected]
158
U.E. STEGMANN
cidae was to recognize this sclerite in adults
as the pronotum in the proper anatomical
sense. Linnaeus (1758) attributed the sclerite to the dorsal part of the thorax, and De
Geer (1773) correctly specified that it belonged to the prothorax or ‘‘corselet.’’ De
Geer’s interpretation was challenged by Germar (1835), who thought the exaggerated
sclerite was a unified dorsal thoracic plate.
When Burmeister (1839) refuted Germar’s
view, he was the first to explicitly acknowledge this sclerite as the notum of the prothorax (‘‘Vorderrücken’’).
Buckton (’03) observed that the external
pronotal processes are not integumental outgrowths communicating with the body cavity, but rather are parts of one enlarged,
cuticular plate (‘‘shell’’: Buckton, ’03) extending over the body and so arched as to form
these pronotal processes as hollow extensions (‘‘hollow chambers,’’ ‘‘air-chambers’’;
Buckton, ’03). He illustrated his findings,
establishing the ‘‘septum’’ as an internal
character of the pronotum and, for the first
time, defined pronotal features that had been
used by taxonomists for more than a century. Referring to external processes, he
made the important observation that ‘‘there
are no corresponding sutures to mark them
anatomically’’ (Buckton, ’03). Consequently,
Buckton must have realized that even his
definitions were anatomically ambiguous.
This conclusion may also be the background
to Funkhouser’s (’17) remark that the pronotal processes ‘‘have no anatomical significance [sensu anatomical definition, U.E.S.]
and are merely hollow extensions of the chitinized wall.’’ The considerable confusion in
early systematics, which relied largely on
descriptions of external pronotal morphology (e.g., Wood and Pesek, ’92), is likely to
have originated from this lack of sutures.
After Buckton’s (’03) pioneering work, the
literature became scattered with few crossreferences, and his own study on pronotal
anatomy was largely forgotten. While the
existence of the pronotal plate was accepted
by later investigators, as can be inferred
from some of their drawings (Marcus, ’50;
Kopp and Yonke, ’72; Strümpel, ’72), its internal composition remained controversial.
Some investigators apparently considered
the pronotal plate to be a massive, cuticular
structure (Kramer, ’50; Kopp and Yonke, ’72;
Strümpel, ’72), while others, working specifically on pronotal histology, discovered living
tissue within (Marcus, ’50; Richter, ’54; Wood,
’75b). With one exception (Rietschel, ’87),
even basic gross morphological aspects ei-
ther were not investigated or remained obscure; e.g., the articulation of the pronotal
plate with the rest of the body. Buckton (’03)
depicted a ‘‘crescentic process for articulating the pronotum’’ on the mesonotum, while
Richter (’53, ’54) assumed muscles to fix an
extended part of the pronotum (‘‘apéndice
pronotal’’) to the rest of the sclerite. Knowledge of the prothoracic anatomy of nymphs
remains restricted to the rough external
shape of the pronotum and its processes
found in various species (e.g., Funkhouser,
’17; Yothers, ’34). Considering the numerous
speculations about the adaptive significance
or insignificance of the exaggerated pronotum, this scarcity of knowledge about pronotal anatomy is surprising.
Here, the prothoracic skeleton of adults
and last-instar nymphs of Stictocephala bisonia, Kopp and Yonke (’77), was investigated
at the gross morphological and histological
level. Emphasis in both nymphs and adults
was on the attachment of the pronotum to
the rest of the body and on the histology and
external morphology of the posterior reduplication in adults. The results are not only
discussed with respect to earlier studies on
S. bisonia, but to any other membracid species in order to review the current knowledge of the prothoracic anatomy in the
Membracidae. Stictocephala bisonia is a univoltine species that is widely distributed and
seasonally abundant in North America (e.g.,
Kopp and Yonke, ’73, ’77) and was introduced to Europe early in the twentieth century (e.g., Poisson, ’37; Hoffrichter and
Tröger, ’73; Günthart, ’80).
MATERIALS AND METHODS
A colony of Stictocephala bisonia was obtained from H. Strübing (’92) and reared on
Vicia faba and Prunus amygdalus (for details, see Stegmann, ’97). The exo- and endoskeleton were investigated using specimens
(six males, eight females, six fifth-instar
nymphs) that were macerated for up to 1 hr
in hot KOH (10%), washed, and dissected
under a Wild stereomicroscope. Figures
1B–E, 2A, 4B–E, and 5A–C are camera lucida drawings of specimens in glycerin. Dissections of muscles, nerves, and tracheae
were performed with four females fixed in
4% formalin and half-embedded in paraffin
wax (modified after Kramer, ’50), and with
two males and one female, using a modified
vital staining procedure (Yack, ’92) with saline (0.1 M phosphate buffer with 5.5% sucrose, pH 7.2) and 0.01% Janus Green B.
159
PROTHORAX OF STICTOCEPHALA
Whole-mounts of the metopidium, dorsum, and septum were prepared from two
males and four females; 0.5–3 mm2 fragments were cut in saline, fixed in 1.75%
glutaraldehyde (in 0.1 M phosphate buffer,
pH 7.2), washed, stained for 12–24 hr in
0.75% Orange G, washed again, and then
stained for 12–24 hr in 0.5% Light Green.
Fragments were then dehydrated in a graded
ethanol series and mounted on microscope
slides in Entellan. Only cellular components
were stained, while the cuticle remained
transparent (Figs. 7C,E, 8D,E,I).
Sections for light microscopy were prepared from four males, four females, and
two third-instar nymphs. After dissection in
saline, relevant material was fixed in a
vacuum-desiccator for 1 hr and then for 24
hr at ⫹6°C (1.75% glutaraldehyde in 0.1 M
phosphate buffer, pH 7.2), and vacuumwashed in saline. Except for nymphs (Fig.
2C–E) and one female (Fig. 8A,N), tissue
was postfixed for 24 hr at ⫹6°C (2% osmium
tetroxide and 5.75% sucrose in 0.1 M phosphate buffer) and washed. Following dehydration in a graded series of ethanol, most
material was imbedded in Technovit 7100
VLC, and stained with Toluidine Blue
O/Methylene Blue (Fig. 2C–E; 10 µm),
Methylene Blue/Azure II (Fig. 8F,M,O; 0.7
µm), Azure II/Basic Fuchsin (Figs. 7A,F,
8B,C,G,L,H; 5 µm), or Delafield’s hematoxylin and eosin Y (H&E) (5 µm). One female
was Bouin-fixed, embedded in Durcupan,
and stained with Heidenhain’s triple chrome
stain (Fig. 8A,N; 2 µm). Material for Figure
7F was imbedded in Spurr’s medium (2 µm).
All staining procedures followed Romeis (’89).
Sections were cut on a Reichert microtome
with glass knifes and examined with an
Olympus BH-2 and a Zeiss–Axiophot microscope. Sections with untanned or slightly
tanned cuticles were from newly eclosed
adults, i.e., 18–24 hr of age (Figs. 6A, 7A,F,
8B,C,G,H,L); sections with fully tanned cuticles are from adults at least 1 month old
(Figs. 6B, 8A,F,M–O).
Specimens for scanning electron microscopy (SEM) were fixed in 4% formalin for 24
hr, sonicated for 10 min, treated with glycerin for 24 hr, and dehydrated in a graded
series of acetone or a graded ethanol series
with a final acetone treatment (30 min per
10% interval from 50% to 100% ethanol or
acetone; five males, five females, four fifthand three third-instar nymphs). After airdrying, they were mounted on aluminum
stubs, gold-coated, and examined under a
Zeiss DSM or ISI-100B SEM.
Body width (the distance between the
outer edges of the eyes) and pronotum width
(the distance between the lateral tips of the
suprahumeral horns) was measured to the
nearest 0.01 mm, using digital calipers. Densities of sensilla trichodea were measured
from en face whole mounts of dried pronotum fragments under a Wild stereomicroscope, using a grid ocular at 40⫻ magnification. Sensilla were counted indirectly by the
number of columns, as sensilla could not be
discerned individually but were always associated with columns (see under Results).
Outer ocular width was used as a measure
for body size, width between suprahumerals
as a measure for pronotum size. These and
the data on sensilla density were compared
using t-tests after being tested for normality
(KS-tests, 0.25 ⬍ P ⬍ 0.91) and homogeneity (F-tests, 0.18 ⬍ P ⬍ 0.49).
Systematic divisions are sensu Deitz and
Dietrich (’93). General gross morphological
terms follow Matsuda (’70); those specific for
membracids follow Buckton (’03). Terminology of sensilla follows Zacharuk (’85). Three
anatomical terms were coined to accommodate new findings. The choanidium of adults
(choan-, greek: ‘‘funnel’’ and -idium, greek:
‘‘diminutive for small structures’’) is the area
of fusion of the pronotal canal with the intersegmental membrane. The pronotal canal of
adults is a canal formed by the interior cuticular layer of the posterior reduplication.
The bases of sensilla trichodea are connected to the lumen of the posterior reduplication by columnar canals. ‘‘Distal’’ and
‘‘proximal’’ refer to the anatomical (not the
spatial) distance from the body’s center.
RESULTS
Fifth-instar nymphs
The prothorax consists of six sclerites: pronotum, episternum, epimeron, precoxal
bridge, sternum, and trochantin (Fig. 1).
From a ventral view (Fig. 1B) the sternum is
a small, nearly rectangular plate with two
pits marking the base of the furca that has
two furcal arms on each side. Anteriolaterally the sternum is continuous with a narrow precoxal bridge fused to the episternum.
There is no postcoxal bridge. The trochantin
lies between the coxa and the episternum.
The episternum is bordered posteriorly by
the pleural sulcus adjacent with the epimeron. At its dorsal end, the pleural sulcus
deepens into a pit (Fig. 1B) that is the origin
of the pleural apophysis (Fig. 1C,E). From a
lateral perspective, the apophyseal pit is
covered by the pronotal cone (Fig. 1D) lying
160
U.E. STEGMANN
Fig. 1. Prothoracic skeleton of fifth-instar nymphs of
Stictocephala bisonia, showing the prothoracic sclerites,
their endoskeletal characters and the substructures of
the pronotum. Bar ⫽ 1 mm. A: Diagrammatic representation of habitus (from a photograph in Remane and
Wachmann, ’93), pronotum black. B: Ventral view (sclerites dotted, membranes striped). C: Frontal view (dor-
sal and ventral processes cut off). D: Left side view.
E: Left side view into the right half. a, propleural apophysis; ap, apophyseal pit; b, precoxal bridge; c, coxa; con,
pronotal cone; dp, dorsal process; em, epimeron; es,
episternum; fp, furcal pit; fu, furca; s, sternum; sb,
suprahumeral bud; soc, supraocular callosity; t, trochantin; vp, ventral process.
on an edge formed by the pronotum. In situ,
the cone is largely covered by the eyes.
The main part of the pronotum extends
dorsal to this edge—a sclerite as broad as
the head in frontal view but converging more
dorsally in a triangular shape (Fig. 1C). From
a lateral view, the pronotum appears elongated in a ventrodorsal axis and bends over
PROTHORAX OF STICTOCEPHALA
the mesonotum, forming a tip (Figs. 1A,D,
2A). The pronotum covers the mesothorax
laterally where its sclerotized part gradually becomes membranous and contains the
stigma (not illustrated). Where the endoskeletal prephragma extends into the body cavity, the posterior pronotal margin joins the
mesonotum (Fig. 2A). For comparison with
adults, it should be emphasized that the
nymphal pronotum is single-layered
throughout, even though the integument
folds in the lateral extensions and in the
posterior tip, so that two layers come into
close contact (Fig. 1E). Internally, the pronotum is filled with hemolymph and fat body
cells that usually extend only into the bases
of the ventral and dorsal processes (Figs.
1D,E, 2C,E; see Table 1 for synonyms).
Hence, these processes are single-layered
extensions of the pronotal integument as are
the suprahumeral buds (Fig. 1D). The external pronotal surface is covered with sensilla
trichodea, each articulated in an elongate
base (Fig. 1B,C). Supraocular callosities are
located on the external surface lateral to the
ventral processes (Fig. 1C,D). Prothoracic
leg muscles originate on their interior side
(Fig. 2D).
Adults
Gross morphology of the prothorax
Female body size (ocular width) and pronotum size (suprahumeral width) are larger
than in males (Table 2). In both sexes, pronotum size correlates with body size, fitting a
positively allometric power function (Fig. 3).
Nevertheless, the shape and components of
the prothoracic skeleton, including pronotal
histology, are the same in females and males.
TABLE 1. List of prothoracic features previously
described for nymphal Stictocephala bisonia
Terminology
used in
this work
Dorsal and ventral processes
Suprahumeral
bud
Sensilla
trichodea on
elongated
bases
Supraocular callosities
Terminology
of previous
investigators
Source
[Drawn in figs.
10 and 11, pl.
xxiv, but not
named]
Median dorsal
spines
Pronotal horn
bud, suprahumeral horn
bud
Chalazae, lateral
scoli
Funkhouser (’17)
[Drawn, but not
named]
Quisenberry et
al. (’78)
Quisenberry et
al. (’78)
Quisenberry et
al. (’78)
Quisenberry et
al. (’78)
161
Hence, the following observations apply to
both.
Adults have the same prothoracic sclerites as nymphs: pronotum, episternum,
epimeron, precoxal bridge, sternum, and trochantin (Fig. 4; see Table 3 for synonyms).
Cervical sclerites were not found. The sternum is small, rectangular, and fused to the
episternum by the precoxal bridge (Fig. 4C).
No postcoxal bridge (postcoxale) was found.
External pits in the sternum mark the origin of the endoskeletal furca, whose lateral
arms merge on each side with the pleural
apophyses (Fig. 4B,E). The area of fusion
usually remains visible. The trochantin articulates freely with the coxa and the episternum. A marked pleural sulcus separates the
pleuron into the episternum and epimeron,
and its dorsal end forms a pit on the outside
(Fig. 4B,D), the base of the endoskeletal
pleural apophysis.
The adult pronotum, however, is more complex than its nymphal form, because it is
composed of two subunits: a proximal singlelayered region, and a distal double-layered
region. The proximal region is a singlelayered integument wall (Fig. 5C) defined
through its boundaries. Ventrally it extends
to the tergopleural boundary that has no
physical demarcation in adults, because the
propleuron fuses seamlessly with the pronotum. Nevertheless, the tergopleural boundary can be estimated to extend from the
pleural pit to the ventral edge of the (pronotal) ventral lobe (Fig. 4D) (Stegmann, ’97),
e.g., because the dorsal termination of the
pleural sulcus is a general criterion for the
tergopleural boundary in the pterygote prothorax (Parsons, ’67). The ventroanterior termination of the single-layered part of the
pronotum consists of the anterior pronotal
margin lined by the dorsal part of the cervical membrane (Figs. 5C, 7F). This membrane does not contain cervical sclerites. Dorsoposteriorly, the single-layered pronotal
region terminates with the posterior margin
of the pronotum that is lined by the intersegmental membrane (Figs. 5C, 7F). Mesally,
the posterior margin runs in immediate proximity to, and parallel with, the anterior pronotal margin: in a median section through
the proximal pronotum and adjacent areas,
the posterior margin ends very close to the
anterior margin, leaving only a narrow
single-layered strip (Fig. 7F). Thus, the prephragma is close to the occiput (Fig. 7F).
Laterally, the posterior margin bends ventrally in a curve ending near the ventral
162
U.E. STEGMANN
Fig. 2. Nymphs of Stictocephala bisonia. A: Diagrammatic representation of a median section through a
fifth-instar nymph showing the relations between prothorax (white), head (dark pattern), and pterothorax and
abdomen (light pattern). B: Sensillum trichodeum on
the pronotum (fifth instar). C: Sensillum trichodeum on
the dorsal process (fifth instar). D: Pronotal muscle
originating at the supraocular callosity (fifth instar).
E: Frontal section (third instar) with the pronotal interior filled with fat cells. D, dorsal; ba, base of sensillum
trichodeum; dp, dorsal process; e, eye; f, fat body cells;
mu, pronotal muscle; p, pronotum; ph, pharynx; pr,
prephragma; oe, esophagus; sg, salivary gland; soc, supraocular callosity.
edge of the ventral lobe (Fig. 5C). Within the
curve, the sclerotized pronotal canal joins
the intersegmental membrane in a funnelshaped zone (choanidium). A stigma is located within the posterior area of the intersegmental membrane (Fig. 5C). From a
frontal view (Fig. 4B), the single-layered region of the pronotum contains the supraocu-
lar callosities and the mesal parts of the
fossae. Muscles arise from the interior surface of the supraocular callosities (Fig. 7A),
whose external surfaces are covered with
low naps 5–11 µm in diameter (Fig. 7B). In
situ, the eyes fit into the shallow caves of the
fossae and the postgenae cover the anterior
part of the episternum.
163
PROTHORAX OF STICTOCEPHALA
TABLE 2. Sexual size dimorphism (mean ⫾ sd) in Strictocephala
Females
Outer ocular width (mm)
Suprahumeral width (mm)
n
Regression of pronotum size (y) on body size (x)
Regression coefficient
3.39 ⫾
(3.56; 3.1–3.5 [sic!])4
5.78 ⫾ 0.323
(5.99; 5.45–6.4)4
51
y ⫽ 1.0457 ⫻ x1.4012
0.7286
0.102
bisonia1
Males
2.98 ⫾ 0.122
4.83 ⫾ 0.353
61
y ⫽ 0.8053 ⫻ x1.6385
0.8755
1Outer ocular width (a measure of body size) is greater in females than in males, as is suprahumeral width (a measure of pronotum
size). In both sexes, these two measures are strongly correlated, fitting an allometric power function. With a ⬎1, the allometric
relationship is positive in both sexes. See also Fig. 3.
2Unpaired t-test, t ⫽ 19.9, P ⬍ 0.0001.
3Unpaired t-test, t ⫽ 15.0, P ⬍ 0.0001.
4Kopp and Yonke (’77); n ⫽ 20.
Distad of the posterior pronotal margin
the pronotum is double-layered; i.e., it consists of two adjacent integumental walls
(e.g., Fig. 6) forming a large, complexly
bent plane (about 50 µm thick). Frontal
(Fig. 4B) and ventral views (Fig. 4C) show
that the double-layered region forms the
strong suprahumeral horns. The median carina runs in the median plane across the
frontal pronotum (metopidium, Fig. 4B). Posterior to the suprahumerals the dorsum is
triangular in cross-section with the median
carina as its dorsal edge and both the left
and right lateral carinae (Fig. 4C) as its
ventral edges. Seen in median sections, the
double-layered region of the pronotum rises
dorsally over the head (Fig. 7F; metopidium), bends posteriorly in a wide arch extending as the posterior process, reflects and
continues anteriad to end over the scutellum
(Figs. 4E, 5A). The latter, reflected part
(⫽septum sensu Buckton, ’03) is concealed
by the dorsum and is seen en face only in
ventral view (Fig. 4C). More anteriorly, the
septum, with its lateral margins, separates
from the lateral carinae in a bow and its
Fig. 3. Relation between pronotum size and body size in Stictocephala bisonia. In both
sexes, pronotum size increases with body size following a positively (a ⬎ 1) allometric power
function. See also Table 2.
164
U.E. STEGMANN
Fig. 4. Prothoracic skeleton of adults of Stictocephala bisonia, showing the prothoracic sclerites, their
endoskeletal characters, and the substructures of the
pronotum. Bar ⫽ 1 mm. A: Diagram of habitus (from a
photograph in Remane and Wachmann, ’93), pronotum
black. B: Frontal view (sclerites dotted, membranes
striped). C: Ventral view. D: Left side view. E: Left side
view into the right half. a, propleural apophysis; ams,
anterior margin of the septum; ap, apophyseal pit; b,
precoxal bridge; c, coxa; ch, choanidium; d, dorsum; em,
epimeron; es, episternum; fp, furcal pit; fo, fossa; fu,
furca; h, humeral angle; lc, lateral carina; m, metopidium; mc, median carina; pc, pronotal canal; pp, posterior process; s, sternum; sh, suprahumeral horn; sp,
septum; soc, supraocular callosity; t, trochantin; vl, ventral lobe.
anterior margin contacts the scutellum (Fig.
4E). Laterally, the anterior margin of the
septum continues into the left and right
pronotal canals that run along the interior of
the dorsum and terminate in the choanidium (Figs. 4E, 5C). The pronotal canal is
seen only from an internal (Figs. 4E, 5C) or
ventral view (Fig. 4C), because only the inte-
165
PROTHORAX OF STICTOCEPHALA
TABLE 3. List of prothoracic features previously described for adult Stictocephala bisonia
Terminology used
in this work
Sternum
Episternum
Precoxal bridge
Furcal pits
Furca
Pleural apophyses
Trochantin
Pleural sulcus
Supraocular callosities
Suprahumeral horns
Median carina
Terminology of
previous investigators
Sternum
Episternum
Precoxa
Furcal pits
Furcal apodemes
Pleural apodemes
Trochantin
Pleural suture
Smooth impunctate areas above the eyes
Base of metopidium notched medially
above the vertex; Fig. 4
Suprahumerals
Suprahumeral horns
Pronotal horns
Metopidium
Carina
[Drawn but not named]
Median carina
Metopidium
Dorsum
Dorsum
Posterior process
Posterior process
Apex
Humeral angles
Upper episternal hook
Humeral angles
Upper episternal hook
Source
rior integument is arched in a semicircle
(Fig. 8B).
The pronotom attaches to the head and
mesothorax through the cervical and intersegmental membranes, respectively. Because of the shape and large size of the
pronotum, especially of its double-layered
part, there are seven areas of secondary
contact between pronotum and nonpronotal
body parts: (1) fossae: postgenae (Fig. 4B,C);
(2) metopidium: mesoscutum (Fig. 5A,B, arrowhead #1); (3) dorsum: mesoscutum (Fig.
5B, arrowhead #2); (4) dorsum: lateral projection of the scutellum (Fig. 5B, arrowhead
#3); (5) septum: scutellum (Fig. 5A, arrowhead #4); (6) septum: abdomen (Fig. 5A,
arrowhead #5); and (7) ventral lobe/humeral
angles: mesepisternum/upper episternal
hook (Fig. 7G).
Histology of the double-layered region
of the pronotum
The double-layered region of the pronotum consists of two integumental walls lying
adjacent and parallel to each other with
their cuticles locally fused to massive columns (Fig. 6). Between the two cuticles is a
lumen, an extension of the body cavity (Fig.
5F). This general composition is seen not
only in cross sections (e.g., Fig. 6), but also in
en face views of pronotum fragments (Fig.
Kramer (’50)
Kramer (’50)
Kramer (’50)
Kramer (’50)
Kramer (’50)
Kramer (’50)
Kramer (’50)
Kramer (’50)
Funkhouser (’17)
Kopp and Yonke (’77)
Branch (’13)
Funkhouser (’17)
Yothers (’34); Kramer (’50); Kopp and Yonke
(’77)
Branch (’13)
Yothers (’34)
Kopp and Yonke (’77)
Branch (’13); Funkhouser (’17); Kramer (’50);
Kopp and Yonke (’77)
Branch (’13); Funkhouser (’17); Kramer (’50);
Kopp and Yonke (’77)
Branch (’13); Funkhouser (’17); Kramer (’50)
Kopp and Yonke (’77)
Branch (’13); Kramer (’50)
Kramer (’50)
7C,E), in which only the cellular components within the lumen are stained dark,
while the cuticle layers remain transparent.
Thus, seen along their longitudinal axis, columns, consisting of massive, transparent cuticle, appear as light circles (Figs. 7E, 8E).
In pronota of newly eclosed adults, the
untanned or slightly tanned external cuticle
is approximately 4–8 µm thick, the internal
cuticle approximately 1 µm (internal cuticle/
integument ⫽ the cuticle/integument forming the posterior pronotal margin; external
cuticle/integument ⫽ the cuticle/integument
forming the anterior pronotal margin). When
tanning is completed the external cuticle
thickens to 25–40 µm, the internal cuticle to
3–8 µm, depending on where exactly measurements are taken. The columns in fully
tanned individuals attain a diameter of
40–70 µm in the metopidium, and about 20
µm in the dorsum. Tanned cuticle stains
light brown/green with Azure II/Basic Fuchsin and H&E, while untanned cuticle stains
red or pink. Large pits cover the external
surface of the external cuticle and can be
seen in the SEM (Fig. 7H) or as circles under
a stereomicroscope (e.g., Fig. 4B). Each pit
corresponds to one column (Fig. 6). On the
external surface of the internal cuticle each
column produces a low cone about 12–20 µm
in diameter (Figs. 6B, 7D, 7D insert). In
166
U.E. STEGMANN
Fig. 5. Prothoracic skeleton of adults of Stictocephala bisonia. A: Diagram of median section through
a female showing the relations between prothorax
(white), head (dark pattern), and pterothorax and abdomen (light pattern). Arrowheads, secondary contact
zones. B: Diagram of oblique-horizontal section showing
the relation between mesothorax (light pattern) and
proximal pronotum (double line). Arrowheads, secondary contact zones. C: Diagram of the right half of the
proximal prothorax showing the single-layered, proximal region of the pronotum as it relates to the doublelayered, distal region in dorsomedioposterior view;
sclerites transparent, membranes black. a, pleural
apophysis; aes, anterior part of the episternum; b, precoxal bridge; c, coxa; ch, choanidium; cm, cervical membrane; d, dorsum; ec, external cuticle; em, epimeron; fo,
fossa; fu, furca; h, head; ic, internal cuticle; im, intersegmental membrane; m, metopidium; pc, pronotal canal;
pp, posterior process; pop, postphragma; pr, prephragma;
s, sternum; sh, suprahumeral horn; sl, mesoscutellum; sp, septum; sti, stigma; su, mesoscutum; t, trochantin; ueh, upper episternal hook; vl, ventral lobe; 1–5,
areas of secondary contact between the pronotum and
other body parts: 1, metopidium/mesoscutum; 2, dorsum/
mesoscutum; 3, dorsum/lateral scutellum; 4, septum/
scutellum; 5, septum/abdomen.
sections stained with Methylene Blue/Azure
II the most exterior layer of the external
cuticle stains brownish, while the main cuticular body stains blue. Where the column
is sectioned through its axis, it can be seen
that the brownish cuticle extends into the
cone. The surface of the internal cuticle is
covered with tiny cuticular protuberances
(Fig. 7D, insert).
As the cuticles thicken after molting the
lumen becomes thinner (30–50 µm in newly
eclosed adults; ⱕ20 µm or less in fully tanned
individuals). The more dramatic effect of age
on the lumen, however, concerns its histology. Only in newly eclosed adults can epidermal cells be distinguished from hemocytes
and the (unstained) intercellular space
(Fig. 6A).
Epidermal cells are characterized by their
smooth cytoplasm, their oval, horizontal nu-
clei, their position along the internal surface
of the internal and external cuticles, and
their extensions that may run obliquely or
straight across the entire lumen (Figs. 6A,
8G,L). Extensions of both epidermal layers
seem to intertwine, implying the breakdown
of the basal lamina; however, epidermal extensions do not occur in areas in which the
two integumental layers are farther apart,
e.g., along the median carina (Fig. 7F) or the
pronotal canal (Fig. 8B).
Hemocytes are usually located in the
middle of the lumen (Figs. 6A, 8L), often
elongated horizontally, and situated along
tracheae or nerves (if present; Fig. 8G). They
usually occur as single cells, lack the extensions across the lumen, and have round nuclei (Fig. 8L). Their cytoplasm contains
densely packed granules that stain in the
same colors as epidermal granules, albeit
PROTHORAX OF STICTOCEPHALA
167
Fig. 6. Sections through the dorsum of Stictocephala
bisonia. A: The pronotal lobe of newly eclosed adults
showing the two, still thin cuticular layers comprising
the lumen with a large intercellular space that is filled,
e.g., with hemocytes. B: The pronotal lobe of matured
adults with the two, thickened cuticular layers showing
a lumen with reduced intercellular space and filled with,
e.g., nuclei. cn, columnar cone; cp, columnar pit; col,
column; ec, external cuticle; he, hemocytes; ic, internal
cuticle; nu, nucleus.
more intensively, especially in H&E and
Heidenhain’s stains (Fig. 8A). These granules are found both in non-lipid-fixed (Fig.
8A) and in lipid-fixed material (e.g., Fig. 8L).
No fat cells were found within the lumen,
except in the most ventroanterior part of the
median carina where a few cells enter from
the large fat body that fills the mid-sagittal,
dorsal region of the head, pro-, and mesothorax (Fig. 7F). Fat cells can be distinguished
from hemocytes by their position and type of
granules. While hemocytes usually occur as
single cells and occasionally in strands, fat
body cells form clumps containing many,
roundly shaped, large cells (Fig. 8A). Lipidfixed fat body cells (Fig. 7A,F) show a great
variety of small to large vesicles that may
also differ in color. For example (Azure II/
Basic Fuchsin; Spurr), within one cell, the
largest vesicles stain olive green, small
vesicles remain transparent, while others
stain blue, purple, and pink. Presumably,
only the large green vesicles contain a large
portion of lipids, because in non-lipid-fixed
material large areas of the fat body cells are
depleted, while small, dark granules remain
(Fig. 8A,N).
In fully sclerotized pronota (e.g., Fig. 6B),
the lumen is filled with four components: (1)
small, dark granules (Fig. 8M); (2) large,
sometimes entirely transparent compart-
ments that are only recognized by their
boundaries (Fig. 8F,O); (3) nuclei (Fig. 6B);
and (4) dendrites within columnar canals
(Fig. 8F). Neither cell bodies nor intercellular space can be found.
The cellular components described below
occur in the lumen of both teneral and old
adults. Tracheae are easily recognized by
their taenidia and by being unstained internally (Fig. 8C). Apparently, tracheae enter
the double-layered pronotum through the
pronotal canal (Fig. 8B) and other areas of
the metopidium and dorsum, but not through
the median carina. No attempt was made to
trace their branching patterns. Nerve
bundles are recognized by horizontal fibers
in cross sections (Fig. 8G). Individual nerves
entering the double-layered pronotum
through the pronotal canal (Fig. 8B) or
through the metopidium were traced back to
the prothoracic ganglion, using serial sections and gross dissections. The prothoracic
ganglion is fused to the mesothoracic ganglion but can be distinguished in microscopic sections by its neuropil. No nerve was
found within the median carina. The dorsal
vessel extends through the mesothorax into
the prothorax, ending near the pharynx/
esophagus transition (Fig. 7F), but no accessory pulsatile organs were found.
168
U.E. STEGMANN
Figure 7
169
PROTHORAX OF STICTOCEPHALA
TABLE 4. Density of sensilla trichodea per 0.2 mm2
(mean ⫾ sd) 1
Sensilla trichodea articulate in the center
of the pits on the external cuticle (Figs.
7E,H, 8E,F). A columnar canal runs through
the column to the base of the seta (e.g., Fig.
8E) containing the dendrite(s) (Fig. 8F), but
cell bodies could not be localized. Type A
setae (Figs. 7H, 8E) are shorter and thinner
(approximately 25–40 µm long, n ⫽ 24; approximately 1 µm diameter, n ⫽ 10) than
type B setae (approximately 65–80 µm long,
n ⫽ 29; approximately 3.5 µm diameter,
n ⫽ 6) (Figs. 7H, 8F). At least the setae of
B-sensilla are hollow (Fig. 8F), but no cuticular openings on the setal surface were found.
The density of sensilla trichodea is greater
in males than in females, irrespective of the
pronotum region examined (Table 4). Both
males and females have a greater density on
the metopidium than on the dorsum (Table
4). Sensilla campaniformia occur in low densities on the external surface of the metopidial and dorsal external cuticle. The apical
dome appears as a circle in an en face view
(Fig. 8D), but can also be seen in cross sections through untanned (Fig. 8H) and fully
tanned cuticle (Fig. 8O). A canal through the
cuticle (approximately 6 µm wide) leads the
dendrite(s) (Fig. 8O). Sensilla coeloconica
(Fig. 8K,N) were only found in the fossae.
In metopidial and dorsal en face fragments, light circular structures of approximately 8–10 µm in diameter occur in the
focal plane of the lumen with a canal terminating on the surface (Fig. 8I). These openings are the small pores (diameter approximately 3 µm) seen in the SEM (Figs. 7H, 8J).
The canals through the external cuticle are
distinguished from those of sensilla campaniformia in that they consist of an approximately 5 µm wide basal part, an approximately 1 µm wide apical part (Fig. 8I,M),
and an approximately 4 µm wide sphere just
below the external opening (Fig. 8L,M).
Fig. 7. Prothorax of adult Stictocephala bisonia.
A: Sagittal section through the supraocular callosity
and the origin of prothoracic muscles. B: En face view of
the supraocular callosity with its naps. Scanning electron micrograph (SEM). C: En face view of the septum
demonstrating its composition of two cuticular layers
(unstained ⫽ transparent) that comprise a lumen of cellular nature (dark). D: Outer surface of internal, metopidial cuticle covered with columnar projections (arrowhead and insert) that each corresponds to one column.
SEM. E: En face view of metopidium demonstrating its
composition of two cuticular layers (unstained ⫽ transparent) that comprise a lumen of cellular nature (dark);
columns remain transparent because they consist of
massive cuticle. F: Mid-sagittal section through the
proximal metopidium and adjacent areas demonstrating the double-layered nature of the pronotal lobe and
the connection between its lumen and the body cavity;
note the prephragma near the occiput. G: Lower base of
left forewing showing sensilla trichodea (arrowhead)
that may touch the humeral angle. SEM. H: Outer
surface of external cuticle with openings of dermal glands
(arrowheads) and the two types of sensilla trichodea.
SEM. A, anterior; D, dorsal; am, anterior margin of the
pronotum; cc, columnar canal; cm, cervical membrane;
col, column; dv, dorsal vessel; ec, external cuticle; f, fat
body cells; h, humeral angle; ic, internal cuticle; im,
intersegmental membrane; m, metopidium; mc, median
carina; mu, pronotal muscle; n, nap; oe, esophagus; ot,
occiput; pm, posterior margin of the pronotum; pr, prephragma; sg, salivary gland; st, sensilla trichodea; su,
mesoscutum; ueh, upper episternal hook.
Prothoracic sclerites of last-instar nymphs
and adults
Last-instar nymphs and adults of Stictocephala bisonia share the same prothoracic
sclerites (pronotum, epimeron, episternum,
sternum, prexocale, and trochantin) and endoskeletal features (pleural apophysis and
furca). However, in adults the lateral furcal
arm on each body side is fused with the
pleural apophysis, while in nymphs it is not.
With the exception of the epimeron, these
sclerites and their endoskeletal components
were already recognized in adults of S. bisonia by Kramer (’50) and his findings were
later confirmed (Hasenoehrl and Cook, ’65;
Table 3). As in those studies, no cervical
sclerites and no postcoxal bridge were found
in the present study.
The first report on the various prothoracic
sclerites of (generalized) adult membracids
was from Funkhouser (’17), who acknowledged the pronotum, episternum, epimeron,
trochantin, and sternum. He did not describe endoskeletal structures. The pronotum, episternum, sternum, precoxale, trochantin, pleural apophysis, and furca were
also found in adult Oxyrhachinae (Has-
Metopidium
Dorsum
n
Females
Males
27 ⫾
17 ⫾ 23,5
17
33 ⫾ 42,4
22 ⫾ 34,5
15
32,3
1In
both males and females, the density of sensilla trichodea is
greater on their metopidium than on their dorsum. Males, however, have more sensilla per area than do females both on the
metopidium and on the dorsum.
2Unpaired t-test, t ⫽ 4.7, P ⬍ 0.0001.
3Paired t-test, t ⫽ 12.4, P ⬍ 0.0001.
4Paired t-test, t ⫽ 10.6, P ⬍ 0.0001.
5Unpaired t-test, t ⫽ 6.2, P ⬍ 0.0001.
DISCUSSION
Figure 8
PROTHORAX OF STICTOCEPHALA
enoehrl and Cook, ’65) and Centrotinae
(Ahmad and Afzal, ’78; Ahmad and Khan,
’79). Hence, the composition of the pleuron
remains the only controversial issue with
respect to the number of sclerites of the
membracid prothorax (Stegmann, ’97).
The pronotum is a ‘‘spine’’ in nymphs. . .
A basic difference between pronotal
anatomy of adults and nymphs of Stictocephala bisonia was found in this study: the
interior of pronotal substructures, e.g., suprahumerals/suprahumeral buds, communicates with the body cavity in nymphs but is
air-filled in adults.
A single-layered outgrowth of the integument communicating with the body cavity is
termed ‘‘Dorn’’ (Weber, ’33) or ‘‘spine’’
(Snodgrass, ’35). Thus, in Stictocephala bisonia, not only the nymphal pronotal substructures are ‘‘spines,’’ but the entire nymphal
pronotum is a large ‘‘spine.’’ This result may
well be generalized to the homologous
nymphal pronota of the Membracidae, because, in Tricentrus albomaculatus, Kershaw (’13) found that the ‘‘tegumentary
bristles of the nymph are hollow and communicate with the body cavity.’’ Judging from
his diagram (fig. 1, Kershaw, ’13), he re-
Fig. 8. Prothorax of adult Stictocephala bisonia.
A: Frontal section through left choanidium showing the
connection between hemocytes and fat cells. B: Frontal
section through left pronotal canal with nerves and
tracheae. C: Trachea in the metopidium of a newly
eclosed female. D: Apical dome (arrowhead) of a sensillum campaniformia in the metopidium, en face view.
E: Cuticular column with a B-type sensillum trichodeum (arrowhead) and its columnar canal. F: A-type
sensillum trichodeum (arrowhead) in a pronotal pit with
dendrite inside the columnar canal; a small part of
cuticle accidentally broke off. G: Dorsum of a newly
eclosed adult showing the intercellular space with epidermal feet, hemocytes and a nerve. H: Sensillum campaniformia in the metopidium (arrowhead on apical dome) of
a newly eclosed adult. I: En face view of dermal gland
with opening on the exterior cuticle (arrowhead), the
canal through the external cuticle, and, toward the left,
a basal area (dark area with light circle inside). J: Opening of dermal gland on the exterior cuticle. SEM. K: Sensillum coeloconicum in the fossa. SEM. L: Cross section
through suprahumeral horn with opening of dermal
gland (arrowhead). M: Cross section through a matured
metopidium showing a cuticular canal with its opening
on the external cuticle (arrowhead). N: Sensillum coeloconicum in the fossa showing its apical area surrounded
by the external cuticle. O: Sensillum campaniformia in
the metopidium (arrowhead on apical dome) of a matured adult. D, dorsal; cc, columnar canal; col, column;
ec, exterior cuticle; ep, epidermal cells; f, fat body cells;
he, hemocytes; ic, internal cuticle; mu, pronotal muscle;
ne, nerve; sc, sensillum coeloconicum; tr, trachea.
171
ferred to the elongated bases of sensilla, but
also to tergal substructures such as the dorsal processes.
Except for Kershaw’s (’13) findings, the
nymphal pronotum and its substructures
were known only with respect to external
morphology. Pronotal processes were reported from Stictocephala bisonia (Funkhouser, ’17; Quisenberry et al., ’78; see Table 1) and other membracids (e.g., Stoll, 1788;
Syn.: ‘‘tuberosities’’: Yothers, ’34). Suprahumeral buds occur in several New World
genera (Quisenberry et al., ’78), in many
Oxyrhachinae (Capener, ’62), and in many
Centrotinae (Capener, ’68). Published figures show setae (as ‘‘chalazae’’ and ‘‘scoli’’)
on the nymphal pronotum of S. bisonia and
other New World genera (Quisenberry et al.,
’78), but also on the pronotum of several
Centrotinae species (Capener, ’68). These
setae are presumably sensilla trichodea.
Nymphal supraocular callosities were labeled as such in the Oxyrhachinae (Capener,
’62) but were also depicted in figures of S.
bisonia, of several other New World species
(Quisenberry et al., ’78), and of Centrotinae
species (Capener, ’68).
. . . but a ‘‘posterior reduplication
of the notum’’ in adults
Except for the proximal single-layered region, the pronotum of adult Stictocephala
bisonia is a plate arched in itself far beyond
the body outline, covering the pterothorax
and abdomen and forming extensions (e.g.,
suprahumeral horns) that are hollow in the
sense that their interior does not communicate with the body cavity, but with the air;
the pronotal plate is composed of two integumental layers connected through cuticular
columns comprising a lumen that communicates with the body cavity. Therefore, what
appear to be the lateral pronotal margins,
i.e., the lateral carinae, are blind endings of
the pronotal plate, not the true terminations
of the sclerite (which are lined, per definitionem, by membranes). In short, the distal
region of the adult pronotum is a double
layer or lobe—an exceptionally large ‘‘posterior reduplication of the notum’’ sensu
Snodgrass (‘‘the posterior edge of the notum
folded downward and forward upon itself,
leaving a free margin overlapping succeeding parts’’; Snodgrass, ’09).
In Stictocephala bisonia, the plate aspect
might be inferred from Branch’s (’13) remark that the dorsum forms a ‘‘tectiform
hood’’ and from drawings by Kramer (fig. 72,
172
U.E. STEGMANN
pl. ix and fig. 106, pl. xii, Kramer, ’50). On a
greater taxonomic scale, the plate aspect
was the first insight into pronotal anatomy
of adult membracids (Buckton, ’03; Branch,
’13; Funkhouser, ’17; Marcus, ’50; Kopp and
Yonke, ’72; Strümpel, ’72). For example,
Buckton (’03) wrote that ‘‘the remarkable
spines of these insects have no bulbous origin, but are hollow tubes rising directly from
the surface’’ and are ‘‘filled with air.’’
Whether this pronotal plate is singlelayered (massive cuticle) or double-layered
(lobe) remained controversial. A massive cuticle could be inferred from drawings of
Stictocephala bisonia (fig. 72, pl. ix and fig.
106, pl. xii, Kramer, ’50), Entylia bactriana
(fig. 1, Kopp and Yonke, ’72), and a generalized membracid (fig. 36, Strümpel, ’72). But
studies focusing on the composition of the
plate always revealed living tissue. Nerves
and tracheae were reported from Aethalion
sp., Aconophora sp., Alchisme sp. (Marcus,
’50), and linear structures (‘‘venas’’) associated with stigmata were described in
Membracis spp., Lycoderes spp., Stegaspis
sp., Oeda inflata, and Gelastogonia sp. (Richter, ’54). Eventually, Wood (’75b) found that
‘‘a matrix of cells between two cuticular layers characterize the wall of the expanded
pronotum’’ of Umbonia crassicornis.
The location of the posterior pronotal margin, the course of the intersegmental membrane, and the presence of a proximal, singlelayered pronotal area were not previously
reported in the Membracidae. This led to
considerable confusion as reflected, e.g., by
Kramer’s (’50) misinterpretation of the posterior pronotal margin in Stictocephala bisonia as a ‘‘muscle partition formed by [the]
apodemal wall of [the] pronotum’’ (mp—fig.
106, pl. xii). Also, it was difficult to understand why and exactly which part of the
pronotum is detachable in Anchistrotus spp.
and why this apparently does not harm
the insect (e.g., Boulard, ’83, Strümpel, ’83,
Rietschel, ’87). It seems that if the gross
morphological (pronotal plate) and histological aspects (double layer) had been considered together, the conspicuous part of the
membracid pronotum would have been immediately recognized as the posterior reduplication of the pronotum.
In this study, internal and external cuticle
of the lobe were found to be fused to columns
with each column associated with an external pit. Both also occur in beetle elytra that
represent another type of lobe (e.g., Weber,
’33; Reuter, ’36; Krzelj, ’69). External pits
were reported by earlier workers in Stictocephala bisonia (‘‘punctured,’’ Branch, ’13;
‘‘punctate,’’ Funkhouser, ’17; ‘‘impunctations’’ Kramer, ’50) and other membracids
(Fabricius, 1803; Kirby, 1829; Buckton, ’03).
Columns were never explicitly described in
the Membracidae; however, a close look at
some studies suggests their presence in many
species. Buckton’s (’03) ‘‘shallow depressions
or punctures’’ appeared as ‘‘bright dots when
suitably placed’’ and could easily be interpreted as columns, because this is the way
they appear in en face views (of S. bisonia).
For the same reason Marcus’ (’50) ‘‘cercos
redondos’’ in the pronota of Aethalion sp.,
Aconophora sp., and Alchisme sp. could be
interpreted as columns, especially because
they correspond to external pits (‘‘hoyuelos’’), at least in the proximal area of the
pronotum. A SEM study showed pronotal
pits in 100 species from six membracid subfamilies (Wood and Morris, ’74). If pronotal
pits are indeed associated with columns, columns are common to the Membracidae and
Aetalionidae.
From spine to lobe: morphogenetic
implications
When Latreille (1802) noted that ‘‘La larve
du membrace du genêt diffère peu de l’insecte
parfait’’ he was the first to indicate strong
similarities between nymphs and adults in
respect to the externally visible substructures of the pronotum. Prominent examples
are the dorsal spine in Umbonia crassicornis
(Pelaez, ’40, ’41) and the dorsal bulb in
Anchistrotus amitteraglobus (Boulard, ’83).
Such pronotal substructures were generally
interpreted as adult primordia, e.g.,
Funkhouser’s (’17) ‘‘vestigial lateral horns’’
(⫽suprahumeral buds) in the Ceresini. Consequently, postembryonic pronotal development was regarded as a progressive, molt-tomolt enlargement (e.g., Funkhouser, ’17;
Strümpel, ’72), suggesting shifts in body proportions but minor morphological change.
But occasionally, even the external pronotal
development seemed to exceed paurometabolism (Müller, ’84).
If pronotal substructures of membracid
nymphs are indeed ‘‘spines,’’ e.g., suprahumeral buds, then they are anatomically
distinguished from adult features of similar
appearance, e.g., suprahumeral horns, that
are parts of the pronotal ‘‘reduplication.’’
Therefore, nymphal substructures are not
early (small) stages of adult substructures.
PROTHORAX OF STICTOCEPHALA
Rather, they may be regarded as sheaths
inside of which the adult substructures develop, necessarily taking the approximate
shape of adult processes. I hypothesize that
the primordium of the adult pronotum develops only within last-instar nymphs, i.e., between apolysis and adult ecdysis, because
otherwise an imaginal disc (non-cuticleproducing epidermis) must be assumed,
which is known only from Holometabola.
Occasional reports of postecdysial expansion of the pronotum (Richter, ’54;
Suchantke, ’76; personal observation in laboratory colonies of Stictocephala bisonia) provide circumstantial evidence for (1) the existence of a unique adult primordium within
the pronotum of last-instar nymphs and for
(2) the hypothesis that due to limited space
within the nymphal sheath the adult primordia unfold completely only after ecdysis.
Membracid last-instar nymphs fasten themselves to the underside of a leaf or twig
before ecdysis (e.g., Funkhouser, ’17; personal observation in S. bisonia). Hanging
upside down, adults may help to expand the
pronotal lobe as they do with their wings.
Another line of evidence for a separate
adult primordium in Stictocephala bisonia
and its expansion after adult ecdysis comes
from histological parallels between postecdysial development (1) of insect wings and
(2) that of the pronotal lobe of S. bisonia.
These parallels concern the occurrence of
epidermal feet and hemocytes, the presumed lack of a basement membrane, the
dissolution of cell membranes, and the disappearance of intercellular space with age.
Pronotal lobes of newly eclosed Stictocephala bisonia exhibit epidermal feet connecting the two integumental layers, thereby
leaving ample space in between for hemolymph. Epidermal feet (Locke and Huie, ’81)
seem to intertwine in S. bisonia, because
extensions of both epidermal layers may form
a single strand on a light microscopical level.
Such epidermal feet are known from the
development of other lobes, such as wings
(e.g., Rehberg, 1886; Weber, ’33; Chapman,
’82; Nardi and Magee-Adams, ’86) and antennal primordia (e.g., Keil and Steiner, ’90).
Intertwining of epidermal feet without the
occurrence of a membranous middle layer
implies breakdown of the basement membrane, which was observed in the development of wings (e.g., Weber, ’33; Chapman,
’82; Nardi and Magee-Adams, ’86), and antennae (e.g., Steiner and Keil, ’93).
173
Hemocytes are regularly found in double
layers like wings (e.g., Reuter, ’36; Zeller,
’38; Nardi and Magee-Adams, ’86) and antennal primordia (Keil and Steiner, ’90; Steiner
and Keil, ’93), where they are involved in the
formation (Nardi and Miklasz, ’89) and
breakdown of the basement membrane
(Nardi and Miklasz, ’89; Steiner and Keil,
’93). ‘‘Hemocyte’’ is used here in the widest
sense, meaning ‘‘the loose cells in the body
cavity of insects’’ (Wigglesworth, ’65). This
definition incorporates the fact that often
there is no sharp distinction between freefloating fat cells and hemocytes sensu stricto
(Wigglesworth, ’65; Chapman, ’82). A similar
situation is suggested for Stictocephala bisonia, because (1) the dominance of nonlipid
granules clearly separates the hemocytes in
the pronotal lobe from fat body cells, but (2)
the hemocytes are linked to the fat body, and
(3) are unusually large. Whatever the genesis of these hemocytes in S. bisonia, the
parallels to the loose cells in wings are obvious: the granules, the position in the middle
of the lumen and between the epidermal
feet, and the presumed mechanism of entering into the lumen by blood pressure during
inflation.
In the fully sclerotized pronotal lobe of
Stictocephala bisonia, the intercellular space
occurring in teneral adults has disappeared.
Whether cell membranes dissolve or still
exist in the sclerotized lobe, albeit not visible on a light microscopic level, remains an
open question. In postecdysial insect wings,
the intercellular space disappears (e.g.,
Weber, ’33; Zeller, ’38), cells fuse after dissolution of the basement membrane and the
lumen either becomes a syncytium or is completely reduced (e.g., Weber, ’33).
Gross morphological features
of the adult pronotum
The general, external shape of the adult
pronotum of Stictocephala bisonia was often
portrayed illustrating features such as the
metopidium, the dorsum, the suprahumeral
horns, the humeral angles, and the posterior
process (Marlatt, 1894; Buckton, ’03; Branch,
’13; Funkhouser, ’17; Yothers, ’34; Poisson,
’37; Kramer, ’50; Kopp and Yonke, ’77; for the
following, see Table 3). The fossae were not
previously described or illustrated for S. bisonia but were reported from several other
species (Branch, ’13; Funkhouser, ’17; drawn
in: Richter, ’54; Wood, ’75b; Ahmad and Khan,
’79). Supraocular callosities in adults were
noticed early in S. bisonia (Funkhouser, ’17;
174
U.E. STEGMANN
Poisson, ’37; Kopp and Yonke, ’77) and many
other genera (e.g., Fowler, 1894; Buckton,
’03; Funkhouser, ’17; Capener, ’62; Capener,
’68). Capener (’62) remarked that ‘‘their function is unknown,’’ but in Anchistrotus spp.
Boulard (’83) noted that muscles of the forelegs originate at the callosities, as was also
found in S. bisonia. Kramer (’50) described
the musculature of S. bisonia but neither
mentioned nor depicted the callosities. At
this point it is uncertain whether muscle
origins are confined to the callosities.
The septum was never described in Stictocephala bisonia, but its external traces can
be found in figures of S. bisonia (Kopp and
Yonke, ’77) and of S. diceros (as Ceresa diceros) (Branch, ’13). It was first recognized by
Buckton (’03) in Hemiptycha punctata, and a
similar structure was located in Anchistrotus sp. (‘‘Unterseite des Pronotums’’:
Rietschel, ’87). Possibly, the septum occurs
in many treehopper species but was overlooked as in S. bisonia. Other internal substructures are the pronotal canals containing nerves and tracheae. Similar features,
two pairs of internal ridges containing tracheae, were mentioned in Umbonia crassicornis (Wood, ’75b). Although some type of accessory pulsatile organs (e.g., Krenn and Pass,
’94) may be expected in the membracid pronotum, no membranous canals or layers were
found within the pronotal canal and the
median carina of S. bisonia. Nevertheless, a
more detailed future investigation may reveal them, possibly in the lateral areas.
As described for Stictocephala bisonia
(Kramer, ’50) and a generalized membracid
(Funkhouser, ’17) the prothoracic stigma is
located in the intersegmental membrane just
anterior to the mesepisternum, a common
position in insects (Weber, ’33; Snodgrass,
’35). Connections from the stigma to the
meso- and prothoracic tracheae were found
in S. bisonia, but not in Umbonia crassicornis, where an ‘‘external opening’’ in or near
the lateral part of the fossa was interpreted
as the opening of prothoracic tracheae (Wood,
’75b). In S. bisonia, a similar pit represents
the external base of the pleural apophysis.
Richter (’53) mentioned proximolateral stigmata in several genera. However, their exact position remains obscure, despite later
drawings (Richter, ’54).
Richter (’53) interpreted the distal pronotum as being transformed prothoracic wings
fused along their costal margins to form the
median carina. He described ‘‘venas’’ and
pronotal areas (e.g., ‘‘parte dorsal,’’ ‘‘membrana basal’’) that supposedly correspond to
wing veins and wing areas, respectively, but
cannot be located despite later figures (e.g.,
figs. 7–10; Richter, ’54). He further assumed
that the distal pronotal plate was fixed to
the proximate pronotum by muscles, but
seems to have confused the mesonotum with
the pronotum (Boulard, ’73), because he depicted propleural characters (‘‘ondulaciones
y dilataciones pleurales’’) on the lateral part
of the mesonotum (fig. 7, Richter, ’54). Boulard’s (’73) arguments against Richter’s hypothesis still hold: median carinae occur in
many insects, the only muscles found are
those inserting on the occiput and anterior
legs, and in nymphs there are no indications
for paired buds.
Cuticular canals and sensilla
of the pronotal lobe
Because of their abundance and wide distribution, cuticular canals in the external
cuticle of the metopidium and dorsum of
Stictocephala bisonia are most easily interpreted as ductules of exocrine glands, specifically of class 3 gland cells (Noirot and
Quennedey, ’74). Apart from the light circles
in en face views, no indications for corresponding cell bodies were identified, though.
In the pronotum of Umbonia crassicornis,
two of three cell types (‘‘large cuboidal cells’’
and ‘‘squamous epithelial cells with elongate
nuclei’’) were regarded as ‘‘probable secretory and/or neurosecretory cells’’ on the basis of similarities in staining properties to
neurosecretory cells in a brain (Wood, ’75b).
This interpretation is questionable, though,
because neither the brain nor the similarities were detailed, and an unspecific stain
(H&E) was used to demonstrate similarities. These difficulties also weaken the hypothesis that, because pronotal pits are surrounded by those cells ‘‘the pits function as
chemoreceptors or perhaps as dispersal sites
for pheromones’’ (Wood, ’75b). In S. bisonia,
pronotal pits are not chemoreceptors and
there are no indications that pheromones
diffuse through the cuticle of pits whose
bases are massive, cuticular columns. As
suggested by circumstantial evidence (see
above), other species are likely to share these
features of S. bisonia.
Setae were noticed early in Stictocephala
bisonia (Funkhouser, ’17) and many other
membracids (e.g., Fairmaire, 1846; Fowler,
1894; Buckton, ’03; Branch, ’13; Funkhouser,
’17; Capener, ’62; ’68). Marcus (’50) first real-
PROTHORAX OF STICTOCEPHALA
ized their morphology to be that of sensilla
trichodea (‘‘cerda táctil’’) and documented
their innervation in three genera. Pronotal
sensilla trichodea in Umbonia crassicornis
are innervated, as well (Wood, ’75b). Sensilla campaniformia were not previously described in the Membracidae and sensilla coeloconica were only found on abdominal
tergites (Dietrich, ’89).
Males of Stictocephala bisonia have
greater sensilla trichodea densities than females. However, in absolute terms males
have fewer sensilla than females, because
comparing the factor of density increase (‘‘D’’)
with the squared factor of pronotal size decrease (i.e., the correction term, ‘‘P’’) gives
D ⬍ P2 both for the metopidium [1.223 ⬍
(1.197) 2] and for the dorsum [1.295 ⬍
(1.197) 2] (data from Table 4); if absolute
sensilla numbers were equal between the
sexes, the expected relation was D ⫽ P2. It
cannot be decided at this point whether the
observed differences represent sex-specific
functions or males achieve the same functions as females with increased sensilla density, tolerating fewer sensilla in absolute
terms.
Biological functions of the pronotal lobe
From the various adaptive (e.g., Kirby,
1829; Poulton, ’03; Wood, ’93) and nonadaptive explanations for pronotal enlargements
(e.g., Funkhouser, ’21; Strümpel, ’72; Boulard, ’73), only the mechanical defence and
aposemantic coloration hypotheses were
tested. In captivity studies, mature Umbonia crassicornis were protected from being
swallowed by a natural predator (Anolis)
mainly due to their acute dorsal horns (Wood,
’75a, ’77). However, pronota of eight other
species were not mechanically protective
(Wood, ’75a). The conspicuously colored, teneral adults of U. crassicornis and Platycotis
vittata are unpalatable to Anolis and Anolis
learns to avoid this prey, suggesting an
aposemantic role of the pronotum (Wood,
’75a). However, at least in U. crassicornis
pronotal coloration did not promote learning
to avoid adults (Wood, ’77). Possibly, Anolis
instead recognizes pronotal shape (Wood,
’77). It is likely, but has not been tested, that
the pronotum itself contributes to unpalatibility.
A group of adaptive hypotheses refers to
pronotal physiology and a critical evaluation
of facts and arguments is appropriate. Accordingly, pronotal enlargement is due to
selection on the pronotum for increasing sur-
175
face area, because this would either (i) increase ‘‘the amount of directional sensory
input’’ (Wood and Morris, ’74; Wood, ’93) or
(ii) ‘‘facilitate dispersal of volatiles’’ (Wood,
’93). Various sensory functions were proposed (Marcus, ’50; Wood, ’75b, ’93), e.g.,
‘‘the detection of odor, air currents, or airborne sound’’ (Wood and Morris, ’74). These
functions could mediate intraspecific communication (Wood, ’75b), e.g., when males touch
the female’s pronotum during precopulatory
behavior (Wood, ’93).
In a narrow sense, these hypotheses potentially could explain pronotal size, but not
shape (Strümpel, ’83), because the same surface area may be achieved by many shapes.
However, additional hypotheses on how
shape affects perception or pheromone dispersal could be proposed. Although it is true
that the pronotal lobe is a living tissue and
most probably its components have special
functions, it is not self-evident to postulate
any of these functions as one or the main
adaptive reasons for past or current evolution of the lobe. Reversing the argument is
just as plausible. Sensilla may occur, because sensory input from an already large
and exposed sclerite is no less vital than it is
from other sclerites. Similarly, pheromonal
glands may occur in the pronotum simply
because it is more exposed than many other
sclerites. Thus, physiological functions, by
themselves, neither exclude (other) adaptive
hypotheses of pronotal evolution nor nonadaptive explanations such as correlated response to increasing body size (e.g.,
Strümpel, ’72; Boulard, ’73).
While sensilla occur in many species, so
far there is no evidence for pheromone glands
within the pronotal lobe, a prerequisite for
the pheromone dispersal hypothesis. Cells
found in the pronotum of Umbonia crassicornis (Wood, ’75b) are not necessarily gland
cells (see above), and if they are, they might
not produce pheromones. As dermal glands
they may well be involved in cuticle formation (Chapman, ’82). Moreover, there is no
evidence for pheromones as a regular means
of communication between living individuals or as a means of defence. Sex pheromones are not known in membracids (Wood,
’93) and alarm pheromones were released
only after deadly ruptures of the body wall
(Nault et al., ’74; Wood, ’76). Finally, intraspecific communication, a central target of
surface hypotheses, was shown to be mediated by vibrational signals (Strübing, ’92;
176
U.E. STEGMANN
Hunt, ’93; Cocroft, ’96). It is likely, but unknown, whether other sensory modes are
involved (e.g., Hunt, ’93).
In summary, while the mechanical defence hypothesis was supported in one species, the aposemantic coloration hypothesis
was not and whether the physiological functions of the pronotal lobe are (part of) its
adaptive causes is just as likely. Conclusions
at the highest explanatory level, i.e., adaptive versus nonadaptive hypotheses, could
be drawn from tests of nonadaptive hypotheses, for example, by deriving and testing
central predictions such as genetic correlations.
ACKNOWLEDGMENTS
I am deeply indebted to Dietrich Mossakowski, Harald Witte, and Gundula Sieber
(Bremen) for advice and equipment and to
Hildegard Strübing (Berlin) for donating
her colony of Stictocephala bisonia. Many
others helped in various ways: B. Ehmer,
C. Gehrig, W. Gronenberg, G. Hartwig, A.
Hoh, H. Karsten-Wohltmann, C. Kleineidam, G. Krohne, G. Krüger, K.E. Linsenmair, H. Meyer, M. Obermayer, S. Osterkamp, G. Roth, K. Schauz, H.-B. Schikora,
H. Strümpel, A. Toltz, W. Vogel, J. Warner,
and A. Wohltmann. I am very grateful to
Lewis L. Deitz, Wulfila Gronenberg, Frederick W. Harrison, Frank-Thorsten Krell, Thomas K. Wood, and two anonymous referees
for reading and commenting on the manuscript. This study was supported by the Studienstiftung des deutschen Volkes.
This work is dedicated to Dr. Rupert Wild
(Staatliches Museum für Naturkunde Stuttgart, Germany) for a long period of sensible
encouragement.
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