An exaggerated trait in insects: The ... - Ulrich E. Stegmann · An Exaggerated Trait in Insects: The Prothoracic Skeleton of Stictocephala bisonia(Homoptera: Membracidae) ULRICH

An Exaggerated Trait in Insects: The Prothoracic Skeletonof Stictocephala bisonia (Homoptera: Membracidae)

ULRICH E. STEGMANN*Institut fur Okologie und Evolutionsbiologie, Universitat Bremen,Bremen, Germany

ABSTRACT The prothoracic skeleton of Stictocephala bisonia was investi-gated in adults and fifth-instar nymphs on a gross morphological (SEM,maceration) and light microscopic level. In both nymphs and adults, theprothoracic skeleton consists of the pronotum, episternum, epimeron, precox-ale, sternum, trochantin, and two endoskeletal characters (furcal arms andpleural apophyses). In nymphs, the entire pronotum is a single-layeredoutgrowth of the integument communicating with the body cavity and filledwith hemolymph and fat body cells (‘‘spine’’); the dorsal and ventral processesand 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 twocuticular layers separated by a thin lumen. The posterior reduplication iselevated above the body and forms hollow (air-filled) extensions (e.g., supra-humeral horns). Its two cuticular layers are connected through cuticularcolumns that appear on the external surface as pits. The lumen between theselayers communicates with the body cavity and contains nerves and tracheae.In the lumen of newly eclosed adults, intercellular space, epidermal cells withlong processes, and hemocytes with nonlipid granules are present. In thelumen of sclerotized adult pronota, the intercellular space has disappeared,together with definite cell boundaries. Several structures are associated withthe external cuticle: two types of innervated sensilla trichodea that articulatein the center of external pits, sensilla campaniformia, sensilla coeloconica,and cuticular canals with exterior openings. The morphogenetic implicationsof pronotal construction, various aspects of adult prothoracic anatomy, andthe value of glands and sensilla for an adaptive interpretation of the prono-tum 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), thedorsal sclerite of the prothorax is extraordi-narily enlarged, assuming an array of bi-zarre shapes across the family—a fact thathas attracted an equally diverse communityof adaptive and nonadaptive hypotheses overthe decades and still awaits satisfactory evo-lutionary explanations (e.g., Wood, ’93). Indealing with the Membracidae, the taxono-mists of the eighteenth and nineteenth cen-turies (e.g., Linnaeus, 1758; De Geer, 1773;Stoll, 1788; Latreille, 1802; Fabricius, 1803;Germar, 1835; Burmeister, 1839; Amyot andServille, 1843; Fairmaire, 1846; Stål, 1859,1866; Fowler, 1894) based their work largelyon the external appearance of this sclerite

(the pronotum). These investigators intro-duced terms describing its commonly foundexternal characters: the lateral horn (‘‘cor-nus’’: Linnaeus, 1758), humeral angle(‘‘angles humeraux’’: Amyot and Serville,1843), posterior process (‘‘cornu postico’’: Stål,1859), and the frontal and dorsal parts of thesclerite (‘‘metopidium’’ and ‘‘dorsum,’’ respec-tively; Fowler, 1894).

The first achievement toward an under-standing of pronotal anatomy of the Membra-

Contract grant sponsor: Studienstiftung des deutschen Volkes.*Correspondence to: Ulrich Stegmann, Biozentrum,

Zoologie III, Am Hubland, 97074 Wurzburg, Germany.E-mail: [email protected]

JOURNAL OF MORPHOLOGY 238:157–178 (1998)

r 1998 WILEY-LISS, INC.

cidae was to recognize this sclerite in adultsas the pronotum in the proper anatomicalsense. Linnaeus (1758) attributed the scle-rite to the dorsal part of the thorax, and DeGeer (1773) correctly specified that it be-longed to the prothorax or ‘‘corselet.’’ DeGeer’s interpretation was challenged by Ger-mar (1835), who thought the exaggeratedsclerite was a unified dorsal thoracic plate.When Burmeister (1839) refuted Germar’sview, he was the first to explicitly acknowl-edge this sclerite as the notum of the protho-rax (‘‘Vorderrucken’’).

Buckton (’03) observed that the externalpronotal processes are not integumental out-growths communicating with the body cav-ity, but rather are parts of one enlarged,cuticular plate (‘‘shell’’: Buckton, ’03) extend-ing over the body and so arched as to formthese pronotal processes as hollow exten-sions (‘‘hollow chambers,’’ ‘‘air-chambers’’;Buckton, ’03). He illustrated his findings,establishing the ‘‘septum’’ as an internalcharacter of the pronotum and, for the firsttime, defined pronotal features that had beenused by taxonomists for more than a cen-tury. Referring to external processes, hemade the important observation that ‘‘thereare no corresponding sutures to mark themanatomically’’ (Buckton, ’03). Consequently,Buckton must have realized that even hisdefinitions were anatomically ambiguous.This conclusion may also be the backgroundto Funkhouser’s (’17) remark that the prono-tal processes ‘‘have no anatomical signifi-cance [sensu anatomical definition, U.E.S.]and are merely hollow extensions of the chi-tinized wall.’’ The considerable confusion inearly systematics, which relied largely ondescriptions of external pronotal morphol-ogy (e.g., Wood and Pesek, ’92), is likely tohave originated from this lack of sutures.

After Buckton’s (’03) pioneering work, theliterature became scattered with few cross-references, and his own study on pronotalanatomy was largely forgotten. While theexistence of the pronotal plate was acceptedby later investigators, as can be inferredfrom some of their drawings (Marcus, ’50;Kopp and Yonke, ’72; Strumpel, ’72), its inter-nal composition remained controversial.Some investigators apparently consideredthe pronotal plate to be a massive, cuticularstructure (Kramer, ’50; Kopp and Yonke, ’72;Strumpel, ’72), while others, working specifi-cally on pronotal histology, discovered livingtissue within (Marcus, ’50; Richter, ’54; Wood,’75b). With one exception (Rietschel, ’87),even basic gross morphological aspects ei-

ther were not investigated or remained ob-scure; e.g., the articulation of the pronotalplate with the rest of the body. Buckton (’03)depicted a ‘‘crescentic process for articulat-ing the pronotum’’ on the mesonotum, whileRichter (’53, ’54) assumed muscles to fix anextended part of the pronotum (‘‘apendicepronotal’’) to the rest of the sclerite. Knowl-edge of the prothoracic anatomy of nymphsremains restricted to the rough externalshape of the pronotum and its processesfound in various species (e.g., Funkhouser,’17; Yothers, ’34). Considering the numerousspeculations about the adaptive significanceor insignificance of the exaggerated prono-tum, this scarcity of knowledge about prono-tal anatomy is surprising.

Here, the prothoracic skeleton of adultsand last-instar nymphs of Stictocephala biso-nia, Kopp and Yonke (’77), was investigatedat the gross morphological and histologicallevel. Emphasis in both nymphs and adultswas on the attachment of the pronotum tothe rest of the body and on the histology andexternal morphology of the posterior redupli-cation in adults. The results are not onlydiscussed with respect to earlier studies onS. bisonia, but to any other membracid spe-cies in order to review the current knowl-edge of the prothoracic anatomy in theMembracidae. Stictocephala bisonia is a uni-voltine species that is widely distributed andseasonally abundant in North America (e.g.,Kopp and Yonke, ’73, ’77) and was intro-duced to Europe early in the twentieth cen-tury (e.g., Poisson, ’37; Hoffrichter andTroger, ’73; Gunthart, ’80).

MATERIALS AND METHODS

A colony of Stictocephala bisonia was ob-tained from H. Strubing (’92) and reared onVicia faba and Prunus amygdalus (for de-tails, see Stegmann, ’97). The exo- and endo-skeleton were investigated using specimens(six males, eight females, six fifth-instarnymphs) that were macerated for up to 1 hrin hot KOH (10%), washed, and dissectedunder a Wild stereomicroscope. Figures1B–E, 2A, 4B–E, and 5A–C are camera lu-cida drawings of specimens in glycerin. Dis-sections of muscles, nerves, and tracheaewere performed with four females fixed in4% formalin and half-embedded in paraffinwax (modified after Kramer, ’50), and withtwo males and one female, using a modifiedvital staining procedure (Yack, ’92) with sa-line (0.1 M phosphate buffer with 5.5% su-crose, pH 7.2) and 0.01% Janus Green B.

158 U.E. STEGMANN

Whole-mounts of the metopidium, dor-sum, and septum were prepared from twomales and four females; 0.5–3 mm2 frag-ments were cut in saline, fixed in 1.75%glutaraldehyde (in 0.1 M phosphate buffer,pH 7.2), washed, stained for 12–24 hr in0.75% Orange G, washed again, and thenstained for 12–24 hr in 0.5% Light Green.Fragments were then dehydrated in a gradedethanol series and mounted on microscopeslides in Entellan. Only cellular componentswere stained, while the cuticle remainedtransparent (Figs. 7C,E, 8D,E,I).

Sections for light microscopy were pre-pared from four males, four females, andtwo third-instar nymphs. After dissection insaline, relevant material was fixed in avacuum-desiccator for 1 hr and then for 24hr at 16°C (1.75% glutaraldehyde in 0.1 Mphosphate buffer, pH 7.2), and vacuum-washed in saline. Except for nymphs (Fig.2C–E) and one female (Fig. 8A,N), tissuewas postfixed for 24 hr at 16°C (2% osmiumtetroxide and 5.75% sucrose in 0.1 M phos-phate buffer) and washed. Following dehy-dration in a graded series of ethanol, mostmaterial was imbedded in Technovit 7100VLC, and stained with Toluidine BlueO/Methylene Blue (Fig. 2C–E; 10 µm),Methylene Blue/Azure II (Fig. 8F,M,O; 0.7µm), Azure II/Basic Fuchsin (Figs. 7A,F,8B,C,G,L,H; 5 µm), or Delafield’s hematoxy-lin and eosin Y (H&E) (5 µm). One femalewas Bouin-fixed, embedded in Durcupan,and stained with Heidenhain’s triple chromestain (Fig. 8A,N; 2 µm). Material for Figure7F was imbedded in Spurr’s medium (2 µm).All staining procedures followed Romeis (’89).Sections were cut on a Reichert microtomewith glass knifes and examined with anOlympus BH-2 and a Zeiss–Axiophot micro-scope. Sections with untanned or slightlytanned cuticles were from newly eclosedadults, i.e., 18–24 hr of age (Figs. 6A, 7A,F,8B,C,G,H,L); sections with fully tanned cu-ticles are from adults at least 1 month old(Figs. 6B, 8A,F,M–O).

Specimens for scanning electron micros-copy (SEM) were fixed in 4% formalin for 24hr, sonicated for 10 min, treated with glyc-erin for 24 hr, and dehydrated in a gradedseries of acetone or a graded ethanol serieswith a final acetone treatment (30 min per10% interval from 50% to 100% ethanol oracetone; five males, five females, four fifth-and three third-instar nymphs). After air-drying, they were mounted on aluminumstubs, gold-coated, and examined under aZeiss DSM or ISI-100B SEM.

Body width (the distance between theouter edges of the eyes) and pronotum width(the distance between the lateral tips of thesuprahumeral horns) was measured to thenearest 0.01 mm, using digital calipers. Den-sities of sensilla trichodea were measuredfrom en face whole mounts of dried prono-tum fragments under a Wild stereomicro-scope, using a grid ocular at 403 magnifica-tion. Sensilla were counted indirectly by thenumber of columns, as sensilla could not bediscerned individually but were always asso-ciated with columns (see under Results).Outer ocular width was used as a measurefor body size, width between suprahumeralsas a measure for pronotum size. These andthe data on sensilla density were comparedusing t-tests after being tested for normality(KS-tests, 0.25 , P , 0.91) and homogene-ity (F-tests, 0.18 , P , 0.49).

Systematic divisions are sensu Deitz andDietrich (’93). General gross morphologicalterms follow Matsuda (’70); those specific formembracids follow Buckton (’03). Terminol-ogy of sensilla follows Zacharuk (’85). Threeanatomical terms were coined to accommo-date new findings. The choanidium of adults(choan-, greek: ‘‘funnel’’ and -idium, greek:‘‘diminutive for small structures’’) is the areaof fusion of the pronotal canal with the inter-segmental membrane. The pronotal canal ofadults is a canal formed by the interior cu-ticular layer of the posterior reduplication.The bases of sensilla trichodea are con-nected to the lumen of the posterior redupli-cation by columnar canals. ‘‘Distal’’ and‘‘proximal’’ refer to the anatomical (not thespatial) distance from the body’s center.

RESULTSFifth-instar nymphs

The prothorax consists of six sclerites: pro-notum, episternum, epimeron, precoxalbridge, sternum, and trochantin (Fig. 1).From a ventral view (Fig. 1B) the sternum isa small, nearly rectangular plate with twopits marking the base of the furca that hastwo furcal arms on each side. Anteriolater-ally the sternum is continuous with a nar-row precoxal bridge fused to the episternum.There is no postcoxal bridge. The trochantinlies between the coxa and the episternum.The episternum is bordered posteriorly bythe pleural sulcus adjacent with the epim-eron. At its dorsal end, the pleural sulcusdeepens into a pit (Fig. 1B) that is the originof the pleural apophysis (Fig. 1C,E). From alateral perspective, the apophyseal pit iscovered by the pronotal cone (Fig. 1D) lying

PROTHORAX OF STICTOCEPHALA 159

on an edge formed by the pronotum. In situ,the cone is largely covered by the eyes.

The main part of the pronotum extendsdorsal to this edge—a sclerite as broad as

the head in frontal view but converging moredorsally in a triangular shape (Fig. 1C). Froma lateral view, the pronotum appears elon-gated in a ventrodorsal axis and bends over

Fig. 1. Prothoracic skeleton of fifth-instar nymphs ofStictocephala bisonia, showing the prothoracic sclerites,their endoskeletal characters and the substructures ofthe pronotum. Bar 5 1 mm. A: Diagrammatic represen-tation of habitus (from a photograph in Remane andWachmann, ’93), pronotum black. B: Ventral view (scle-rites 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 apophy-sis; 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, trochan-tin; vp, ventral process.

160 U.E. STEGMANN

the mesonotum, forming a tip (Figs. 1A,D,2A). The pronotum covers the mesothoraxlaterally where its sclerotized part gradu-ally becomes membranous and contains thestigma (not illustrated). Where the endoskel-etal prephragma extends into the body cav-ity, the posterior pronotal margin joins themesonotum (Fig. 2A). For comparison withadults, it should be emphasized that thenymphal pronotum is single-layeredthroughout, even though the integumentfolds in the lateral extensions and in theposterior tip, so that two layers come intoclose contact (Fig. 1E). Internally, the prono-tum is filled with hemolymph and fat bodycells that usually extend only into the basesof the ventral and dorsal processes (Figs.1D,E, 2C,E; see Table 1 for synonyms).Hence, these processes are single-layeredextensions of the pronotal integument as arethe suprahumeral buds (Fig. 1D). The exter-nal pronotal surface is covered with sensillatrichodea, each articulated in an elongatebase (Fig. 1B,C). Supraocular callosities arelocated on the external surface lateral to theventral processes (Fig. 1C,D). Prothoracicleg muscles originate on their interior side(Fig. 2D).

AdultsGross morphology of the prothorax

Female body size (ocular width) and prono-tum size (suprahumeral width) are largerthan in males (Table 2). In both sexes, prono-tum size correlates with body size, fitting apositively allometric power function (Fig. 3).Nevertheless, the shape and components ofthe prothoracic skeleton, including pronotalhistology, are the same in females and males.

Hence, the following observations apply toboth.

Adults have the same prothoracic scle-rites as nymphs: pronotum, episternum,epimeron, precoxal bridge, sternum, and tro-chantin (Fig. 4; see Table 3 for synonyms).Cervical sclerites were not found. The ster-num is small, rectangular, and fused to theepisternum by the precoxal bridge (Fig. 4C).No postcoxal bridge (postcoxale) was found.External pits in the sternum mark the ori-gin of the endoskeletal furca, whose lateralarms merge on each side with the pleuralapophyses (Fig. 4B,E). The area of fusionusually remains visible. The trochantin ar-ticulates freely with the coxa and the epister-num. A marked pleural sulcus separates thepleuron into the episternum and epimeron,and its dorsal end forms a pit on the outside(Fig. 4B,D), the base of the endoskeletalpleural apophysis.

The adult pronotum, however, is more com-plex than its nymphal form, because it iscomposed of two subunits: a proximal single-layered region, and a distal double-layeredregion. The proximal region is a single-layered integument wall (Fig. 5C) definedthrough its boundaries. Ventrally it extendsto the tergopleural boundary that has nophysical demarcation in adults, because thepropleuron fuses seamlessly with the prono-tum. Nevertheless, the tergopleural bound-ary can be estimated to extend from thepleural pit to the ventral edge of the (prono-tal) ventral lobe (Fig. 4D) (Stegmann, ’97),e.g., because the dorsal termination of thepleural sulcus is a general criterion for thetergopleural boundary in the pterygote pro-thorax (Parsons, ’67). The ventroanterior ter-mination of the single-layered part of thepronotum consists of the anterior pronotalmargin lined by the dorsal part of the cervi-cal membrane (Figs. 5C, 7F). This mem-brane does not contain cervical sclerites. Dor-soposteriorly, the single-layered pronotalregion terminates with the posterior marginof the pronotum that is lined by the interseg-mental membrane (Figs. 5C, 7F). Mesally,the posterior margin runs in immediate prox-imity to, and parallel with, the anterior pro-notal margin: in a median section throughthe proximal pronotum and adjacent areas,the posterior margin ends very close to theanterior margin, leaving only a narrowsingle-layered strip (Fig. 7F). Thus, the pre-phragma is close to the occiput (Fig. 7F).Laterally, the posterior margin bends ven-trally in a curve ending near the ventral

TABLE 1. List of prothoracic features previouslydescribed for nymphal Stictocephala bisonia

Terminologyused inthis work

Terminologyof previous

investigators Source

Dorsal and ven-tral processes

[Drawn in figs.10 and 11, pl.xxiv, but notnamed]

Funkhouser (’17)

Median dorsalspines

Quisenberry etal. (’78)

Suprahumeralbud

Pronotal hornbud, supra-humeral hornbud


Sensillatrichodea onelongatedbases

Chalazae, lateralscoli


Supraocular cal-losities

[Drawn, but notnamed]



edge of the ventral lobe (Fig. 5C). Within thecurve, the sclerotized pronotal canal joinsthe intersegmental membrane in a funnel-shaped zone (choanidium). A stigma is lo-cated within the posterior area of the inter-segmental membrane (Fig. 5C). From afrontal view (Fig. 4B), the single-layered re-gion of the pronotum contains the supraocu-

lar callosities and the mesal parts of thefossae. Muscles arise from the interior sur-face of the supraocular callosities (Fig. 7A),whose external surfaces are covered withlow naps 5–11 µm in diameter (Fig. 7B). Insitu, the eyes fit into the shallow caves of thefossae and the postgenae cover the anteriorpart of the episternum.

Fig. 2. Nymphs of Stictocephala bisonia. A: Diagram-matic representation of a median section through afifth-instar nymph showing the relations between protho-rax (white), head (dark pattern), and pterothorax andabdomen (light pattern). B: Sensillum trichodeum onthe pronotum (fifth instar). C: Sensillum trichodeum onthe dorsal process (fifth instar). D: Pronotal muscle

originating at the supraocular callosity (fifth instar).E: Frontal section (third instar) with the pronotal inte-rior filled with fat cells. D, dorsal; ba, base of sensillumtrichodeum; dp, dorsal process; e, eye; f, fat body cells;mu, pronotal muscle; p, pronotum; ph, pharynx; pr,prephragma; oe, esophagus; sg, salivary gland; soc, su-praocular callosity.

162 U.E. STEGMANN

Distad of the posterior pronotal marginthe pronotum is double-layered; i.e., it con-sists of two adjacent integumental walls(e.g., Fig. 6) forming a large, complexlybent plane (about 50 µm thick). Frontal(Fig. 4B) and ventral views (Fig. 4C) showthat the double-layered region forms thestrong suprahumeral horns. The median ca-rina runs in the median plane across thefrontal pronotum (metopidium, Fig. 4B). Pos-terior to the suprahumerals the dorsum istriangular in cross-section with the mediancarina as its dorsal edge and both the left

and right lateral carinae (Fig. 4C) as itsventral edges. Seen in median sections, thedouble-layered region of the pronotum risesdorsally over the head (Fig. 7F; metop-idium), bends posteriorly in a wide arch ex-tending as the posterior process, reflects andcontinues anteriad to end over the scutellum(Figs. 4E, 5A). The latter, reflected part(5septum sensu Buckton, ’03) is concealedby the dorsum and is seen en face only inventral view (Fig. 4C). More anteriorly, theseptum, with its lateral margins, separatesfrom the lateral carinae in a bow and its

TABLE 2. Sexual size dimorphism (mean 6 sd) in Strictocephala bisonia1

Females Males

Outer ocular width (mm) 3.39 6 0.102

(3.56; 3.1–3.5 [sic!])4 2.98 6 0.122

Suprahumeral width (mm) 5.78 6 0.323

(5.99; 5.45–6.4)4 4.83 6 0.353

n 51 61Regression of pronotum size (y) on body size (x) y 5 1.0457 3 x1.4012 y 5 0.8053 3 x1.6385

Regression coefficient 0.7286 0.8755

1Outer ocular width (a measure of body size) is greater in females than in males, as is suprahumeral width (a measure of pronotumsize). In both sexes, these two measures are strongly correlated, fitting an allometric power function. With a .1, the allometricrelationship is positive in both sexes. See also Fig. 3.2Unpaired t-test, t 5 19.9, P , 0.0001.3Unpaired t-test, t 5 15.0, P , 0.0001.4Kopp and Yonke (’77); n 5 20.

Fig. 3. Relation between pronotum size and body size in Stictocephala bisonia. In bothsexes, pronotum size increases with body size following a positively (a . 1) allometric powerfunction. See also Table 2.


anterior margin contacts the scutellum (Fig.4E). Laterally, the anterior margin of theseptum continues into the left and rightpronotal canals that run along the interior of

the dorsum and terminate in the choa-nidium (Figs. 4E, 5C). The pronotal canal isseen only from an internal (Figs. 4E, 5C) orventral view (Fig. 4C), because only the inte-

Fig. 4. Prothoracic skeleton of adults of Sticto-cephala bisonia, showing the prothoracic sclerites, theirendoskeletal characters, and the substructures of thepronotum. Bar 5 1 mm. A: Diagram of habitus (from aphotograph in Remane and Wachmann, ’93), pronotumblack. B: Frontal view (sclerites dotted, membranesstriped). C: Ventral view. D: Left side view. E: Left sideview 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, metop-idium; mc, median carina; pc, pronotal canal; pp, poste-rior process; s, sternum; sh, suprahumeral horn; sp,septum; soc, supraocular callosity; t, trochantin; vl, ven-tral lobe.

164 U.E. STEGMANN

rior integument is arched in a semicircle(Fig. 8B).

The pronotom attaches to the head andmesothorax through the cervical and inter-segmental membranes, respectively. Be-cause of the shape and large size of thepronotum, especially of its double-layeredpart, there are seven areas of secondarycontact between pronotum and nonpronotalbody parts: (1) fossae: postgenae (Fig. 4B,C);(2) metopidium: mesoscutum (Fig. 5A,B, ar-rowhead #1); (3) dorsum: mesoscutum (Fig.5B, arrowhead #2); (4) dorsum: lateral projec-tion of the scutellum (Fig. 5B, arrowhead#3); (5) septum: scutellum (Fig. 5A, arrow-head #4); (6) septum: abdomen (Fig. 5A,arrowhead #5); and (7) ventral lobe/humeralangles: mesepisternum/upper episternalhook (Fig. 7G).

Histology of the double-layered regionof the pronotum

The double-layered region of the prono-tum consists of two integumental walls lyingadjacent and parallel to each other withtheir cuticles locally fused to massive col-umns (Fig. 6). Between the two cuticles is alumen, an extension of the body cavity (Fig.5F). This general composition is seen notonly in cross sections (e.g., Fig. 6), but also inen face views of pronotum fragments (Fig.

7C,E), in which only the cellular compo-nents within the lumen are stained dark,while the cuticle layers remain transparent.Thus, seen along their longitudinal axis, col-umns, consisting of massive, transparent cu-ticle, appear as light circles (Figs. 7E, 8E).

In pronota of newly eclosed adults, theuntanned or slightly tanned external cuticleis approximately 4–8 µm thick, the internalcuticle approximately 1 µm (internal cuticle/integument 5 the cuticle/integument form-ing the posterior pronotal margin; externalcuticle/integument 5 the cuticle/integumentforming the anterior pronotal margin). Whentanning is completed the external cuticlethickens to 25–40 µm, the internal cuticle to3–8 µm, depending on where exactly mea-surements are taken. The columns in fullytanned individuals attain a diameter of40–70 µm in the metopidium, and about 20µm in the dorsum. Tanned cuticle stainslight brown/green with Azure II/Basic Fuch-sin and H&E, while untanned cuticle stainsred or pink. Large pits cover the externalsurface of the external cuticle and can beseen in the SEM (Fig. 7H) or as circles undera stereomicroscope (e.g., Fig. 4B). Each pitcorresponds to one column (Fig. 6). On theexternal surface of the internal cuticle eachcolumn produces a low cone about 12–20 µmin diameter (Figs. 6B, 7D, 7D insert). In

TABLE 3. List of prothoracic features previously described for adult Stictocephala bisonia

Terminology usedin this work

Terminology ofprevious investigators Source

Sternum Sternum Kramer (’50)Episternum Episternum Kramer (’50)Precoxal bridge Precoxa Kramer (’50)Furcal pits Furcal pits Kramer (’50)Furca Furcal apodemes Kramer (’50)Pleural apophyses Pleural apodemes Kramer (’50)Trochantin Trochantin Kramer (’50)Pleural sulcus Pleural suture Kramer (’50)Supraocular callosities Smooth impunctate areas above the eyes Funkhouser (’17)

Base of metopidium notched mediallyabove the vertex; Fig. 4

Kopp and Yonke (’77)

Suprahumeral horns Suprahumerals Branch (’13)Suprahumeral horns Funkhouser (’17)Pronotal horns Yothers (’34); Kramer (’50); Kopp and Yonke

(’77)Median carina Carina Branch (’13)

[Drawn but not named] Yothers (’34)Median carina Kopp and Yonke (’77)

Metopidium Metopidium Branch (’13); Funkhouser (’17); Kramer (’50);Kopp and Yonke (’77)

Dorsum Dorsum Branch (’13); Funkhouser (’17); Kramer (’50);Kopp and Yonke (’77)

Posterior process Posterior process Branch (’13); Funkhouser (’17); Kramer (’50)Apex Kopp and Yonke (’77)

Humeral angles Humeral angles Branch (’13); Kramer (’50)Upper episternal hook Upper episternal hook Kramer (’50)


sections stained with Methylene Blue/AzureII the most exterior layer of the externalcuticle stains brownish, while the main cu-ticular body stains blue. Where the columnis sectioned through its axis, it can be seenthat the brownish cuticle extends into thecone. The surface of the internal cuticle iscovered with tiny cuticular protuberances(Fig. 7D, insert).

As the cuticles thicken after molting thelumen becomes thinner (30–50 µm in newlyeclosed adults; #20 µm or less in fully tannedindividuals). The more dramatic effect of ageon the lumen, however, concerns its histol-ogy. Only in newly eclosed adults can epider-mal cells be distinguished from hemocytesand the (unstained) intercellular space(Fig. 6A).

Epidermal cells are characterized by theirsmooth cytoplasm, their oval, horizontal nu-

clei, their position along the internal surfaceof the internal and external cuticles, andtheir extensions that may run obliquely orstraight across the entire lumen (Figs. 6A,8G,L). Extensions of both epidermal layersseem to intertwine, implying the breakdownof the basal lamina; however, epidermal ex-tensions do not occur in areas in which thetwo integumental layers are farther apart,e.g., along the median carina (Fig. 7F) or thepronotal canal (Fig. 8B).

Hemocytes are usually located in themiddle of the lumen (Figs. 6A, 8L), oftenelongated horizontally, and situated alongtracheae or nerves (if present; Fig. 8G). Theyusually occur as single cells, lack the exten-sions across the lumen, and have round nu-clei (Fig. 8L). Their cytoplasm containsdensely packed granules that stain in thesame colors as epidermal granules, albeit

Fig. 5. Prothoracic skeleton of adults of Sticto-cephala bisonia. A: Diagram of median section througha female showing the relations between prothorax(white), head (dark pattern), and pterothorax and abdo-men (light pattern). Arrowheads, secondary contactzones. B: Diagram of oblique-horizontal section showingthe relation between mesothorax (light pattern) andproximal pronotum (double line). Arrowheads, second-ary contact zones. C: Diagram of the right half of theproximal prothorax showing the single-layered, proxi-mal region of the pronotum as it relates to the double-layered, distal region in dorsomedioposterior view;sclerites transparent, membranes black. a, pleural

apophysis; aes, anterior part of the episternum; b, pre-coxal bridge; c, coxa; ch, choanidium; cm, cervical mem-brane; d, dorsum; ec, external cuticle; em, epimeron; fo,fossa; fu, furca; h, head; ic, internal cuticle; im, interseg-mental membrane; m, metopidium; pc, pronotal canal;pp, posterior process; pop, postphragma; pr, prephragma;s, sternum; sh, suprahumeral horn; sl, mesoscutel-lum; sp, septum; sti, stigma; su, mesoscutum; t, trochan-tin; ueh, upper episternal hook; vl, ventral lobe; 1–5,areas of secondary contact between the pronotum andother body parts: 1, metopidium/mesoscutum; 2, dorsum/mesoscutum; 3, dorsum/lateral scutellum; 4, septum/scutellum; 5, septum/abdomen.

166 U.E. STEGMANN

more intensively, especially in H&E andHeidenhain’s stains (Fig. 8A). These gran-ules 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 themedian carina where a few cells enter fromthe large fat body that fills the mid-sagittal,dorsal region of the head, pro-, and mesotho-rax (Fig. 7F). Fat cells can be distinguishedfrom hemocytes by their position and type ofgranules. While hemocytes usually occur assingle cells and occasionally in strands, fatbody cells form clumps containing many,roundly shaped, large cells (Fig. 8A). Lipid-fixed fat body cells (Fig. 7A,F) show a greatvariety of small to large vesicles that mayalso differ in color. For example (Azure II/Basic Fuchsin; Spurr), within one cell, thelargest vesicles stain olive green, smallvesicles remain transparent, while othersstain blue, purple, and pink. Presumably,only the large green vesicles contain a largeportion of lipids, because in non-lipid-fixedmaterial large areas of the fat body cells aredepleted, 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 theirboundaries (Fig. 8F,O); (3) nuclei (Fig. 6B);and (4) dendrites within columnar canals(Fig. 8F). Neither cell bodies nor intercellu-lar space can be found.

The cellular components described belowoccur in the lumen of both teneral and oldadults. Tracheae are easily recognized bytheir taenidia and by being unstained inter-nally (Fig. 8C). Apparently, tracheae enterthe double-layered pronotum through thepronotal canal (Fig. 8B) and other areas ofthe metopidium and dorsum, but not throughthe median carina. No attempt was made totrace their branching patterns. Nervebundles are recognized by horizontal fibersin cross sections (Fig. 8G). Individual nervesentering the double-layered pronotumthrough the pronotal canal (Fig. 8B) orthrough the metopidium were traced back tothe prothoracic ganglion, using serial sec-tions and gross dissections. The prothoracicganglion is fused to the mesothoracic gan-glion but can be distinguished in micro-scopic sections by its neuropil. No nerve wasfound within the median carina. The dorsalvessel extends through the mesothorax intothe prothorax, ending near the pharynx/esophagus transition (Fig. 7F), but no acces-sory pulsatile organs were found.

Fig. 6. Sections through the dorsum of Stictocephalabisonia. A: The pronotal lobe of newly eclosed adultsshowing the two, still thin cuticular layers comprisingthe 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 showinga 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, internalcuticle; nu, nucleus.


Figure 7

168 U.E. STEGMANN

Sensilla trichodea articulate in the centerof the pits on the external cuticle (Figs.7E,H, 8E,F). A columnar canal runs throughthe column to the base of the seta (e.g., Fig.8E) containing the dendrite(s) (Fig. 8F), butcell bodies could not be localized. Type Asetae (Figs. 7H, 8E) are shorter and thinner(approximately 25–40 µm long, n 5 24; ap-proximately 1 µm diameter, n 5 10) thantype B setae (approximately 65–80 µm long,n 5 29; approximately 3.5 µm diameter,n 5 6) (Figs. 7H, 8F). At least the setae ofB-sensilla are hollow (Fig. 8F), but no cuticu-lar openings on the setal surface were found.The density of sensilla trichodea is greaterin males than in females, irrespective of thepronotum region examined (Table 4). Bothmales and females have a greater density onthe metopidium than on the dorsum (Table4). Sensilla campaniformia occur in low den-sities on the external surface of the metop-idial and dorsal external cuticle. The apicaldome appears as a circle in an en face view(Fig. 8D), but can also be seen in cross sec-tions through untanned (Fig. 8H) and fullytanned cuticle (Fig. 8O). A canal through thecuticle (approximately 6 µm wide) leads thedendrite(s) (Fig. 8O). Sensilla coeloconica(Fig. 8K,N) were only found in the fossae.

In metopidial and dorsal en face frag-ments, light circular structures of approxi-mately 8–10 µm in diameter occur in thefocal plane of the lumen with a canal termi-nating on the surface (Fig. 8I). These open-ings are the small pores (diameter approxi-mately 3 µm) seen in the SEM (Figs. 7H, 8J).The canals through the external cuticle aredistinguished from those of sensilla campani-formia in that they consist of an approxi-mately 5 µm wide basal part, an approxi-mately 1 µm wide apical part (Fig. 8I,M),and an approximately 4 µm wide sphere justbelow the external opening (Fig. 8L,M).

DISCUSSIONProthoracic sclerites of last-instar nymphs

and adultsLast-instar nymphs and adults of Sticto-

cephala bisonia share the same prothoracicsclerites (pronotum, epimeron, episternum,sternum, prexocale, and trochantin) and en-doskeletal features (pleural apophysis andfurca). However, in adults the lateral furcalarm on each body side is fused with thepleural apophysis, while in nymphs it is not.With the exception of the epimeron, thesesclerites and their endoskeletal componentswere already recognized in adults of S. biso-nia by Kramer (’50) and his findings werelater confirmed (Hasenoehrl and Cook, ’65;Table 3). As in those studies, no cervicalsclerites and no postcoxal bridge were foundin the present study.

The first report on the various prothoracicsclerites of (generalized) adult membracidswas from Funkhouser (’17), who acknowl-edged the pronotum, episternum, epimeron,trochantin, and sternum. He did not de-scribe endoskeletal structures. The prono-tum, episternum, sternum, precoxale, tro-chantin, pleural apophysis, and furca werealso found in adult Oxyrhachinae (Has-

TABLE 4. Density of sensilla trichodea per 0.2 mm2

(mean 6 sd) 1

Females Males

Metopidium 27 6 32,3 33 6 42,4

Dorsum 17 6 23,5 22 6 34,5

n 17 15

1In both males and females, the density of sensilla trichodea isgreater on their metopidium than on their dorsum. Males, how-ever, have more sensilla per area than do females both on themetopidium and on the dorsum.2Unpaired t-test, t 5 4.7, P , 0.0001.3Paired t-test, t 5 12.4, P , 0.0001.4Paired t-test, t 5 10.6, P , 0.0001.5Unpaired t-test, t 5 6.2, P , 0.0001.

Fig. 7. Prothorax of adult Stictocephala bisonia.A: Sagittal section through the supraocular callosityand the origin of prothoracic muscles. B: En face view ofthe supraocular callosity with its naps. Scanning elec-tron micrograph (SEM). C: En face view of the septumdemonstrating its composition of two cuticular layers(unstained 5 transparent) that comprise a lumen of cel-lular nature (dark). D: Outer surface of internal, meto-pidial cuticle covered with columnar projections (arrow-head and insert) that each corresponds to one column.SEM. E: En face view of metopidium demonstrating itscomposition of two cuticular layers (unstained 5 trans-parent) that comprise a lumen of cellular nature (dark);columns remain transparent because they consist ofmassive cuticle. F: Mid-sagittal section through theproximal metopidium and adjacent areas demonstrat-ing the double-layered nature of the pronotal lobe andthe connection between its lumen and the body cavity;note the prephragma near the occiput. G: Lower base ofleft forewing showing sensilla trichodea (arrowhead)that may touch the humeral angle. SEM. H: Outersurface 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 thepronotum; cc, columnar canal; cm, cervical membrane;col, column; dv, dorsal vessel; ec, external cuticle; f, fatbody cells; h, humeral angle; ic, internal cuticle; im,intersegmental membrane; m, metopidium; mc, mediancarina; mu, pronotal muscle; n, nap; oe, esophagus; ot,occiput; pm, posterior margin of the pronotum; pr, pre-phragma; sg, salivary gland; st, sensilla trichodea; su,mesoscutum; ueh, upper episternal hook.


Figure 8

enoehrl and Cook, ’65) and Centrotinae(Ahmad and Afzal, ’78; Ahmad and Khan,’79). Hence, the composition of the pleuronremains the only controversial issue withrespect to the number of sclerites of themembracid prothorax (Stegmann, ’97).

The pronotum is a ‘‘spine’’ in nymphs. . .A basic difference between pronotal

anatomy of adults and nymphs of Sticto-cephala bisonia was found in this study: theinterior of pronotal substructures, e.g., su-prahumerals/suprahumeral buds, communi-cates with the body cavity in nymphs but isair-filled in adults.

A single-layered outgrowth of the integu-ment communicating with the body cavity istermed ‘‘Dorn’’ (Weber, ’33) or ‘‘spine’’(Snodgrass, ’35). Thus, in Stictocephala biso-nia, not only the nymphal pronotal substruc-tures are ‘‘spines,’’ but the entire nymphalpronotum is a large ‘‘spine.’’ This result maywell be generalized to the homologousnymphal pronota of the Membracidae, be-cause, in Tricentrus albomaculatus, Ker-shaw (’13) found that the ‘‘tegumentarybristles of the nymph are hollow and commu-nicate with the body cavity.’’ Judging fromhis diagram (fig. 1, Kershaw, ’13), he re-

ferred to the elongated bases of sensilla, butalso to tergal substructures such as the dor-sal processes.

Except for Kershaw’s (’13) findings, thenymphal pronotum and its substructureswere known only with respect to externalmorphology. Pronotal processes were re-ported from Stictocephala bisonia (Funk-houser, ’17; Quisenberry et al., ’78; see Ta-ble 1) and other membracids (e.g., Stoll, 1788;Syn.: ‘‘tuberosities’’: Yothers, ’34). Supra-humeral buds occur in several New Worldgenera (Quisenberry et al., ’78), in manyOxyrhachinae (Capener, ’62), and in manyCentrotinae (Capener, ’68). Published fig-ures show setae (as ‘‘chalazae’’ and ‘‘scoli’’)on the nymphal pronotum of S. bisonia andother New World genera (Quisenberry et al.,’78), but also on the pronotum of severalCentrotinae species (Capener, ’68). Thesesetae are presumably sensilla trichodea.Nymphal supraocular callosities were la-beled 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 Centrotinaespecies (Capener, ’68).

. . . but a ‘‘posterior reduplicationof the notum’’ in adults

Except for the proximal single-layered re-gion, the pronotum of adult Stictocephalabisonia is a plate arched in itself far beyondthe body outline, covering the pterothoraxand abdomen and forming extensions (e.g.,suprahumeral horns) that are hollow in thesense that their interior does not communi-cate with the body cavity, but with the air;the pronotal plate is composed of two integu-mental layers connected through cuticularcolumns comprising a lumen that communi-cates with the body cavity. Therefore, whatappear to be the lateral pronotal margins,i.e., the lateral carinae, are blind endings ofthe pronotal plate, not the true terminationsof the sclerite (which are lined, per defini-tionem, by membranes). In short, the distalregion of the adult pronotum is a doublelayer or lobe—an exceptionally large ‘‘poste-rior reduplication of the notum’’ sensuSnodgrass (‘‘the posterior edge of the notumfolded downward and forward upon itself,leaving a free margin overlapping succeed-ing parts’’; Snodgrass, ’09).

In Stictocephala bisonia, the plate aspectmight be inferred from Branch’s (’13) re-mark that the dorsum forms a ‘‘tectiformhood’’ and from drawings by Kramer (fig. 72,

Fig. 8. Prothorax of adult Stictocephala bisonia.A: Frontal section through left choanidium showing theconnection between hemocytes and fat cells. B: Frontalsection through left pronotal canal with nerves andtracheae. C: Trachea in the metopidium of a newlyeclosed female. D: Apical dome (arrowhead) of a sensil-lum campaniformia in the metopidium, en face view.E: Cuticular column with a B-type sensillum tricho-deum (arrowhead) and its columnar canal. F: A-typesensillum trichodeum (arrowhead) in a pronotal pit withdendrite inside the columnar canal; a small part ofcuticle accidentally broke off. G: Dorsum of a newlyeclosed adult showing the intercellular space with epider-mal feet, hemocytes and a nerve. H: Sensillum campani-formia in the metopidium (arrowhead on apical dome) ofa newly eclosed adult. I: En face view of dermal glandwith opening on the exterior cuticle (arrowhead), thecanal through the external cuticle, and, toward the left,a basal area (dark area with light circle inside). J: Open-ing of dermal gland on the exterior cuticle. SEM. K: Sen-sillum coeloconicum in the fossa. SEM. L: Cross sectionthrough suprahumeral horn with opening of dermalgland (arrowhead). M: Cross section through a maturedmetopidium showing a cuticular canal with its openingon the external cuticle (arrowhead). N: Sensillum coelo-conicum in the fossa showing its apical area surroundedby the external cuticle. O: Sensillum campaniformia inthe metopidium (arrowhead on apical dome) of a ma-tured 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.


pl. ix and fig. 106, pl. xii, Kramer, ’50). On agreater taxonomic scale, the plate aspectwas the first insight into pronotal anatomyof adult membracids (Buckton, ’03; Branch,’13; Funkhouser, ’17; Marcus, ’50; Kopp andYonke, ’72; Strumpel, ’72). For example,Buckton (’03) wrote that ‘‘the remarkablespines of these insects have no bulbous ori-gin, but are hollow tubes rising directly fromthe surface’’ and are ‘‘filled with air.’’

Whether this pronotal plate is single-layered (massive cuticle) or double-layered(lobe) remained controversial. A massive cu-ticle could be inferred from drawings ofStictocephala bisonia (fig. 72, pl. ix and fig.106, pl. xii, Kramer, ’50), Entylia bactriana(fig. 1, Kopp and Yonke, ’72), and a general-ized membracid (fig. 36, Strumpel, ’72). Butstudies focusing on the composition of theplate always revealed living tissue. Nervesand tracheae were reported from Aethalionsp., Aconophora sp., Alchisme sp. (Marcus,’50), and linear structures (‘‘venas’’) associ-ated with stigmata were described inMembracis spp., Lycoderes spp., Stegaspissp., Oeda inflata, and Gelastogonia sp. (Rich-ter, ’54). Eventually, Wood (’75b) found that‘‘a matrix of cells between two cuticular lay-ers characterize the wall of the expandedpronotum’’ of Umbonia crassicornis.

The location of the posterior pronotal mar-gin, the course of the intersegmental mem-brane, and the presence of a proximal, single-layered pronotal area were not previouslyreported in the Membracidae. This led toconsiderable confusion as reflected, e.g., byKramer’s (’50) misinterpretation of the pos-terior pronotal margin in Stictocephala biso-nia as a ‘‘muscle partition formed by [the]apodemal wall of [the] pronotum’’ (mp—fig.106, pl. xii). Also, it was difficult to under-stand why and exactly which part of thepronotum is detachable in Anchistrotus spp.and why this apparently does not harmthe insect (e.g., Boulard, ’83, Strumpel, ’83,Rietschel, ’87). It seems that if the grossmorphological (pronotal plate) and histologi-cal aspects (double layer) had been consid-ered together, the conspicuous part of themembracid pronotum would have been im-mediately recognized as the posterior redu-plication of the pronotum.

In this study, internal and external cuticleof the lobe were found to be fused to columnswith each column associated with an exter-nal pit. Both also occur in beetle elytra thatrepresent another type of lobe (e.g., Weber,

’33; Reuter, ’36; Krzelj, ’69). External pitswere reported by earlier workers in Sticto-cephala bisonia (‘‘punctured,’’ Branch, ’13;‘‘punctate,’’ Funkhouser, ’17; ‘‘impuncta-tions’’ Kramer, ’50) and other membracids(Fabricius, 1803; Kirby, 1829; Buckton, ’03).Columns were never explicitly described inthe Membracidae; however, a close look atsome studies suggests their presence in manyspecies. Buckton’s (’03) ‘‘shallow depressionsor punctures’’ appeared as ‘‘bright dots whensuitably placed’’ and could easily be inter-preted as columns, because this is the waythey appear in en face views (of S. bisonia).For the same reason Marcus’ (’50) ‘‘cercosredondos’’ in the pronota of Aethalion sp.,Aconophora sp., and Alchisme sp. could beinterpreted as columns, especially becausethey correspond to external pits (‘‘hoyue-los’’), at least in the proximal area of thepronotum. A SEM study showed pronotalpits in 100 species from six membracid sub-families (Wood and Morris, ’74). If pronotalpits are indeed associated with columns, col-umns are common to the Membracidae andAetalionidae.

From spine to lobe: morphogeneticimplications

When Latreille (1802) noted that ‘‘La larvedu membrace du genet differe peu de l’insecteparfait’’ he was the first to indicate strongsimilarities between nymphs and adults inrespect to the externally visible substruc-tures of the pronotum. Prominent examplesare the dorsal spine in Umbonia crassicornis(Pelaez, ’40, ’41) and the dorsal bulb inAnchistrotus amitteraglobus (Boulard, ’83).Such pronotal substructures were generallyinterpreted as adult primordia, e.g.,Funkhouser’s (’17) ‘‘vestigial lateral horns’’(5suprahumeral buds) in the Ceresini. Con-sequently, postembryonic pronotal develop-ment was regarded as a progressive, molt-to-molt enlargement (e.g., Funkhouser, ’17;Strumpel, ’72), suggesting shifts in body pro-portions but minor morphological change.But occasionally, even the external pronotaldevelopment seemed to exceed paurometabo-lism (Muller, ’84).

If pronotal substructures of membracidnymphs are indeed ‘‘spines,’’ e.g., supra-humeral buds, then they are anatomicallydistinguished from adult features of similarappearance, e.g., suprahumeral horns, thatare parts of the pronotal ‘‘reduplication.’’Therefore, nymphal substructures are notearly (small) stages of adult substructures.

172 U.E. STEGMANN

Rather, they may be regarded as sheathsinside of which the adult substructures de-velop, necessarily taking the approximateshape of adult processes. I hypothesize thatthe primordium of the adult pronotum devel-ops only within last-instar nymphs, i.e., be-tween apolysis and adult ecdysis, becauseotherwise an imaginal disc (non-cuticle-producing epidermis) must be assumed,which is known only from Holometabola.

Occasional reports of postecdysial ex-pansion of the pronotum (Richter, ’54;Suchantke, ’76; personal observation in labo-ratory colonies of Stictocephala bisonia) pro-vide circumstantial evidence for (1) the exis-tence of a unique adult primordium withinthe pronotum of last-instar nymphs and for(2) the hypothesis that due to limited spacewithin the nymphal sheath the adult primor-dia unfold completely only after ecdysis.Membracid last-instar nymphs fasten them-selves to the underside of a leaf or twigbefore ecdysis (e.g., Funkhouser, ’17; per-sonal observation in S. bisonia). Hangingupside down, adults may help to expand thepronotal lobe as they do with their wings.

Another line of evidence for a separateadult primordium in Stictocephala bisoniaand its expansion after adult ecdysis comesfrom histological parallels between postec-dysial development (1) of insect wings and(2) that of the pronotal lobe of S. bisonia.These parallels concern the occurrence ofepidermal feet and hemocytes, the pre-sumed lack of a basement membrane, thedissolution of cell membranes, and the disap-pearance of intercellular space with age.

Pronotal lobes of newly eclosed Sticto-cephala bisonia exhibit epidermal feet con-necting the two integumental layers, therebyleaving ample space in between for hemo-lymph. Epidermal feet (Locke and Huie, ’81)seem to intertwine in S. bisonia, becauseextensions of both epidermal layers may forma single strand on a light microscopical level.Such epidermal feet are known from thedevelopment of other lobes, such as wings(e.g., Rehberg, 1886; Weber, ’33; Chapman,’82; Nardi and Magee-Adams, ’86) and anten-nal primordia (e.g., Keil and Steiner, ’90).Intertwining of epidermal feet without theoccurrence of a membranous middle layerimplies breakdown of the basement mem-brane, which was observed in the develop-ment of wings (e.g., Weber, ’33; Chapman,’82; Nardi and Magee-Adams, ’86), and an-tennae (e.g., Steiner and Keil, ’93).

Hemocytes are regularly found in doublelayers like wings (e.g., Reuter, ’36; Zeller,’38; Nardi and Magee-Adams, ’86) and anten-nal primordia (Keil and Steiner, ’90; Steinerand Keil, ’93), where they are involved in theformation (Nardi and Miklasz, ’89) andbreakdown of the basement membrane(Nardi and Miklasz, ’89; Steiner and Keil,’93). ‘‘Hemocyte’’ is used here in the widestsense, meaning ‘‘the loose cells in the bodycavity of insects’’ (Wigglesworth, ’65). Thisdefinition incorporates the fact that oftenthere is no sharp distinction between free-floating fat cells and hemocytes sensu stricto(Wigglesworth, ’65; Chapman, ’82). A similarsituation is suggested for Stictocephala biso-nia, because (1) the dominance of nonlipidgranules clearly separates the hemocytes inthe pronotal lobe from fat body cells, but (2)the hemocytes are linked to the fat body, and(3) are unusually large. Whatever the gen-esis of these hemocytes in S. bisonia, theparallels to the loose cells in wings are obvi-ous: the granules, the position in the middleof the lumen and between the epidermalfeet, and the presumed mechanism of enter-ing into the lumen by blood pressure duringinflation.

In the fully sclerotized pronotal lobe ofStictocephala bisonia, the intercellular spaceoccurring in teneral adults has disappeared.Whether cell membranes dissolve or stillexist in the sclerotized lobe, albeit not vis-ible on a light microscopic level, remains anopen question. In postecdysial insect wings,the intercellular space disappears (e.g.,Weber, ’33; Zeller, ’38), cells fuse after disso-lution of the basement membrane and thelumen either becomes a syncytium or is com-pletely reduced (e.g., Weber, ’33).

Gross morphological featuresof the adult pronotum

The general, external shape of the adultpronotum of Stictocephala bisonia was oftenportrayed illustrating features such as themetopidium, the dorsum, the suprahumeralhorns, the humeral angles, and the posteriorprocess (Marlatt, 1894; Buckton, ’03; Branch,’13; Funkhouser, ’17; Yothers, ’34; Poisson,’37; Kramer, ’50; Kopp and Yonke, ’77; for thefollowing, see Table 3). The fossae were notpreviously described or illustrated for S. biso-nia but were reported from several otherspecies (Branch, ’13; Funkhouser, ’17; drawnin: Richter, ’54; Wood, ’75b;Ahmad and Khan,’79). Supraocular callosities in adults werenoticed early in S. bisonia (Funkhouser, ’17;


Poisson, ’37; Kopp and Yonke, ’77) and manyother genera (e.g., Fowler, 1894; Buckton,’03; Funkhouser, ’17; Capener, ’62; Capener,’68). Capener (’62) remarked that ‘‘their func-tion is unknown,’’ but in Anchistrotus spp.Boulard (’83) noted that muscles of the fore-legs originate at the callosities, as was alsofound in S. bisonia. Kramer (’50) describedthe musculature of S. bisonia but neithermentioned nor depicted the callosities. Atthis point it is uncertain whether muscleorigins are confined to the callosities.

The septum was never described in Sticto-cephala bisonia, but its external traces canbe found in figures of S. bisonia (Kopp andYonke, ’77) and of S. diceros (as Ceresa dice-ros) (Branch, ’13). It was first recognized byBuckton (’03) in Hemiptycha punctata, and asimilar structure was located in Anchis-trotus sp. (‘‘Unterseite des Pronotums’’:Rietschel, ’87). Possibly, the septum occursin many treehopper species but was over-looked as in S. bisonia. Other internal sub-structures are the pronotal canals contain-ing nerves and tracheae. Similar features,two pairs of internal ridges containing tra-cheae, were mentioned in Umbonia crassicor-nis (Wood, ’75b).Although some type of acces-sory pulsatile organs (e.g., Krenn and Pass,’94) may be expected in the membracid pro-notum, no membranous canals or layers werefound within the pronotal canal and themedian carina of S. bisonia. Nevertheless, amore detailed future investigation may re-veal them, possibly in the lateral areas.

As described for Stictocephala bisonia(Kramer, ’50) and a generalized membracid(Funkhouser, ’17) the prothoracic stigma islocated in the intersegmental membrane justanterior to the mesepisternum, a commonposition in insects (Weber, ’33; Snodgrass,’35). Connections from the stigma to themeso- and prothoracic tracheae were foundin S. bisonia, but not in Umbonia crassicor-nis, where an ‘‘external opening’’ in or nearthe lateral part of the fossa was interpretedas the opening of prothoracic tracheae (Wood,’75b). In S. bisonia, a similar pit representsthe external base of the pleural apophysis.Richter (’53) mentioned proximolateral stig-mata in several genera. However, their ex-act position remains obscure, despite laterdrawings (Richter, ’54).

Richter (’53) interpreted the distal prono-tum as being transformed prothoracic wingsfused along their costal margins to form themedian carina. He described ‘‘venas’’ and

pronotal areas (e.g., ‘‘parte dorsal,’’ ‘‘mem-brana basal’’) that supposedly correspond towing veins and wing areas, respectively, butcannot be located despite later figures (e.g.,figs. 7–10; Richter, ’54). He further assumedthat the distal pronotal plate was fixed tothe proximate pronotum by muscles, butseems to have confused the mesonotum withthe pronotum (Boulard, ’73), because he de-picted propleural characters (‘‘ondulacionesy dilataciones pleurales’’) on the lateral partof the mesonotum (fig. 7, Richter, ’54). Bou-lard’s (’73) arguments against Richter’s hy-pothesis still hold: median carinae occur inmany insects, the only muscles found arethose inserting on the occiput and anteriorlegs, and in nymphs there are no indicationsfor paired buds.

Cuticular canals and sensillaof the pronotal lobe

Because of their abundance and wide dis-tribution, cuticular canals in the externalcuticle of the metopidium and dorsum ofStictocephala bisonia are most easily inter-preted as ductules of exocrine glands, specifi-cally of class 3 gland cells (Noirot andQuennedey, ’74). Apart from the light circlesin en face views, no indications for corre-sponding cell bodies were identified, though.

In the pronotum of Umbonia crassicornis,two of three cell types (‘‘large cuboidal cells’’and ‘‘squamous epithelial cells with elongatenuclei’’) were regarded as ‘‘probable secre-tory and/or neurosecretory cells’’ on the ba-sis of similarities in staining properties toneurosecretory cells in a brain (Wood, ’75b).This interpretation is questionable, though,because neither the brain nor the similari-ties were detailed, and an unspecific stain(H&E) was used to demonstrate similari-ties. These difficulties also weaken the hy-pothesis that, because pronotal pits are sur-rounded by those cells ‘‘the pits function aschemoreceptors or perhaps as dispersal sitesfor pheromones’’ (Wood, ’75b). In S. bisonia,pronotal pits are not chemoreceptors andthere are no indications that pheromonesdiffuse through the cuticle of pits whosebases are massive, cuticular columns. Assuggested by circumstantial evidence (seeabove), other species are likely to share thesefeatures of S. bisonia.

Setae were noticed early in Stictocephalabisonia (Funkhouser, ’17) and many othermembracids (e.g., Fairmaire, 1846; Fowler,1894; Buckton, ’03; Branch, ’13; Funkhouser,’17; Capener, ’62; ’68). Marcus (’50) first real-

174 U.E. STEGMANN

ized their morphology to be that of sensillatrichodea (‘‘cerda tactil’’) and documentedtheir innervation in three genera. Pronotalsensilla trichodea in Umbonia crassicornisare innervated, as well (Wood, ’75b). Sen-silla campaniformia were not previously de-scribed in the Membracidae and sensilla coe-loconica were only found on abdominaltergites (Dietrich, ’89).

Males of Stictocephala bisonia havegreater sensilla trichodea densities than fe-males. However, in absolute terms maleshave fewer sensilla than females, becausecomparing the factor of density increase (‘‘D’’)with the squared factor of pronotal size de-crease (i.e., the correction term, ‘‘P’’) givesD , P2 both for the metopidium [1.223 ,(1.197)2] and for the dorsum [1.295 ,(1.197)2] (data from Table 4); if absolutesensilla numbers were equal between thesexes, the expected relation was D 5 P2. Itcannot be decided at this point whether theobserved differences represent sex-specificfunctions or males achieve the same func-tions as females with increased sensilla den-sity, tolerating fewer sensilla in absoluteterms.

Biological functions of the pronotal lobeFrom the various adaptive (e.g., Kirby,

1829; Poulton, ’03; Wood, ’93) and nonadap-tive explanations for pronotal enlargements(e.g., Funkhouser, ’21; Strumpel, ’72; Bou-lard, ’73), only the mechanical defence andaposemantic coloration hypotheses weretested. In captivity studies, mature Umbo-nia crassicornis were protected from beingswallowed by a natural predator (Anolis)mainly due to their acute dorsal horns (Wood,’75a, ’77). However, pronota of eight otherspecies were not mechanically protective(Wood, ’75a). The conspicuously colored, ten-eral adults of U. crassicornis and Platycotisvittata are unpalatable to Anolis and Anolislearns to avoid this prey, suggesting anaposemantic role of the pronotum (Wood,’75a). However, at least in U. crassicornispronotal coloration did not promote learningto avoid adults (Wood, ’77). Possibly, Anolisinstead recognizes pronotal shape (Wood,’77). It is likely, but has not been tested, thatthe pronotum itself contributes to unpalat-ibility.

A group of adaptive hypotheses refers topronotal physiology and a critical evaluationof facts and arguments is appropriate. Ac-cordingly, pronotal enlargement is due toselection on the pronotum for increasing sur-

face area, because this would either (i) in-crease ‘‘the amount of directional sensoryinput’’ (Wood and Morris, ’74; Wood, ’93) or(ii) ‘‘facilitate dispersal of volatiles’’ (Wood,’93). Various sensory functions were pro-posed (Marcus, ’50; Wood, ’75b, ’93), e.g.,‘‘the detection of odor, air currents, or air-borne sound’’ (Wood and Morris, ’74). Thesefunctions could mediate intraspecific commu-nication (Wood, ’75b), e.g., when males touchthe female’s pronotum during precopulatorybehavior (Wood, ’93).

In a narrow sense, these hypotheses poten-tially could explain pronotal size, but notshape (Strumpel, ’83), because the same sur-face area may be achieved by many shapes.However, additional hypotheses on howshape affects perception or pheromone dis-persal could be proposed. Although it is truethat the pronotal lobe is a living tissue andmost probably its components have specialfunctions, it is not self-evident to postulateany of these functions as one or the mainadaptive reasons for past or current evolu-tion of the lobe. Reversing the argument isjust as plausible. Sensilla may occur, be-cause sensory input from an already largeand exposed sclerite is no less vital than it isfrom other sclerites. Similarly, pheromonalglands may occur in the pronotum simplybecause it is more exposed than many othersclerites. Thus, physiological functions, bythemselves, neither exclude (other) adaptivehypotheses of pronotal evolution nor non-adaptive explanations such as correlated re-sponse to increasing body size (e.g.,Strumpel, ’72; Boulard, ’73).

While sensilla occur in many species, sofar there is no evidence for pheromone glandswithin the pronotal lobe, a prerequisite forthe pheromone dispersal hypothesis. Cellsfound in the pronotum of Umbonia crassicor-nis (Wood, ’75b) are not necessarily glandcells (see above), and if they are, they mightnot produce pheromones. As dermal glandsthey may well be involved in cuticle forma-tion (Chapman, ’82). Moreover, there is noevidence for pheromones as a regular meansof communication between living individu-als or as a means of defence. Sex phero-mones are not known in membracids (Wood,’93) and alarm pheromones were releasedonly after deadly ruptures of the body wall(Nault et al., ’74; Wood, ’76). Finally, intra-specific communication, a central target ofsurface hypotheses, was shown to be medi-ated by vibrational signals (Strubing, ’92;


Hunt, ’93; Cocroft, ’96). It is likely, but un-known, whether other sensory modes areinvolved (e.g., Hunt, ’93).

In summary, while the mechanical de-fence hypothesis was supported in one spe-cies, the aposemantic coloration hypothesiswas not and whether the physiological func-tions of the pronotal lobe are (part of) itsadaptive causes is just as likely. Conclusionsat the highest explanatory level, i.e., adap-tive versus nonadaptive hypotheses, couldbe drawn from tests of nonadaptive hypoth-eses, for example, by deriving and testingcentral predictions such as genetic correla-tions.

ACKNOWLEDGMENTS

I am deeply indebted to Dietrich Mossa-kowski, Harald Witte, and Gundula Sieber(Bremen) for advice and equipment and toHildegard Strubing (Berlin) for donatingher colony of Stictocephala bisonia. Manyothers helped in various ways: B. Ehmer,C. Gehrig, W. Gronenberg, G. Hartwig, A.Hoh, H. Karsten-Wohltmann, C. Klein-eidam, G. Krohne, G. Kruger, K.E. Linsen-mair, H. Meyer, M. Obermayer, S. Oster-kamp, G. Roth, K. Schauz, H.-B. Schikora,H. Strumpel, A. Toltz, W. Vogel, J. Warner,and A. Wohltmann. I am very grateful toLewis L. Deitz, Wulfila Gronenberg, Freder-ick W. Harrison, Frank-Thorsten Krell, Tho-mas K. Wood, and two anonymous refereesfor reading and commenting on the manu-script. This study was supported by the Stu-dienstiftung des deutschen Volkes.

This work is dedicated to Dr. Rupert Wild(Staatliches Museum fur Naturkunde Stutt-gart, Germany) for a long period of sensibleencouragement.

LITERATURE CITED

Ahmad, I., and M. Afzal (1978) Thoracic sclerites andsutures of Oxyrhachis taranda (Fabr.) (Homoptera:Membracidae). Pakistan J. Zool. 10:91–94.

Ahmad, I., and N.A. Khan (1979) Studies on the thoracicsclerites and sutures of Leptobelus gazella (Fairm.)and Hypsauchenia subfusca Buckton (Homoptera:Membracidae: Centrotinae), with notes on their sys-tematic positions. Pakistan J. Zool. 11:273–279.

Amyot, C.J.B., and J.G.A. Serville (1843) Histoire Na-turelle des Insectes. Hemipteres. Paris: Librairie En-cyclopedique de Roret.

Boulard, M. (1973) Le pronotum des Membracides: cam-ouflage selectionne ou orthogenese hypertelique? Bull.Mus. Nat. Hist. Nat. 83:145–165.

Boulard, M. (1983) Sur deux Anchistrotus et la mutila-tion naturelle du pronotum chez les Membracides dece genre. Bull. Soc. Entomol. France. 88:274–283.

Branch, H. (1913) Morphology and Biology of the Mem-bracidae of Kansas. Kansas Univ. Bull. 8:75–115, pls.v–xxi.

Buckton, G.B. (1903) A Monograph of the Membracidae.London: Lovell & Reeve.

Burmeister, H. (1839) Handbuch der Entomologie. Vol.2. Berlin: T.C.F. Enslin.

Capener, A.L. (1962) The taxonomy of the African Mem-bracidae. Part 1. The Oxyrhachinae. Rep. South Af-rica, Dept. Agr. Tech. Serv., Entomol. Mem. 6:1–164.

Capener, A.L. (1968) The taxonomy of the African Mem-bracidae. Part 2. The Centrotinae. Rep. South Africa,Dept. Agr. Tech. Serv., Entomol. Mem. 17:ii, 1–124.

Chapman, R.F. (1982) The Insects—Structure and Func-tion. 3rd Ed. Cambridge, MA: Harvard UniversityPress.

Cocroft, R.B. (1996) Insect vibrational defence signals.Nature 382:679–680.

De Geer, C. (1773) Memoires pour servir a l’Histoire desInsectes. Vol. 3. Stockholm: P. Hesselberg.

Deitz, L.L., and C.H. Dietrich (1993) Superfamily Mem-bracoidea (Homoptera:Auchenorrhyncha). I. Introduc-tion and revised classification with new family-grouptaxa. Syst. Entomol. 18:287–296.

Dietrich, C.H. (1989) Surface sculpturing of the abdomi-nal integument of Membracidae and other Auchenor-rhyncha (Homoptera). Proc. Entomol. Soc. Wash. 91:143–152.

Fabricius, I.C. (1803) Systema Rhyngotorum secundumordines, genera, species, adiectis synonymis, locis, ob-servationibus, descriptionibus. Brunsvigae: C. Rei-chard.

Fairmaire, M.L. (1846) Revue de la tribu des Membra-cides. Ann. Soc. Entomol. Fr. 4:512.

Fowler, W.W. (1894) Fam. Membracidae. In: BiologicaCentrali-Americana, pp. 1–173, pl. 1–10.

Funkhouser, W.D. (1917) Biology of the Membracidae ofthe Cayuga Lake Basin. Cornell Univ. Agr. Exp. St.,Mem. 2:v, 1–445.

Funkhouser, W.D. (1921) Orthogenesis in the Membraci-dae. Science 54:157.

Germar, E.F. (1835) Species Membracidum musci Ger-mari et dispositio generum Membracidum. Silber-mans Rev. Entomol. 3:223–261, 307–311.

Gunthart, H. (1980) Neuer Fundort und neuer Namefuer die altbekannte Bueffelzikade ‘‘Ceresa bubalus’’(Hom.Auch. Membracidae). Mitt. Entomol. Ges. Basel.N.F. 30:105–109.

Hasenoehrl, S.G., and P.P. Cook (1965) A clarification ofcertain structures in the thoracic region of Oxyrhachis(Homoptera: Membracidae). Ann. Entomol. Soc. Am.58:219–221.

Hoffrichter, O., and E.J. Troger (1973) Ceresa bubalus F(Homoptera: Membracidae)—Beginn der Einwan-derung in Deutschland. Mitt. bad. Landesver.Naturkunde u. Naturschutz. N.F. 11:33–43.

Hunt, R.E. (1993) Role of vibrational signals in matingbehavior of Spissistilus festinus (Homoptera: Membra-cidae). Ann. Entomol. Soc. Am. 86:356–361.

Keil, T.A., and C. Steiner (1990) Morphogenesis of theantenna of the male silkmoth, Antheraea polyphemus.I. The leaf-shaped antenna of the pupa from diapauseto apolysis. Tissue Cell 22:319–336.

Kershaw, J.G.C. (1913) Anatomical notes on a mem-bracid. Ann. Soc. Entomol. Belg. Brux. 55:191–201.

Kirby, W. (1829) An outline and description of CentrotusBennetii and Hardwickii. Mag. Nat. Hist. 2:20–22.

Kopp, D.D., and T.R. Yonke (1972) Morphological obser-vations on the alimentary canal of Entylia bactriana.J. Kansas Entomol. Soc. 45:46–51.

Kopp, D.D., and T.R. Yonke (1973) The treehoppers ofMissouri: Part 2. Subfamily Smiliinae; tribes Acu-talini, Ceresini, and Polyglyptini (Homoptera: Mem-bracidae). J. Kansas Entomol. Soc. 46:233–276.

176 U.E. STEGMANN

Kopp, D.D., and T.R. Yonke (1977) Taxonomic status ofthe Buffalo Treehopper and the name Ceresa bubalus.Ann. Entomol. Soc. Am. 70:901–905.

Kramer, S. (1950) The morphology and phylogeny ofauchenorhynchous Homoptera (Insecta). Illinois Biol.Monogr. 20:vii, 1–111.

Krenn, H.W., and G. Pass (1994) Morphological diver-sity and phylogenetic analysis of wing circulatory or-gans in insects. Part I: Non-Holometabola. Zoology-Analysis of Complex Systems 98:7–22.

Krzelj, S. (1969) Structure anatomique comparee deselytres de Coleopteres. Ann. Soc. R. Zool. Belg. 99:85–109.

Latreille, P.A. (1802) Histoire Naturelle, generale etparticuliere, des Crustaces et des Insectes. Vol. 3.Paris: F. Dufort.

Linnaeus, C. (1758) Systema Naturae per regna trianaturae, secundum Classes, Ordines, Genera, Spe-cies, cum characteribus, differentiis, synonymis, locis.10th Ed. Vol. 1. Holmiae: L. Salvii.

Locke, M., and P. Huie (1981) Epidermal feet in insectmorphogenesis. Nature 293:733–735.

Marcus, H. (1950) Observaciones sobre Membracidae.Fol. Univ. Cochabamba. 4:63–77.

Marlatt, C.L. (1894) The buffalo tree-hopper. Ins. Life.7:8–14.

Matsuda, R. (1970) Morphology and evolution of theinsect thorax. Mem. Entomol. Soc. Canada 76:1–431.

Muller, H.J. (1984) Zur Entwicklung und Lebensweiseder Larven der Dornzikade Centrotus cornutus (L.)(Homoptera: Auchenorryhncha: Membracidae) unterbesonderer Berucksichtigung der Kotschleuder. Zool.Jb. Abt. Anat. Ontog. Tiere. 111:385–399.

Nardi, J.B., and S.M. Magee-Adams (1986) Formation ofscale spacing patterns in a moth wing. I. Epithelialfeet may mediate cell rearrangement. Dev. Biol. 116:278–290.

Nardi, J.B., and S.D. Miklasz (1989) Hemocytes contrib-ute to both the formation and breakdown of the basallamina in developing wings of Manduca sexta. TissueCell 21:559–567.

Nault, L.R., T.K. Wood, and A.M. Goff (1974) Treehopper(Membracidae) alarm pheromones. Nature 249:387–388.

Noirot, C., and A. Quennedey (1974) Fine structure ofinsect epidermal glands. Annu. Rev. Entomol. 19:61–80.

Parsons, M.C. (1967) Modifications of the prothoracicpleuron in Hydrocorisae (Heteroptera). Trans. R. Ento-mol. Soc. Lond. 119:215–234.

Pelaez, D. (1940) Estudios sobre Membracidos. I. Losestadios ninfales de Umbonia crassicornis (Am. etServ.) (Hemipt. Homopt.). An. Inst. Biol. Mexico. 11:611–632.

Pelaez, D. (1941) Estudios sobre Membracidos. II. Losadultos de Umbonia crassicornis (Am. et Serv.)(Hemipt. Homopt.). An. Inst. Biol. Mexico 12:327–344.

Poisson, M.R. (1937) Quelques observations biologiqueset morphologiques sur Ceresa bubalus (Fab.). InsecteHemiptere-Homoptere de la famille des Membracides,d’origine americaine. Bull. Soc. Scient. Bretagne,Rennes Fasc. h.s. 14:32–50.

Poulton, E.B. (1903) Suggestions as to the meaning ofthe shapes and colours of the Membracidae, in thestruggle for existence. In G.B. Buckton (ed.): A Mono-graph of the Membracidae. London: Lovell & Reeve,pp. 273–285.

Quisenberry, S.S., T.R. Yonke, and D.D. Kopp (1978) Keyto the genera of certain immature treehoppers of Mis-

souri with notes on their host plants (Homoptera:Membracidae). J. Kansas Entomol. Soc. 51:109–122.

Rehberg, A. (1886) Ueber die Entwicklung des Insekten-flugels. Jb. Gymn. Marienwerder. 36:1–13.

Remane, R., and E. Wachmann (1993) Zikaden kennen-lernen, beobachten. Augsburg: Naturbuch.

Reuter, E. (1936) Elytren und Alae wahrend der Pup-pen- und Kaferstadien von Calandra granaria undCalandra oryzae. Zool. Jb. Abt. Anat. Ontog. Tiere62:449–506.

Richter, L. (1953) El apendice pronotal en los Membraci-dos. Lozania. 7:1–4.

Richter, L. (1954) Membracidae Colombianae. Caldasia.6:269–380.

Rietschel, S. (1987) Autotomie des Pronotum bei Buckel-zirpen (Homoptera: Membracidae). Entomol. Gen. 12:209–220.

Romeis, B. (1989) Mikroskopische Techniken. 17th Ed.Vienna: Urban und Schwarzenberg.

Snodgrass, R.E. (1909) The thorax of insects and thearticulation of the wings. Proc. U.S. Nat. Mus. 36:511–595, pls. 40–69.

Snodgrass, R.E. (1935) Principles of Insect Morphology.New York: McGraw-Hill.

Stål, C. (1859) Hemiptera. In: Kongliga Svenska Fregat-ten Eugenies Resa Omkring Jorden Andra Delen.Zoologi. I. Insecta, pp. 219–298.

Stål, C. (1866) Hemiptera Africana. Vol. 4. Holmiae:Norstedt.

Stegmann, U.E. (1997) Revaluation of the prothoracicpleuron of the Membracidae (Homoptera): the pres-ence of an epimeron and a subdivided episternum inStictocephala bisonia Kopp & Yonke, Oxyrhachistaranda (Fabr.), and Centrotus cornutus (L.). Int. J.Insect Morphol. Embryol. 26:35–42.

Steiner, C., and T.A. Keil (1993) Morphogenesis of theantenna of the male silkmoth, Antheraea polyphemus.IV. Segmentation and branch formation. Tissue Cell.25:447–464.

Stoll, C. (1788) Representation exactement coloreed’apres nature des Cigales, qui se trouvent dans lesquatre parties du monde, l’Europe, l’Asie, l’Afrique, etl’Amerique. Amsterdam: J.C. Sepp.

Strubing, H. (1992) Vibrationskommunikation imPaarungsverhalten der Buffelzikade Stictocephalabisonia Kopp and Yonke 1977 (Homoptera-Auchenor-rhyncha, Membracidae). Mitt. Dtsch. Ges. Allg. Ang.Entomol. 8:60–62.

Strumpel, H. (1972) Beitrag zur Phylogenie der Membra-cidae Rafinesque. Zool. Jb., Abt. Syst. Okol. Geogr.Tiere 99:313–407.

Strumpel, H. (1983) Beobachtungen zur Autotomie desPronotums bei Anchistrotus-Arten (Homoptera, Mem-bracidae). Entomol. Mitt. Zool. Mus. Hamburg. 119:391–396.

Suchantke, A. (1976) Die Buckelzirpen (Membracidae)und die Formensprache der Insekten. Elemente Natur-wiss. 24:1–14.

Weber, H. (1933) Lehrbuch der Entomologie. Stuttgart:G. Fischer.

Wigglesworth, V.B. (1965) The Principles of Insect Physi-ology. 6th Ed. London: Methuen.

Wood, T.K. (1975a) Defense in two pre-social membrac-ids (Homoptera: Membracidae). Can. Entomol. 107:1227–1231.

Wood, T.K. (1975b) Studies of the function of the mem-bracid pronotum (Homoptera). II. Histology. Proc. En-tomol. Soc. Wash. 77:78–82.

Wood, T.K. (1976) Alarm behavior of brooding femaleUmbonia crassicornis (Homoptera: Membracidae).Ann. Entomol. Soc. Am. 69:340–344.


Wood, T.K. (1977) Defense in Umbonia crassicornis: roleof the pronotum and adult aggregations (Homoptera:Membracidae). Ann. Entomol. Soc. Am. 70:524–528.

Wood, T.K. (1993) Diversity in the New World Membra-cidae. Annu. Rev. Entomol. 38:409–435.

Wood, T.K., and G.K. Morris (1974) Studies of the func-tion of the membracid pronotum (Homoptera). I. Occur-rence and distribution of articulated hairs. Can. Ento-mol. 106:143–148.

Wood, T.K., and J.D. Pesek (1992) Pronotal shape: asource of confusion or panacea in systematic studies oftreehoppers (Homoptera: Membracidae)? In J.T.Sorensen and R. Foottit (eds.): Ordination in the studyof Morphology, Evolution and Systematics of Insects:Applications and Quantitative Genetic Rationals. Am-sterdam: Elsevier, pp. 349–384.

Yack, J.E. (1992) A multiterminal stretch receptor, chor-dotonal organ, and hair plate at the wing-hinge ofManduca sexta: Unravelling the mystery of thenoctuid moth ear B cell. J. Comp. Neurol. 324:500–508.

Yothers, M.A. (1934) Biology and control of tree hoppersinjurious to fruit trees in the Pacific Northwest. U.S.Dept. Agr. Tech. Bull. 402:1–46.

Zacharuk, R.Y. (1985) Antennae and Sensilla. In G.A.Kerkut and L.I. Gilbert (eds.): Comprehensive InsectPhysiology, Biochemistry, and Pharmacology. Oxford:Pergamon Press, pp. 1–69.

Zeller, H. (1938) Blut und Fettkorper im Flugel derMehlmotte Ephestia Kuhniella Zeller. Z. Morph. Okol.Tiere 34:663–738.

178 U.E. STEGMANN

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An exaggerated trait in insects: The ... - Ulrich E. Stegmann · An Exaggerated Trait in Insects: The Prothoracic Skeleton of Stictocephala bisonia(Homoptera: Membracidae) ULRICH