Great Basin Naturalist Memoirs Volume 12 Research in the , Article 6 Homoptera: A Tribute to Paul W. Oman

10-1-1988 Some aspects of the biology, morphology, and evolution of (Homoptera: Cicadelloidea and Membracoidea) J. W. Evans Australian Museum, Sydney, N. S. W., Australia

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Recommended Citation Evans, J. W. (1988) "Some aspects of the biology, morphology, and evolution of leafhoppers (Homoptera: Cicadelloidea and Membracoidea)," Great Basin Naturalist Memoirs: Vol. 12 , Article 6. Available at: https://scholarsarchive.byu.edu/gbnm/vol12/iss1/6

This Article is brought to you for free and open access by the Western North American Naturalist Publications at BYU ScholarsArchive. It has been accepted for inclusion in Great Basin Naturalist Memoirs by an authorized editor of BYU ScholarsArchive. For more information, please contact [email protected], [email protected]. SOME ASPECTS OF THE BIOLOGY, MORPHOLOGY, AND EVOLUTION OF LEAFHOPPERS (HOMOPTERA: CICADELLOIDEA AND MEMBRACOIDEA)

J. W. Evans'

Abstract —This article summarizes some observations of a varied nature on the biology, morphology, and evolution of the Cicadelloidea (Cicadellidae, Hylicidae, Eurymelidae) and Membracoidea(Membracidae, , Biturri- tidae, Nicomiidae). These observations, made over a period of more than half a century, have previously been recorded at different times, but lie buried in the literature. It is hoped that their interest will justify repetition and draw attention to some promising lines of research.

Biology ulatum Linnaeus (Evans 1946b). In his discus- sion of the function of the songs of various Food Plant Associations Auchenorrhyncha, Ossiannilsson described

As Southwood (1961) has pointed out, in- some as being "calls of courtship." Subse- sects have a particularly close association with quently, I noted the presence of well-devel- plants belonging to the predominant flora of oped tymbals in nymphs belonging to every the time. Thus, most Australian cicadelloids instar but the first in both sexes of A. reticida- feed on eucalypts and numerous membracids tiim (Evans 1957). As, presumably, nymphal on acacias. Of particular interest are relict song cannot have a sexual significance, it may that feed on representatives of ancient serve an assembling purpose since aetalionids are insects. floras. Examples are Koebelia californica gregarious However, amongst the Baker on conifers in California and Cornutipo Eurymelidae, which are likewise gregarious, spp. (Eurymelidae) on representatives of the I have been unable to find any trace of tym- Proteaceae in Australia. The Cephalelini, a bals. Nevertheless, prior to mating, eu- tribe of the Ulopinae which have an Antarctic rymelids indulge in a prolonged courtship distribution, provide another example, for (Evans 1931). their feeding seems to be restricted to an an- Tymbal sound production occurs among cient family of plants, the Restionaceae, in representatives of all the superfamilies of the Australia, South Africa, and New Zealand. Auchenorrhyncha, and even in the

Changes of food plants have recently oc- Cicadoidea it is not confined to one sex since curred in the Tartessinae (Cicadellidae). females of Tettigarcta can "sing." Thus, it These are primarily eucalypt feeders, but must have been a feature acquired in early some have become adapted to living in tropi- Mesozoic, if not Palaeozoic, times (Evans cal rain forests and have taken to feeding on 1941). Moreover, it would seem that during other kinds of trees (F. Evans 1981). the early Mesozoic some Auchenorrhyncha were capable of stridulation. This is supposed Sound Production and Courtship because some Upper Homoptera

(e.g. , Eoscartoides bryani Evans) have stridu- Ossiannilsson, in his notable study of the latory areas on the proximal costal area of their "songs" of Homoptera, was the first to draw (Evans 1961). attention to the presence of tymbals in insects tegmina of both sexes belonging to the Cicadelloidea, Oviposition Cercopoidea, and Cicadoidea (Ossiannilsson

1949). Previously, I had noted the presence of When ovipositing, the majority of leafhop- structures that I described as "resembling pers insert their eggs into plant tissue, either tymbals" on the first abdominal segment of singly or in batches. In the latter case, the Darthula hardwickii Gray and Aetalion retic- eggs are covered with secretions that harden

'Australian Museum, Sydney, N.S.W., Australia. Present address; 47 Bundarra Road, Bellevue Hill, Sydney 2023, Australia.

61 62 Great Basin Naturalist Memoirs No. 12 on exposure to the air. The eggs of aetahonids loides punctata [Signoret]) (Evans 1966). and of some bitturitids and membracids are The largest known leaffiopper, the aetal- contained in oothecae situated on the surface ionid Darthula hardwickii Gray, has a length of the plants. Because the AetaHonidae are an of 28 mm, of which the apical 12 mm in both ancient group of insects, it might be thought sexes consists of the prolonged ninth abdomi- that such a method of oviposition predated nal segment. The smallest leafhoppers are egg insertion in plant tissue. However, this is comprised in the Typhlocybinae (Cicadelli- improbable, as the last-named method is dae), some species of which are no more than shared with insects belonging to the super- 2 mm long. Evolutionary development seems families of the Auchenorrhyncha; and eggs, to be frequently accompanied by increase in whether laid inside plants or on their surface, size. Thus, for example, in the Eurymelidae, are equally subject to heavy parasitism. the largest species are seemingly the most recently evolved (e.g., Eunjmelops generosa Gregariousness and Attendance [Stal]).

While all eurymelids and aetalionids, many The two sexes of Cicadelloidea usually re- membracids, and possibly all bitturitids are semble each other in coloration and size. An gregarious, so far as I am aware, no cicadellids exception in respect to color is provided by have this behavior pattern. Since female the sole representative of the Tartessinae to membracids sometimes remain with their occur in New Caledonia. This , Calo- eggs after oviposition, some authors, such as tartessus stalii (Signoret), has males that are Haviland (1925), have credited them with ma- largely black and females that are predomi- ternal care. Eurymelids of both sexes have nantly brown. In regard to size, the Stenoco- been recorded as remaining with their eggs tini () have males that are consider- for a period. It is possible that the gregarious ably smaller than females. habit in this family may be associated with the The Head fact that their nymphs, unlike those of other leafhoppers, lack the ability to jump. The most puzzling feature of the heads of It would seem that all gregarious leafliop- is associated with the origin of pers are ant attended, but the Pogonoscopini, their feeding apparatus. Insects in some other a tribe of the Eurymelidae, are the only ones orders feed by suction, but with all these the that have developed the characteristics of true nature of the transition from mandibulate to myrmecophiles; i.e., they have unusually haustellate mouthparts can be readily under- long legs and small eyes and live in the nests of stood. (Evans 1966). Previously, 1 have suggested that, though the ocelli are on the crown in representatives Morphology of the relict subfamily, the Ulopinae, this con-

dition is a secondary one. If this is correct, Color and Size even though insects with ventral ocelli do not Previously, 1 have suggested that early seem to be disadvantaged, such a change of leafhoppers were brown, as, for instance, is position would seem to be an adaptive one.

Darthula hardwickii , and that green was the Other primitive features of leaffiopper first alternative color to be acquired (Evans heads are the presence of a sensory pit on the 1966). Later evolutionary developments have maxillary plates, which may possibly be given rise to insects that may be predomi- derived from the maxillary palp (Evans 1973), nantly black and have, or lack, yellow, red, or and the complete separation of the maxillary occasionally bluish markings. Some Cicadelli- plates from the genae. dae from Madagascar have striking color pat- Male Genitalia tern differences (Evans 1953). In others, spe- cies occur that have identical male genitalia The male genitalia of insects are more sub- and comprise populations with differing, but ject to change than any other parts of their stable, color patterns (e.g., Eunjmela fenes- bodies. For this reason, they are extensively trata Le Peletier & Serville) (Evans 1933). used for species recognition. The nature and Then, some species have individuals with a the extent of observable differences between very variable color pattern (e.g., Euryme- the aedeagi of closely related insects vary "

1988 EvANS; Biology, Morphology, and Evolution 63 widely and range from slight and constant to nae), and Euacanthella sp. (Euacanthellinae). considerable and variable ones. The subgeni- The best-known examples of the acquisition tal plates and accessory processes are also sub- of morphological features among leaflioppers, ject to considerable change of shape. which are seemingly of nonadaptive signifi- While male genitalia differences are useful cance, are to be found among the Mem- for species separation and genus recognition, bracidae. This phenomenon has been dis- they are sometimes also helpful for family cussed by many authors (e.g., Haviland 1925) recognition purposes. Thus, for example, who observed these insects in the territory while within the Cicadellidae the aedeagus then known as British Guiana. She pointed invariably arises from a basal connective situ- out that the early stages of exaggerated prono- ated between the paired parameres, in the tal development in insects, which, in their

Eurymelidae it lacks any association with the extreme form, were either cryptic or mimetic, basal plate and the parameres. cannot have conferred any protective advan- Inasmuch as simple male genitalia serve the tage, and yet the insects survived. Moreover, same purpose as complex ones and pre- the pronota of many membracids seem to lack sumably in an equally satisfactory manner, any degree of protective significance. and the structure of female genitalia is con- Above I have suggested that the extreme stant, it is difficult to understand the nature of differences found among leaflioppers belong- the advantages conferred by increasingly ing to the genus Colloborrhis Germar in complex male genitalia unless female insects Madagascar may have been initiated by avoid mating with males that have the wrong "explosive speciation." I have also formerly "key. suggested that the same phenomenon may have occurred among Membracidae isolated Adaptive Characters in the Neotropical Region during Tertiary

In addition to the ocelli noted above, other times (Evans 1959). This is because, though adaptive characters among leaflioppers are to doubtless enlarged pronota were a mem- be found in the Stenocotini, an endemic Aus- bracid characteristic before this isolation took tralian subfamily of the Ledrinae, and in the place, it is in South America only that the Eurymelidae. Stenocotids, which live under evolution of such a range of bizarre forms took bark of eucalypts, are flattened insects, and place. their nymphs are paper thin. While most eu- The development in leaflioppers of bizarre rymelids are wedge-shaped, one species, structures, which apparently lack adaptive Platyeurymela semifascia (Walker), which, significance, is not confined to changes in the like stenocotids, lives under bark, is oval in shape of the prothorax. These occur also in the shape and convex. heads of leaflioppers, as, for example, in those Alary dimorphism and polymorphism are of of Cornutipo tricornis Evans, Listrophora widespread occurrence in the , evansi Evans, and Wolfella caternaulti they are rare in the Homoptera-Auchenor- Spinola (all illustrated in Evans 1975a). rhyncha, and in the Cicadellidae they would seem to be particularly associated with insects Evolution living at high altitudes or in a marsh environ- Fossils and the Classification of Recent Forms ment. Thus, Monteithia spp. (Monteithiini, Ulopinae), which live at high altitudes in New An abundance of wings of Homoptera has Guinea, and of which fully winged insects been found in and Triassic strata in have not been recorded, have males that dif- both the northern and southern hemispheres. fer from females in the extent to which their These seem to provide evidence that all the wings are foreshortened (Evans 1968). Then, existing superfamilies of the Auchenorrhyn- in Cephalelini, which inhabit both alpine and clia were already differentiated by Triassic low-level marsh environments, both sexes oc- and possibly Permian times. If this suggestion cur in a flightless and a fully winged condition. is valid, it provides an example of unusual Some other leaflioppers with both brachyp- evolutionary stability (Evans 1964). terous and fully winged individuals are In the forewings, or tegmina, of some Taslopa montana Evans (Ulopini, Ulopinae), Upper Permian Homoptera (e.g., Homa- Chiasmus varicolor (Kirkaldy) (Deltocephali- loscytina plana Tillyard) six veins support 64 Great Basin Naturalist Memoirs No. 12 their apices. These are as follows: Rib, Rs, lateral prominences of varying size, or be lat- Ml, M2, M3, and M4. In some recent Ci- erally humped, and it may be widest either cadelloidea, only four veins serve the same anteriorly or posteriorly, while the scutellum purpose, and it is of interest to note that the may be of normal size or raised into a large, identity of these is different in each of the vertical crest. The tegmina may have basic comprised families. Thus, in the Hylicidae, cicadellid, or reticulate, venation. One spe- they are Rib, Rs, Ml + 2, and M3+4 + CuA; cies (C. rugosa Evans) has a characteristic in the Eurymelidae, Rl, Ml + 2, M3+4, shared only with the tegmina of Permian and and CuA; and in the Cicadellidae, Rib, Triassic Homoptera. This is the proximal This circum- Rs + Ml+2, M3 + 4, and CuA. arching of vein CuA so that it makes contact stance would seem to provide evidence of the with vein M. Finally, the hind tibae may be separate, direct derivation of insects com- narrowly rectangular in section, or broadly in the leafhopper families from a com- prised spatulate. It is of interest to note that some of 1964). mon ancestral stock (Evans 1949, The the characteristics listed above are shared fossil insect placed in a new recently found with the Ledrinae, while others are of a mem- family, the Jascopidae, belongs in Homoptera bracidlike nature (Evans 1953, 1959). my opinion to the Cicadellidae (Evans 1972). Supposed Sympatric Speciation Parallel Evolution During 1959 a symposium was held in Mel- The most striking example of parallel evolu- bourne to celebrate the centenary of the Royal tion in the family Cicadellidae is provided by Society of Victoria. Its proceedings were later the resemblance between insects comprised published under the title "Evolution of living in the Cephalelini (Ulopinae) and the Para- organisms." At the end of the paper I con- dorydiini (Hecalinae). Leafhoppers in both tributed to this symposium (Evans 1962), I tribes have species with short, triangular said: heads and others with long, narrow ones, the complete insect being seedlike in appearance. The concept of sympatric speciation is at the present While the Paradorydiini, unlike the Cephale- time ahnost universally discredited and any mention of it, even as a possibility, might seem to have no place in a lini, do not feed on the rushlike Restionaceae, contribution purporting to be scientific. This is especially some have been recorded from "rushes ' grow- so when, as in the case of the present instance, a sugges- ing in marshes. The Ulopinae and the Hecali- tion is made that is unsupported by experimental evi- nae are not closely related and probably were dence. Nevertheless, in my opinion, it is possible that differentiated during different geological pe- sympatric speciation may take place within a particular group of leaflioppers, the Typhlocybinae, and the reason riods, the former being of Mesozoic and the for this opinion is because amongst these insects disconti- latter possibly Tertiary origin. nuities between populations of an ecological and ethologi- cal nature would seem to be more readily capable of Explosive Speciation achievement than isolation of a geographical nature. Typhlocybids, which are of world-wide distribution, Above I have mentioned an instance of sup- are particularly well represented in the Holarctic Region. posed "explosive speciation that has occurred They range in length from 2-4 mm. This group comprises in Madagascar with leafhoppers belonging to some hundred genera, several of which contain many the genus Coloborrhis Germar (Ulopini, Ulo- hundreds of distinct species. These leaflioppers differ pinae). The type species of the genus, C. cor- greatly in the extent to which they are restricted in their feeding requirements. Some feed, mate and breed only ticina Germar, has an extensive distribution on a single species of plant or on a limited range ol related in Africa from where no other species has plants. Others have wider feeding habits. The mere fact been recorded. It is established also in Mada- that related species have different ranges of food plants gascar, from where no less than 16 other spe- implies an ability, on occasion, to become accommodated to a new diet. cies, which could equally well be regarded as Mention has already been made of the songs of Ho- belonging to separate genera, have been de- moptera and it may be of significance that typhlocN bids scribed. These differ strikingly from one an- have unusually large apodemes for the support of their other in characters of the head and thorax. tymbal muscles and hence, presumably, are particularK' Thus, the head may be rounded anteriorly, or vocal. It is accordingly suggested that an isolating factor which may have enabled the evolution of large numbers narrowly, or broadly spatulate, and it may of sympatric species might be the s\nchronization of the have differently shaped prominences on the ac(iuisition of a new call note with that of a new food plant.

crown. Then, the pronotum may have a pair of The reason it has been suggested that it is improbable 1988 EVANS: LEAFHOPPER BiOLOCJY , MOKPMOLOGY, AND EVOLUTION 65

that geographical isohition has been tlie principal factor most widely distributed and contain the enabhng prohfic speciation to take place among typhlocv - largest number of species. The characteristics bids is because their small size and swarming habits make of representatives of this subfamily, given them particularly liable to transport in the upper air and be- hence to rapid and wide dispersal. low, precede those of D. hardwickii, which are given in parentheses. Wide maxillary My views on the above matter have not plates with sensory pits, continuous with the changed during the 25 years that have elapsed genae (narrow maxillary plates with sensory since I first expressed them. pits, separated from the genae by a subgenal suture); hind margin of lora widely separated Some Characteristics of from the antennal bases (hind of lora Island and Montane Faunas margins adjacent to the antennal bases); frontoclypeus When the gene flow of insects is restricted lacking any trace of epistomal suture and ex- following the isolation of small initial popula- tending posteriorly as far as the hind margin of tions, the process of evolution is often acceler- the face (frons separated from the postclypeus ated. Mention has already been made of de- by an epistomal suture anteriorly and the velopments that have occurred on the island arms of the epicranial suture posteriorly); of Madagascar following the presumed isola- ocelli situated near the sides of the fronto- tion of a population of the ulopid Coloborrhis clypeus and close to, or on, the margin of the

corticina . The occurrence of aberrant leaf- head separating the face from the crown hoppers is not confined to large islands. Thus, (ocelli on the face of the head close to the sides on Juan Fernandez Island there occurs possi- of the epicranial suture and at a considerable bly the most grotesque of all leafhoppers, distance from the hind margin of the face) Evansiola kiischeli (China). The head of this (Evans 1975a). species is twice as wide as long, and, when The thorax. —Some supposed relict char- observed from above, projects laterally con- acters are the small pronotal paranota, such as siderably beyond the sides of the rest of the occur in the Myerslopiini (Ulopinae), and ex- body (Evans 1975a). tensions of the costal region of the tegminal Montane faunas in Australia and New pads of the nymphs of some ulopids, such as Guinea comprise survivors from a time when those of Coloborrhis corticina and also a few prevailing climates were cooler than at pres- macropsids (Evans 1968). These paranota and ent and from immigrant species belonging to the mesothorasic costal expansions are re- later evolved groups. Examples belonging to garded as relict features because the former the first category are provided by Taslopa were possessed by many Palaeozoic insects montana Evans (Ulopinae, Ulopini), which and the latter occur also in the , and has been recorded only from high altitudes in in some Cicadelloidea and Membracoidea, Tasmania and southeastern Australia, and which, for other reasons, are regarded as Monteithia spp., which inhabit high-level en- relict forms. vironments in New Guinea (Evans 1966, The abdomen.—Among relict characters is 1968). A leafhopper in the second category is the retention of tymbals in the nymphs as well Atistroagalloides rosea Evans (Austroagal- as in the adults of some aetalionids, and the loidinae) (Evans 1966). presence in the male genitalia of bisegmented

subgenital plates. I have suggested that the Relict Characteristics latter, which occur in some Ulopinae, The relict characteristics of leafhoppers can Macropsinae, and Agallinae, represent the be recognized by making a comparison of gonocoxites and the gonostyli of the ninth ab- those features in which presumed recently dominal segment (Evans 1975). evolved forms differ from those of presumed earlier origin. Conclusions The head. —Below are given particulars of how recent Deltocephalinae differ in head The observations recorded in this article structure from the ancient aetalionid, serve to emphasize that the factors responsi- Darthula hardwickii. Not only are the Del- ble for evolutionary change are of varied na- tocephalinae probably the most recently ture. Some, involving major changes of struc- evolved of all cicadellids, but they are also the tural organization, present puzzling features. 66 Great Basin Naturalist Memoirs No. 12

gascar. Mem. Inst. Sci. Madagascar E. 11: 481- Others suggest that evolutionary develop- 507. ments need not always be of an adaptive na- 1961. Some Upper Triassic Heniiptera from ture, that isolation of populations need not Queensland. Mem. Queensland Mus. 14: 13-23. 1962. Evolution in the Homoptera. Pages 250- always be of a geographical nature, and that 259 in The evolution of living organisms. Mel- is particu- the development of bizarre forms bourne University Press. larly associated with isolation of populations 1964. The periods of origin and diversification of the superfamilies of the Auchenorrhyncha as on islands. de- termined by a study of the wings of Palaeozoic and Mesozoic fossils. Proc. Linn. Soc. London 175: 171-181. Literature Cited 1966. The lealhoppers and of Aus- tralia and New Zealand. Mem. Australian Mus. Evans, F. 1981. The Tartessinae of Australia and New 12: 1-347. Guinea (Homoptera, Cicadellidae). Pacificlnsects 1968. Some relict New Guinea lealhoppers and 23: 112-188. their significance in relation to the comparative

Evans, J. W 1931. Notes on the biology and morphology morphology of the head and thorax of the Ho- of the Eurymelinae. Proc. Linn. Soc. N.S.W. 56: moptera-Auchenorrhvncha. Pacific Insects 10: 210-226. 215-229. 1933. A revision of the Eurymelini (Homoptera, 1972. Some remarks on the family Jascopidae (Ho- Bythoscopidae). Trans. R. Soc. S. Australia 57: moptera, Auchenorrhyncha). Psyche 79: 120-121. 73-90. 1973. The maxillary plate of Homoptera-Auchen- 1941. The morphology of Tettigarcta toinentosa orrhyncha. J. Entomol. 48: 43-47. White. Pap. Roy. Soc. Tasmania 1940; 35-49. 197.5a. The external features of the heads of 1946a. A natural classification of lealhoppers Qas- lealhoppers. Rec. Australian Mus. 29: 407-439.

soidea, Homoptera) Pt. I. Trans. R. Soc. London 1975b. The structure, function and origins of the

96: 47-60. subgenital plates of leafhoppers. J. Australian En- 1946b. A natural classification of lealhoppers Pt. tomol. Soc. 14: 77-80. II. Trans. R. Soc. London 97: 39-54. Haviland, M D 1925. The Membracidae of Kartabo, 1953. Les Cicadellidae de Madagascar. Mem. British Guiana. Zoologica 6: 239-290. Inst. Sci. Madagascar E. 4: 87-137. OssiANNlLSSON, F 1949. Insect drummers. Opusc. Ento- 1957. Some aspects of the morphology and inter- mol. Suppl. 10: 1-142. relationships of extinct and recent Homoptera. SouTHWOOD, T R E 1961. The numbers of species of

Trans. R. Entomol. Soc. London 169: 275-294. insects associated with various trees. J. Anim. 1959. Quelques nouveaux Cicadellides de Mada- Ecol. 30: 1-8.