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Digitale Literatur/Digital Literature

Zeitschrift/Journal: Denisia

Jahr/: 2002

Band/Volume: 0004

Autor(en)/Author(s): Rakitov Roman

Artikel/Article: What are brochosomes for? An enigma of (, Cicadellidae) 411-432 © Biologiezentrum Linz/Austria; download unter www.biologiezentrum.at

What are brochosomes for? An enigma of leafhoppers (Hemiptera, Cicadellidae)

R.A. RAKITOV

Abstract

Production of brochosomes is an enig- are functionally analogous to the waxy matic trait unique to leafhoppers (Cicadel- particulate coatings of epidermal origin on lidae). These curiously structured ultra- the integument and eggs of various insec- microscopic protein-lipid particles are pro- ts. The synthesis of secretory products by duced in the specialized cells of the Mal- the Malpighian tubules and the habit of pighian tubules, but it is unlikely that they applying these products on the integument are an excretory product. Leafhoppers may have evolved in the ancestral Cicado- actively apply brochosomes to their inte- morpha as an adaptation to a subterranean gument and, sometimes, to their egg nests. habitat of the immatures. These traits may The small size and intricate surface struc- have been preadaptations to using such ture of brochosomes apparently render products, rather than epidermal waxes, as layers of these particles unwettable with a protective coating when the immatures water and sticky . Another pos- of early switched to free- sible function of such coatings is direct or living. The inadequate knowledge of the indirect protection against the attachment properties of brochosomes and complete and germination of fungal spores. It is lack of experimental studies render the unlikely that any of the other proposed current interpretations highly speculative. roles, that include the protection from To fully elucidate the function of brocho- desiccation, UV light, temperature fluc- somes, future studies should employ diver- tuations, and from predators and parasites, se experimental and comparative approa- is the major function of this secretion in ches. the extant Cicadellidae. None of the hypo- Key words: Hemiptera, Cicadellidae, thetical roles of brochosomes has yet been brochosomes, integument, eggs, Malpighi- investigated experimentally. All such an tubules, wax, secretion, structure, Denisia 04, roles, however, suggest that brochosomes zugleich Kataloge des OÖ. Landesmuseums, behavior, function, . Neue Folge Nr. 176 (2002), 411-432

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1. Introduction immatures and adults of the same (STOREY & NICHOLS 1937; NAVONE 1987; Leafhoppers (Cicadellidae) can he charac- RAKITOV 1996, 2000b). An adult terized as organisms coated with brochosomes. usually picks up a droplet of the secretion from The known exceptions are immatures from the anus with its hind legs and spreads it all certain , that do not produce bro- over the ventral body surface and appendages; chosomes until the last , and a few aber- a few minutes later it releases a few more dro- rant species. Production of this unique bioma- plets, transfers them onto the forewings, and terial sets leafhoppers apart from the rest of spreads them over the dorsal side of the for- and in general. ewings, pronotum, and head (Figs 3, 4)- The Leafhoppers actively apply brochosomes on fluid dries leaving a sediment of brochosomes. and spread them over the body using modified Anointing is followed by vigorous grooming: legs. Apparently, brochosomes play a certain the leafhopper rapidly rubs and brushes its role in the life of leafhoppers. What might this body and appendages. During this process bro- role be? Answering this question is integral to chosomes are redistributed more evenly across understanding the ecology and physiology of this largest of the extant exopterygote the integument. In particular, in adults, bro- insects as well as the causes of its spectacular chosomes are scraped from the dorsal forewing radiation. Yet, fifty after the discovery of surface onto the hindwings and the dorsal the "ultramicroscopic bodies" (TULLOCH et al. abdomen. Rows and groups of strong setae on 1952) their properties remain poorly known, the legs of leafhoppers (Fig. 5) serve as minute and their function is essentially enigmatic. rakes or brushes for manipulating the brocho- This contribution briefly reviews what isknown some powder (VlDANO & ARZONE 1984; about brochosomes from the perspective of NAVONE 1987; RAKITOV 1998). Anointing is Fig. 1. A female of sp. and its Malpighian tubules, shown at their function and discusses the hypotheses the same scale. The blind posterior aiming to explain it. ends of the two left tubules are atta- ched to the rectum. The tubule pro- ducts are released through the anteri- 2. Brochosomes or ends that open into alimentary canal between the midgut and the hindgut (not shown). The relatively 2.1 Brochosomes on Integument large size of the brochosome-secreting segments (arrow) may be viewed as Brochosomes are protein-lipid particles an indirect indication of the important synthesized in the glandular segments of the role played by brochosomes. Bar = 1mm Malpighian tubules of leafhoppers (Fig. 1). Size and structure of brochosomes vary among species, but in the majority of examined - hoppers they are hollow spheres, 0.2-0.6 urn in Fig. 2. A brochosome of diameter, with a honeycomblike surface irroratus (SAY). Particles of this type (Fig. 2). The bottoms of the hexagonal and are produced by the majority of the pentagonal surface compartments usually have examined leafhopper species. Bar = 100nm. openings leading into the central cavity. Brochosomes originate in Golgi complexes and acquire their final shape before leaving secretory cells (DAY &. BRIGGS 1958; SMITH & LlTTAU 1960; GOURANTON & MAILLET 1967;

CHEUNG & PURCELL 1991; RAKITOV 1999a, 2000a). Figs 3-4. Successive moments of anointing in flavicollis (L). Fig. 3. The brocho- After molts, leafhoppers release a colloidal some-containing secretion is being released suspension of hrochosomes through the hind- from the anus and picked up with the hind legs. The fluid appears opaque because of gut and apply it on the new integument. the presence of brochosomes. Fig. 4. The Details of this behavior, referred to as anoin- hind legs are spreading this fluid over the ting, vary7 between species and also between dorsal integument.

412 © Biologiezentrum Linz/Austria; download unter www.biologiezentrum.at usually observed within 1-3 hours after the can be done under the stereomicroscope by molt before the leathopper starts reeding. It touching the integument with a preheated may be repeated several times; adults appa- entomological pin: melting of the particulate rently retain the ability to secrete hrochoso- wax is readily seen, while the layer ot brocho- mes throughout their lifetime (RAKITOV somes remains unchanged. To draw a final 1996). In the leafhoppers that have the inte- conclusion, however, the material should be gument already coated with hrochosomes, studied under the electron microscope. A tew bouts of grooming are observed as a stand- known cases or wax production in leafhoppers alone behavior. will be touched on below. Brochosomes can be

Figs 5-8. External appearance of brochosome coats. Fig. 5. exitiosus UHLER. A very thin light deposit of brocho- somes can be noticed on only the dark parts of abdomen, thorax, and legs. The bluish tint of the coat is created by scattering of light by the particles close to 0.5pm in dia- meter, known as the TINDALL effect. Fig. 6. Sochinsogonia robonea YOUNG. The brochosome coat is con- spicuous on the dorsal surface of the forewings as well as on the other body parts. Fig. 7. Proconia sp. The white bro- chosome powder is very conspi- cuous on the brown cuticle of this male specimen. Fig. 8. Vilbasteana oculata (LINDB.) displays reserves of brochosomes in the form of white oval spots in the costal part of each forewing (only left spot is visible in the photo). Often referred to as "wax-areas", such spots are common among .

The brochosome coat varies in continuity found on all of the body parts, including and thickness among species, individuals, and antennae (Figs 9-14), but the eyes usually body parts of the same individual from scatte- remain clean, and the dorsal surface of the for- red particles to a dense layer (Figs 5-14). It ewings, from which brochosomes are transfer- may be visible in the stereomicroscope as a red to other body parts, often is almost bare pale, non-shiny thin deposit on the darker (RAKITOV 1995). As a modification of the body parts (Fig. 5). Thicker coats, visible by typical adult anointing described above, some naked eye, occur more rarely (Figs 6, 7) and species do not spread the droplets ot the resemble particulate waxy coats produced by brochosome suspension but let them dry the epidermis of various insects. A quick test on the forewings as a pair of spots (Fig. 8).

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These spots, referred to in older literature rity of the examined subfamilies produce bro- as "wax areas", serve as temporary1 reserves of chosomes. These have not been found, how- ready-to-use secretion. From here brocho- ever, in the nymphs of Idiocerinae, Macro- somes are spread across the entire body sur- psinae, , Agalliinae, and Typhlocy- face through grooming (VlDANO & ARZONE binae. The nymphs of the studied Idiocerinae 1984; NAVONE 1987; RAKITOV 2000b). did not display anointing behaviors (NAVONE I have examined the integument in adult 1987; RAKITOV 1996), while those of the representatives of the majority of the current- other four subfamilies anointed themselves ly recognized subfamilies of Cicadellidae with Malpighian tubule secretions lacking

Figs 9-14. Brochosomes on the integument. Figs 9, 10, 11, 12. Paraphlepsius irro- ratus (SAY), zooming into the hind coxa. White rec- tangles in Figs 9, 10, and 11 display the field of view at the next magnifi- cation. Bars: Fig. 9— 500pm; Fig. 10—50um; Fig. 11—5um; Fig. 12—0.5pm. Fig. 13. Brochosome coat on the ventral forewing surface of an adult Xesto- cephalus desertorum (BERG). Bar = 10pm. Fig. 14. The outer surface of the hind tibia in a 5th instar of X. deser- torum is also coated with brochosomes. Bar = 50um.

(RAKITOV 1995, 1998). Brochosomes have not brochosomes (RAKITOV 1996, 1999a). Never- been found only in several species of Jossus, theless, scattered brochosomes can be seen on Ledm, , and Cephalelus. They have the micrographs of the integument of the last been found, however, in other , instar nymphs of fabae Harris , and Ulopinae, suggesting that the (McGuiRE 1985), indicating that not all species lacking the trait lost it secondarily. In typhlocybine nymphs lack brochosomes. Myerslopia, recently placed into a separate family (HAMILTON 1999), brochosomes also Anointing behaviors similar to those of leaf- have not been found. Nymphs from the majo- hoppers have been observed in

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(Membracidae): adult Heteronotus (EKKENS ra of the tribe Proconiini () are 1972, p. 267), immature and adult Gargara known to powder such egg nests with brocho- (RAKITOV 1996), and adult Plancotis (RAKI- somes (Figs 15-18) (SWAIN 1937; TURNER & TOV unpublished). Treehoppers have in their POLLARD 1959; RAKITOV 1999b and unpublis- Malpighian tubules glandular segments similar hed; Hix 2001). Immatures, males and virgin to those of leafhoppers, but these synthesize females of these species produce typical sphe- secretory products distinct from brochosomes rical "brochosomes-for-integument" (see abo- (RAKITOV unpublished). Such products are ve) and spread them over the body, while the apparently applied onto the integument gravid females produce morphologically

Figs 15-18. Use of brocho- somes in oviposition in orbona (F.). Figs 15, 16. A female scra- pes brochosomes from the white pellets present on its forewings onto the ovi- position site with synchro- nous strokes of the both hind tibiae. Fig. 17. The egg nest on the adaxial side of a 5/7- phium sp. leaf several days after oviposition. The eggs with dark embryonic eye spots are partly visible through the epider- mis. The epidermis is une- venly coated with white brochosome powder. Fig. 18. Elongate "brocho- somes-for-eggs". Such par- ticles comprise the pellets on the forewings of the egg-laying females and the coat on the egg nests. Bar = 5 urn.

during anointing but form no particulate coa- distinct particles, "brochosomes-for-eggs" tings. No brochosomes have been found on (Fig. 18) (RAKITOV 2000a; Hix 2001). Shortly the integument of treehoppers (DIETRICH before oviposition, a female places droplets of the brochosome suspension onto its forewings, 1989). where they dry as a pair of conspicuous white 2.2 Brochosomes on Egg Nests pellets. During oviposition, the female scrapes this material with its hind tibiae onto the ovi- Most leafhoppers insert their eggs into position site (Fig. 15, 16), making a pulveru- living plant tissues. Species from several gene- lent coat (Fig. 17).

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2.3 Chemical Properties other insects do not? And why do not some species or stages of leafhoppers produce bro- Brochosomes have not yet been isolated chosomes? A satisfactory explanation of the and analyzed with modern biochemical role of brochosomes must address each of the- methods. Most of the available data on their se questions. Different authors interpreted composition are derived from histological stu- brochosomes as waste products, a protective dies. The brochosome-secreting cells display material, or as reservoirs of hypothetical an extensively developed rough endoplasmic . Below, these hypotheses will be reticulum, indicating production of large considered in more detail. quantities of protein (SMITH & LlTTAU 1960; GOURANTON & MAILLET 1967; RAKITOV 1999a, 2000a). Histochemical tests demon- 3.2 Brochosomes and Excretion strated that brochosomes contain both protein Because brochosomes contain protein and and lipid. One study suggested that brochoso- are produced in the Malpighian tubules, the mes comprise a protein skeleton coated with primary excretory organs of insects, it has saturated lipids (SMITH & LlTTAU 1960), but been suggested that they are bizarre nitroge- another found that they contain proteins and nous waste products (SMITH & LlTTAU 1960; unsaturated phospholipids that are not spatial- WlCCLESWORTH 1972). This interpretation ly separated (GOURANTON & MAILLET 1967). seemed to gain support from histochemical GOURANTON (1967) detected an alkaline tests that indicated that the Malpighian tubu- phosphatase in developing brochosomes in les of leafhoppers contained neither urates, viridis (L.) but not in two other spe- nor any other end products of nitrogen meta- cies. MAYSE (1981) tested masses of "brocho- bolism commonly found in terrestrial insects somes-for-eggs" collected from the forewings (SMITH & LlTTAU 1960). The qualitative tests of (F.) for the presence of of MAYSE (1981), that detected allantoin and several common excretory products urea in the "brochosomes-for-eggs", have not and detected allantoin and urea. Brochosomes been published in full and do not indicate are remarkably resilient: they are not soluble whether these compounds are major constitu- in organic solvents (GOURANTON & MAILLET ents in the material. More recent studies 1967); in the dry form they are rigid and found the regular watery excretion of Proconi- durable. ini to contain very dilute concentrations of allantoin and uric acid but high concentrati- 3. Function of Brochosomes ons of ammonia, suggesting that the latter is the primary waste product in these insects 3.1 Problems and Hypotheses (BRODBECK et al. 1993). Because these studies did not take into account production of bro- Nothing currently known about the habi- chosomes, the conclusion that proconiines are tats, life history, feeding mode, locomotion, ammonotelic should be reassessed when the communication, protection, or reproduction composition and the amount of brochosomes of Cicadellidae appears to explain the func- produced in the Malpighian tubules are known. tion of brochosomes. Most of the biological While the relations between the nutritional features of the family can be found among the physiology of Cicadellidae and synthesis of rest of Auchenorrhyncha, for example, in Del- brochosomes remain obscure, it is clear that phacidae. Do brochosomes have a special fun- there is no direct connection between a parti- ction or are they merely excretory products? cular diet and the production of brochosomes. Or, perhaps, they are excretory products that The leafhopper species feeding on occasionally serve accessory functions? Is the (Cicadellinae sensu lato), mesophyll (most intricate structure of brochosomes finely tun- Typhlocybinae), and (the rest of leaf- ed to perform certain function? Or, is their hoppers) often produce brochosomes of simi- shape the artifact of a peculiar crystallization lar structure. Moreover, immatures of several process? Do the brochosomes covering egg subfamilies do not produce brochosomes, whi- nests have the same function as the brochoso- le sharing the diet with the brochosome-pro- mes coating the integument? In general, why ducing adults (RAKITOV 1995, 1996, 1999a). do leafhoppers produce brochosomes while

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In other insects, not everything that mal (CA=180°). Surfaces are generally refer- comes out of the Malpighian tubules is an red to as wettable if CA<90° and unwettable excretory product. These organs appear to be if CA>90°. A droplet placed between two apt to evolving secondary functions quite solid surfaces (e.g., wings) will pull unrelated to excretion, and in one case even them together if the surfaces are wettable or function as luminescent organs (GREEN 1979). push them apart it they are unwettable. If any Malpighian tubules modified to perform an given smooth surface is wettable, adding rough- accessory synthetic function are known in ness will increase its wettability. If it is various insect groups. For example, specialized unwettable, the added roughness will increase segments of the tubules synthesize and export CA leading to still greater unwettability (for silk for spinning cocoons in larvae of Neurop- more details, see HOLLOWAY 1970). The mate- tera and certain Coleoptera (for more details, rials forming the exposed surfaces in terrestri- see RAKITOV in press). In none of these cases al and insects are often poorly wettable have the synthetic products been shown to be by water due to their chemical properties, but related to the excretory function. CA on the smooth layers of such materials still does not exceed 110-120° (Fig. 23B). Lar- Ultrastructural data suggest that brochoso- ger CA (up to 160-170°) are achieved by mes are unlikely excretory products. The bro- development of a microsculpture at the chosome-secreting cells display only poorly micron and submicron range (HOLDGATE developed labyrinth and apical microvil- 1955; HOLLOWAY 1970; JUNIPER 1991; WAG- li—cell features that are typically associated NER et al. 1996; BARTHLOTT & NEINHUIS with excretion (SMITH &. LlTTAU 1960; GOU- 1997). Roughness can be developed to such an RANTON & MAILLET 1967; CHEUNG &. PUR- extent that the water-covered surface holds CELL 1991; RAKITOV 1999a, 2000a). It is unli- air. Such surfaces, referred to as "composite", kely that waste products can be transferred display extremely large CA. from the other tubule parts into the cells of the glandular segment to acquire here the sha- It is clear now that, even if the material pe of brochosomes. comprising the surface of brochosomes is only moderately hydrophobic (due to an external lipid layer? hydrophobic protein chains?), bro- 3.3 Water-repellence and Incontaminability chosome masses may be highly water-repellent because they form a complex fractal surface Immersing a fresh leafhopper in saline structure in the submicron-to-nanometer ran- solution to dissect its Malpighian tubules or ge (Fig. 12). When covered with water, the gluing a leafhopper specimen to a cardboard layer of brochosomes may be able to trap the triangle with a water-based glue are often air between the particles, in their wall com- tedious because the brochosome-coated inte- partments, and in their central cavities. gument repels the liquids. A simple experi- Indeed, a plastron of air is readily visible on ment demonstrates that small droplets of submerged leafhoppers that are coated with water adhere to clean intact leafhopper inte- brochosomes. Such coats are also repellent to gument but are repelled when it is coated with aqueous sugar solutions and other water-based brochosomes (Figs 19-22). sticky substances (personal observations). The physical principles of wetting of plant Another property of brochosome coats derives and surfaces have been extensively stu- from their particulate nature. Because of the died (CASSIE & BAXTER 1945; FOGG 1948; loose attachment of the particles to each other HOLDGATE 1955; HOLLOWAY 1970; JUNIPER and to the integument, a brochosome-coated body part brought in contact with water or a 1991; WAGNER et al. 1996; BARTHLOTT & sticky substance will more likely to lose some NEINHUIS 1997). A commonly used measure brochosomes rather than become trapped. of wettability is contact angle (CA), i.e., the angle between the surface and the contour of Why should leafhoppers care about wet- a small liquid drop placed upon it (Fig. 23A- ting and sticking? As with all small terrestrial C). The area of contact between a completely , contact with water may result in unwettable surface and the drop is infinitesi- the organism becoming trapped by the surface

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tension. Water can block the spiracles, stick duce large amounts of paniculate wax that movable body parts together, and stimulate renders them invulnerable to the honeydew germination of entomopathogenic fungal spo- (see next section). res. Rain and dew endanger insects living far Highly hydrophobic, powdery brochosome from water. , that excrete sticky coats of leafhoppers may be an efficient pro- sugar-containing "honeydew" if feeding on tection from rain and dew. The coat may also phloem and mesophyll or non-sticky but far supplement the excrement-shooting mecha- more copious watery excretion if feeding on nism as a protection from the leafhoppers' xylem, may be at even greater risk. Not surpri- own excretion (GüNTHART 1977; ARZONE

Figs 19-22. Brochosome coat and wettability of the integument in Nio- nia palmeri (VAN DUZEE). Fig. 19. An adult with a poorly developed coat displays its black and shiny cuticle. Fig. 20. An adult collec- ted at the same locality but at a different time is completely coated with pink brochosome pow- der. Inset: brochosomes. Bar = 0.5 urn. Fig. 21. A droplet of water placed upon the forewing of the speci- men from Fig. 19 wets the integument. Contact angle <90°. Fig. 22. A similar droplet does not adhere to the brochosome-coated for- ewing of the specimen from Fig. 20. Contact angle is ca. 160°.

singly, this group demonstrates an array of 1986; NAUINE 1987; RAKITOV 1995). This ingenious defense mechanisms that includes kind of protection may be especially impor- incorporating the excretion into the scale tant in denser populations, where the leafhop- covers in armored scale insects (FOLDI 1982), pers are at risk of being contaminated with the coating the honeydew droplets with a layer of neighbor's excrement directly or through the wax in immature psyllids (WEBER 1930), contaminated plant surface. Moreover, the removing droplets from the anus with the legs "anal gun" is not completely faultless, and the in some (KUNKEL 1972), and shooting excretion sometimes accumulates at the rear excreta in aphids, psyllids, , and body end (personal observation). The brocho- Auchenorrhyncha (WEBER 1930; KUNKEL some coat may prevent the abdomen and 1972; STRC'MPEL 1983). Many Homoptera pro- wings from sticking together when the excre-

418 © Biologiezentrum Linz/Austria; download unter www.biologiezentrum.at tion penetrates between them or if dew preci- typhlocybine species in which no brochoso- pitates on their surface. The brochosome pow- mes have been found (Vilbasteana, , der on the integument may also help leafhop- spp.—RAKITOV 1995), in contrast to pers escape from spider webs, similarly to lepi- the brochosome-coated adults, feed on only dopterans that sometimes escape leaving but a the lower surfaces of (personal observa- few scales on the adhesive threads (NENTWIG tion). This habit may partly compensate for 1982). Of equal importance may be protection the absence of the protective paniculate coat, from sticky glandular trichomes on the surface because the nymphs are protected from rain of plants (TlNGEY 1985) and from sticky spo- and because their honeydew falls down with-

res of certain entomopathogenic fungi (see out contaminating the leaf surface and the Fig. 23. Wetting of surfaces displaying different contact angles. (A) Smooth neighbors. Wetting and sticking are especially below). In case of the Proconiini egg nests, the surface of a wettable material; contact brochosomes placed upon the fresh egg scar, hazardous for small insects, because such ins- angle < 90°. (B) Smooth surface of an left in the plant by the ovipositor, may prevent ects may not be able to overcome the surface unwettable material (e.g., wax); contact angle >90°. (C). Surface coated flooding of the eggs by plant fluids and ensure tension of the liquids. Brochosome coats are with hydrophobic particles (e.g., bro- the penetration of air to the developing usually better developed in smaller leafhop- chosomes) holds a film of air and dis- embryos. pers. Reserves of brochosomes in the shape of plays the largest contact angle. Redra- wn with modification from JUNIPER Some particular cases of variation in the "wax spots" on the forewings are most com- (1991). development of brochosome coats are consi- monly found in the subfamilies Typhlocybinae stent with these hypothetical functions. Leaf- (VIDANO & ARZONE 1984) and Xestocephali- hopper species occurring in moist habitats nae (RAKITOV 2000b), that contain many often display a better developed, thicker coat. small species. For instance, Erotettix cyane (BOH.), the only Old World leafhopper species known to live 3.4 Protection Against Microbes on floating leaves, differs from most other Del- tocephalinae in being completely coated with Several authors listed protection against a dense, conspicuous layer of brochosomes microbial infection as another possible func- (hence the species name derived from Gr. kya~ tion of brochosomes (MAYSE 1981; NAVONE nos = dark blue) and in having permanent 1987; HlX 2001), but this has not yet been reserves of brochosomes in form of spots on tested experimentally. If proved, it may the forewings (RAKITOV 1995). In Scenergates explain the presence of brochosomes on the viridis (VlLB.), a deltocephaline that develops integument of adult and immature leafhoppers inside of closed (MlTIAEV 1968), the from a wide variety of habitats, as well as on adults are covered with an unusually thick lay- the egg nests. er of brochosomes (personal observation). Like other plant-sucking insects, leafhop- The galls contain a "white waxy substance" pers are not generally susceptible to virus and (MlTIAEV 1968), which is probably the bro- bacteria pathogens, that need to be ingested to chosomes produced by the nymphs. The cause infection. However, they are known to importance of protecting the leafhoppers con- be infected by many species of entomopatho- fined in the closed space of the from their genic fungi (SOPER 1985). Most of these appe- excrement is obvious. Nymphs of the ar to be not specific to Cicadellidae. Natural

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epizootics caused by fungi have been observed with brochosomes. Here they may form a sig- in Cicadella (MITIAEV 1963), and nificant barrier against spores and germ tubes. (ROMBACH et al. 1987), Empoasca The spores trapped in the brochosome coat (GÄLAINI-WRAIGHT et al. 1991), and other may be subsequently removed during groo- leafhoppers (MÜLLER 1956). The entomopht- ming. Zoophthora and some other entomopa- horalean fungus Zoophthora radiums (HUMBER thogenic fungi form specialized passively dis- et al.) has been studied as a control agent of tributed spores, capilliconidia, which secrete Empoasca (McGuiRE 1985; WRAIGHT et al. droplets of viscid fluid at their tips and adhere 1990). to a passing insect (GLARE et al. 1985; Bou- Initial events of fungal infection in insec- CIAS & PENDLAND 1991). As mentioned abo- ts have been reviewed by BOUCIAS & PEND- ve, the layer of brochosomes is repellent to LAND (1991). These include non-specific sticky substances. In this case, as well as in the adsorption of the spore to the insect cuticle, case of the pathogenic spores distributed with host recognition, consolidation of attach- rain splashes, the brochosome coat may provi- ment, germination and growth on the surface de efficient protection. In to germinate and, finally, penetration into the body. Ento- and penetrate the host, the spores require mopathogenic spores range from dry hydro- moist conditions. Natural epizootics of Z. radi- phobic to sticky hydrophilic. They can disper- cans in Empoasca coincided with periods of se by air or by rain splashes, or they will adhe- heavy night dews (WRAIGHT et al. 1991). It is re to a passing insect. Brochosomes may direc- not clear whether the spores require presence tly protect leafhoppers either by containing of films or microdroplets of water on the host substances that inhibit spore germination or integument, but if so, brochosome coats may kill the germ tubes, or as a mechanical barrier play a role in protecting leafhoppers from against the spore attachment and subsequent mycopathogens by preventing condensation penetration. Because moisture is critical for of water on the body surface. germination of most pathogenic fungi, bro- chosomes may also protect leafhoppers indi- 3.5 Resistance to Desiccation rectly by keeping the integument dry. Another possible role of brochosomes is Fungistatic lipids and aldehydes have been the protection against desiccation (ARZONE identified in the cuticle of some insects 1986; HlX 2001). Resisting cuticular transpira- (SMITH & GRULA 1982; SOSA-GOMEZ et al. tion is essential for survival of terrestrial 1997). Hypothetically, similar compounds arthropods, especially those of small size may be present in brochosomes, on the surfa- (HADLEY 1994). It is assumed that the princi- ce or inside. In the latter case, the contents of pal barrier to diffusion is formed by the lipids the particle may be released through the ope- present in the epicuticle. As with certain nings in its wall (Fig. 2). In the last instar waxy paniculate coats (HADLEY 1979, 1994), nymphs of Empoasca, most Z. radicans pene- brochosomes potentially contribute to the trations occur through the abdominal inter- anti-desiccation function of the integument segmental membranes (McGuiRE 1985; either directly, as a lipid-containing mesh- WRAIGHT et al. 1990). These nymphs have on work, or by forming around the integument a their integument only a loose coating of bro- boundary layer of unstirred air. Sealing of chosomes (micrographs in McGuiRE 1985). sutures and intersegmental folds with brocho- Because the spores of the fungus species kno- somes must also reduce water loss. Still ano- wn to infect leafhoppers are 3-100 times larger ther possibility is that brochosomes contain in than ca. 0.4 urn brochosomes found in most their central cavities a lipid, that is released leafhoppers (SOPER 1985) only a dense layer of through the wall openings (Fig. 2) and forms brochosomes is likely to keep the spores far on the integument an impermeable film. enough from the cuticle to prevent their ger- Nevertheless, the ecology of leafhoppers does mination. In leafhoppers that display denser not suggest that desiccation is a crucial factor brochosome coats, grooming often results in for most species. Leafhoppers occur in a caulking the sutures and intersegmental folds variety of habitats, from moist to extremely

420 © Biologiezentrum Linz/Austria; download unter www.biologiezentrum.at dry and, like all plant-sucking insects, receive inocarpi BAKER (Nirvaninae) is completely excessive amounts of water with their food. clothed in a conspicuous layer of unusual On the egg nests of Proconiini, brochosomes brick-red brochosomes (personal observa- may play some role in resisting water loss, but tion). C. F. Baker, who observed live specimens such a function also appears unessential in Singapore, noticed them first as "little red because the eggs are protected with the plant objects, tightly appressed to the surface of the epidermis and, most probably, can absorb leaves" which he "passed for some time, sup- water from the air and the surrounding living posing them to be scale insects affected by a plant tissue, as has been found in other insec- red parasitic fungus, such affected scales being ts (HADLEY 1994). Moreover, the bulk of the common in the gardens" (BAKER 1923, p. Proconiini species that powder their egg nests 378). Further describing the insect, he reports with brochosomes occur in the wet tropics of that "it is thickly covered with brick red waxy the New World (RAKITOV 1999b), where the powder which does not rub off easily" and that risk of desiccation is reduced. the color of the insect is "almost exactly that of the common scale fungus". This anecdote emphasizes the versatility of the brochosome 3.6 Other Protective Functions coats and suggests that disentangling the pri- It has been suggested that brochosomes mary function of brochosomes from their may also serve as a thermal insulation or as a accessory functions may be a difficult task. layer reflecting the excessive sunlight, especi- ally in the ultraviolet part of the spectrum (NAVONE 1987; Hix 2001). Brochosome coats 3.7 Brochosomes and Pheromones are apparently too thin to buffer fluctuations The unusual and complex shape of bro- of temperature. However, they indeed reflect chosomes may be indicative of an equally UV light (RAKITOV unpublished). This pro- complex function, such as the accommodati- perty and the protection from excessive heat on of pheromones (DAY 1993). When inside may be beneficial for some desert leafhoppers the secretory cells, brochosomes are filled with densely coated with brochosomes (e.g. Achrus an electron-transparent liquid substance ahngeri (MEL.), Adelungiinae — RAKITOV (SMITH & LITTAU I960; GOURANTON & 1995). Neither excessive sunlight nor heat, MAILLET 1967; RAKITOV 1999a, 2000a). however, appear to be principal hazards for the Apparently the same substance fills the space majority of leafhoppers. between brochosomes in the secretory vacuo- Brochosome coats are too thin to mecha- les. Whether this liquid simply evaporates nically deter predators or parasites. The possi- when brochosomes are placed onto the inte- bility of chemical deterrence, however, merits gument is uncertain. DAY (1993) has sugge- future study. As a group, leafhoppers have a sted that the particles carry a that large suite of parasites (FREYTAG 1985). Many slowly evaporates through the openings in the such species parasitize both leafhoppers and wall compartments (Fig. 2). However, it is occurring in the same habitat unlikely that brochosomes contain a sex (e.g., GREATHEAD 1983; SUBBA RAO 1983). It pheromone because, in many species, they are seems unlikely that such have produced and applied on the body by the evolved specific mechanisms of overcoming immatures as well as the adults of both sexes. the brochosome barrier and still retained a In general, there is no evidence that Cicadel- broad range of the host taxa. More probably, lidae produce any kind of pheromones (for dis- this barrier is not difficult to overcome. The cussion about sex pheromones in other brochosome-coated egg nests of Proconiini are Hemiptera see ALDRICH 1996). "Brochoso- also attacked by numerous parasitoids (TRIA- mes-for-eggs" may prevent females from repea- PITSYN et al. 1998; TRIAPITSYN & PHILLIPS ted oviposition into the same place (HlX 2000). 2001) by releasing a pheromone, but in this In some exceptional cases brochosomes situation the visual signal alone would seem to may serve as masquerade make-up. Stenotortor be enough.

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4. Brochosomes and Wax: hoppers to the behaviors of two unrelated Evolutionary Convergences groups of small insects that actively coat their integument with waxy particles: whiteflies 4.1 Participate Waxes (Hemiptera, Aleyrodidae) and dustywings The epicuticle of insects includes a thin (, , also known as layer of wax which forms the exposed surface "waxflies"). Freshly eclosed adults or lies under a still thinner cement layer, scrape off minute chunks of wax from the depending on the species (CHAPMAN 1998). abdominal fields of wax glands with the legs This wax is produced by specialized epidermal and distribute them over the entire surface of cells and is released across the deeper cuticular the body and appendages; the process is assi- layers through a system of canals. As a modifi- sted by rows of strong setae present on the legs cation of this basic process, in some insects, (see also WEBER 1931; BYRNE & HADLEY the epidermal glandular cells or their comple- 1988). Adult dustywings use their legs to make xes secrete an extracuticular wax in form of on the integument a coat of microscopic waxy particles or filaments. Although such particu- particles produced by scattered groups of epi- late waxes can be found among certain species dermal glands. The waxy coats, waxing beha- of , Neuroptera, Coleoptera, Lepid- viors and, in the case of whiteflies, leg modifi- optera, or , they are especially cations are remarkably similar to the brocho- common and diverse in Hemiptera. Especially some coats and related behaviors and structu- copious amounts of wax are produced by some res of leafhoppers. Moreover, the waxy par- and Fulgoromorpha: scale ins- ticles, although larger than typical brochoso- ects (FOLDI 1991), aphids (POPE 1983; SMITH mes (1.3-3.0 urn), also display an intricate sur- 1999), psyllids (HODKINSON 1974), whiteflies face geometry (NAVONE 1987). (NAVONE 1987; BYRNE 6k HADLEY 1988; NELS- ON et al. 1999), and planthoppers (Figs 24-28) 4. 3 Functions of Body Wax (O'BRIEN & WILSON 1985; MASON et al. The function of the particulate waxy 1989). The hemipteran waxes are mixtures secretions is poorly understood in most that may contain long-chained aldehydes, instances. Only the waxy blooms of some alcohols, esters of alcohols and fatty acids, free desert tenebrionid have been studied fatty acids, or hydrocarbons, depending on the in some detail from an adaptive perspective species and location in the body (MASON et al. (HADLEY 1979; MCCLAIN et al. 1985, 1986; 1989; FOLDI 1991; BUCKNER et al. 1999; NELS- WARD & SEELY 1996). No detailed studies of ON et al. 1999). Brochosome coats of leafhop- the properties, except structural and chemical, pers have often been confused with extracuti- and function of the hemipteran waxes have cular waxes (VlDANO & ARZONE 1984), and been conducted. Functional interpretations of this contributed to the delay in the recogniti- such secretions are mainly derived from com- on and study of brochosomes. Brochosomes parisons between life histories of the species differ from the epidermal waxes in their gene- producing copious wax and those that produ- sis, composition, and structure. Nevertheless, ce little or no wax. It is remarkable that all of both waxes and brochosomes form highly the hypothetical functions proposed for bro- hydrophobic particulate coatings that may chosomes have also been proposed for waxes. have similar functions. Hemipteran waxes have been suggested to be waste products associated with the phyto- 4.2 Waxing Behaviors phagy (POLLISTER as cited in POPE 1983, The apparent functional analogy between p. 495). Somewhat surprisingly, the possible brochosomes and particulate waxes was noted connection between the nutrition and pro- by NAVONE (1987) in his study "Origin, struc- duction of wax in Hemiptera has not been ture, and functions of insect excretions and investigated. Some of the long-chained mole- secretions, of a waxy aspect, distributed on the cules in the waxes are apparently synthesized body by means of legs". Navone has compared from smaller subunits by the insects themsel- the anointing and grooming behaviors of leaf- ves (JACKSON & BLOMQUIST 1976). Still it

422 © Biologiezentrum Linz/Austria; download unter www.biologiezentrum.at remains unclear whether the precursors of ting radiation and, in some species, yields a such molecules are abundant in plant . The cryptic coloration (MCCLAIN et al. 1985,1986). fact that in the family The correlation between aridity of the habitat the nymphs, feeding on decaying wood or fun- and presence of wax blooms in the Ony- gi, produce copious wax like the nymphs of macris has been tested statistically in a phyloge- other planthoppers (HEPBURN 1967) suggests netic framework (WARD & SEELY 1996). The that feeding on living plant saps is not requisi- mechanism by which die blooms reduce tran- te for wax secretion. Other proposed hypothe- spiration is not fully clear. HADLEY (1979) sug- tical roles of the hemipteran extracuticular gested that the actual barriers may be either the waxes include protection from contamination meshwork of filaments itself or the layer of with honeydew and wetting with water, from unstirred air between these and the cuticle. fungal pathogens, desiccation, parasites and However, he also pointed out that the filaments predators, excessive heat, and harmful radiati- eventually "dissolve" into the epicuticular wax on (HODKINSON 1974; POPE 1983, 1985; and contribute to its thickness. It seems possible NAVONE 1987; BYRNE & HADLEY 1988; FOLDI that this increase of the epicuticular wax layer 1991; SMITH 1999). It has also been suggested at least partly accounts for the observed reduc- that the wax particles produced in whiteflies tion in water loss, and that the secretion of wax contain a sex pheromone (BYRNE & HADLEY blooms may also be a mechanism to restore this layer that becomes abraded when the insects 1988). burrow into the sand. The waxy blooms of The role of the particulate waxes in pro- Hemiptera may also reduce transpiration from tection from honeydew in many cases appears the integument surface, but such a function can consistent with the biology of the wax-produ- hardly explain secretion of wax by a great many cers. Indeed, the vast majority of the Hemip- species living in mesic or humid environments tera producing copious wax are phloem-fee- and receiving an excess of water from plant sap. ders excreting sticky honeydew. Some species of Coniopterygidae (but not all) are speciali- zed predators of such hemipterans and may 4.4 Wax on Eggs also benefit from a barrier against honeydew. Many insects that produce extracuticular In some aphids and planthoppers, a copious wax use it also to coat their eggs. Examples waxy bloom surrounds the anal body end. include whiteflies (WEBER 1931; NAVONE Excessive production of wax is observed in 1987), some aphids (SMITH 1999), and Coni- gall-inhabiting aphids that cannot avoid opterygidae (NAVONE 1987). In some whitef- direct contact with their sticky wastes (SMITH lies, the wax that is used to powder the eggs 1999). On the other hand, -attended spe- differs in its composition from the body coat cies, from which the honeydew is removed by wax and is produced by special fields of wax , often produce little wax compared to glands that are present in females only (NEL- unattended species. The waxy secretions are SON et al. 1999). In all above cases the eggs are extremely hydrophobic (FOLDI 1991; SMITH laid exposed. Proposed functions of such wax 1999). As in the case of brochosomes, this coatings are the same as for the other life sta- may be explained in part by the intricate sha- ges: protection from desiccation, flooding, pe of the wax particles; masses of such par- harmful radiation, fungal infection, predators, ticles form a finely sculptured, composite sur- and parasites. There is a close similarity bet- face capable of holding air. Large accumulati- ween the egg laying habits of leafhoppers, that ons of wax (Fig. 24) may act as a simple usually insert eggs into plant tissues, and some mechanical barrier. planthoppers (Fulgoromorpha). Planthoppers, In response to low humidity some desert as a group, demonstrate a variety of ovipositi- tenebrionid beetles secrete a filamentous waxy on techniques and often also coat the egg bloom that slightly reduces die transpiration nests with wax (reviewed in O'BRIEN & WlL- rate and is interpreted as a barrier against desic- SON 1985). Some species insert eggs into cation (HADLEY 1979). The bloom apparently living plants and powder the egg scar with also plays a role in diermoregulation by reflec- wax. This behavior closely resembles the ovi-

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position behavior of the Proconiini leafhop- egg scar and the surrounding epidermis pers that powder their egg nests with brocho- (Fig. 25). The completed egg nests were conspi- somes (Figs 15-18). In Illinois, I observed cuous due to the powdery coats (Fig. 26), that females of sp. () lay- consisted of broken wax filaments with a hig- ing groups of several eggs into the blades of hly complex surface structure (Figs 27-28). In Cyperus esculentus L. After inserting each egg another delphacid species, to place wax onto the female brushed the ventral side of the the egg scars, females use their hindlegs (MET- abdomen tip against the plant, rubbing the CALFE 1968). As with the brochosome coats of copious wax produced on the pygofer into the egg nests, the function of these coatings may

Figs 24-28. Secretion and use of wax in planthoppers. Fig. 24. A 5th instar nymph of Anormenis sp. () is barely visible under the "cot- ton candy" of wax it has produced. The wax also covers the nearby parts of the host plant stem. Fig. 25. Female Steno- cranus sp. (Delphaci- dae) coating her eggs, inserted into a blade of Cyperus, with the wax secreted on its pygofer. She is rubbing the ven- tral surface of the abdomen end, where a white mass of wax is visible, against the egg scar and the surroun- ding plant epidermis. Fig. 26. The completed oviposition site of 5fe- nocranus sp. The eggs are not visible under the plant epidermis and wax. Fig. 27. Rods of wax from the egg nest of Stenocranus sp. Bar = 1um. Fig. 28. Close-up of one such rod reveals an extraordinarily com- plex surface structure. Bar = 1um.

424 © Biologiezentrum Linz/Austria; download unter www.biologiezentrum.at be the protection of the egg scar from flooding 5. Brochosomes and with plant fluids (to aerate the eggs) and the Evolution of Cicadellidae protection against infection of the wound with phyto- and entomopathogenic microbes. Brochosomes are a tentative apomorphy of Remarkably, in both Cicadellidae and Delpha- Cicadellidae (DIETRICH et al. 2001). Conela- cidae only a few species coat their egg nests ting the origin of the family with certain shifts with the paniculate materials. Further compa- in the life history or habitat may shed light rative studies of the ecology of oviposition upon the primary function of brochosomes. and, perhaps, of the respiratory systems of the Relationships between the extant leafhopper eggs in the two families may shed light upon taxa that display variation in the brochosome- the adaptive significance of these unusual related traits may also provide necessary clues. maternal behaviors. Evolution of the major cicadomorphan lineages—Cercopoidea (spittlebugs), Cica- doidea (), and Membracoidea (leaf- 4.5 Leafhoppers: Brochosomes hoppers and treehoppers)—has been reviewed Instead of Wax? by DIETRICH (this volume). Synthetic modifi- Among , conspicuous amo- cations of the Malpighian tubules are charac- unts of paniculate body wax are produced in teristic of all the three lineages (RAKITOV in cicadas (Cicadoidea) and certain treehoppers press). In spittlebugs and cicadas, the tubules (Membracidae). No species of Cicadellidae is synthesize and export secretory products known to secrete copious wax, which is remar- during the nymphal stage only. Such products kable given the extreme diversity of the fami- are released with the main flow of excreta. In ly. This pattern is consistent with the hypo- spittlebugs they make a part of the nymphal thesis that brochosomes and waxes have a "spittle", and in cicadas a part of the "anal similar function. At the same time, small liquid" that is used to strengthen the walls of amounts of particulate wax have been found the nymphal burrows and clean the body. Pro- in some leafhopper species (RAKITOV 1995). duction of secretory products in the Malpighi- In particular, the integuments display a thin an tubules and their application on the inte- particulate waxy coating in the nymphs of cer- gument may, therefore, be plesiomorphic traits tain species from Macropsinae, Idiocerinae, of Cicadomorpha. I have conjectured (RAKI- TOV in press) that the nymphs of early cicado- Typhlocybinae, and in nymphs and adults of morphans were subterranean and xylem-fee- lassus, all of which apparently do not produce ding, and that their Malpighian tubules were brochosomes. Very small amounts of wax have modified to synthesize products that possibly also been found on certain body parts of sever- prevented the growth of fungi in the soil moi- al species known to produce brochosomes stened with the nymphal excretion, neutrali- (e.g., in Oncometopia, , ), zed toxic waste products contained in the suggesting that this secretion can sometimes nymphal excretion, or optimized the pH of the coexist with brochosomes. Further studies will substrate. The integument of such nymphs was probably find microscopic quantities of the coated with their own liquid excreta and particulate wax in more leafhopper species. secreta, as in modern spittlebugs. In the linea- The incidental coexistence of brochosomes ge leading to the extant Membracoidea, the and wax does not necessarily dismantle the nymphs switched from cryptobiosis to the hypotheses of functional similarity between open and agile life style. Apparently, they these secretory products. It should be noted, retained the habit of applying the Malpighian however, that the apparent absence of wax in tubule products on the integument instead of leafhoppers may have explanations other than developing protective extracuticular waxy substitution with brochosomes. The absence coatings. Anointing behavior, therefore, may of massive waxy blooms (as in Fig. 24) in leaf- have evolved before the origin of brochoso- hoppers is clearly related to their agility: leaf- mes, and its original function might have been hoppers can escape certain hazards actively different from that in extant leafhoppers. Bro- instead of relying on the passive protection. chosomes or their precursors are not known in

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the record. However, the imprints of the 2001). This clearly indicates that the use of earliest known membracoids, Karajassidae brochosomes in oviposition is a derived trait. from the (SHCHERBAKOV 1992), show Preliminary results suggest that the egg nest rows of tibial macrosetae that may have served powdering is an apomorphy of a single lineage for distribution of a paniculate material over within Proconiini that contains ca. 200 integument, as in modern Cicadellidae (RAKI- described species (RAKITOV 1999b). TOV 1998). Treehoppers (, Melizoderi- Among modern Cicadellidae, brochoso- dae, and Membracidae) have apparently ari- mes have been found in all of the major subfa- sen from within Cicadellidae and lost the milies (RAKITOV 1995, 1998), suggesting that capability of synthesizing brochosomes secon- extant "pre-brochosomic" leafhoppers may darily (RAKITOV 1998; DIETRICH et al. 2001). not exist. Xylem-feeding, displayed among the Nymphs of Membracidae share a specific type extant leafhoppers by Cicadellinae (sensu of anointing—"bathing" in the brochosome- lato) only, is considered to be a plesiomorphic free Malpighian tubule secretions—with nym- trait shared with cicadas and spittlebugs (e.g., phs from the subfamilies Macropsinae, Ulo- HAMILTON 1983). Such a diet results in pro- pinae, and Agalliinae that represent a sister duction of copious watery, non-sticky excreta. lineage of treehoppers (RAKITOV 1996; DlE- The fact that Cicadellinae produce brochoso- TRICH et al. 2001). This indicates that during mes suggests that this secretion evolved befo- the evolution of treehoppers the production of re the more advanced leafhopper lineages brochosomes was first lost by the immatures switched to phloem-feeding and, therefore, and later by the adults. These changes may be that protection from sticky honeydew could related to ant-, that is frequently observed among plesiomorphic treehoppers not be its original function. Relationships and sometimes in the related subfamilies of among the extant Cicadellidae are only partly leafhoppers (DIETRICH this volume). Other resolved (DIETRICH et al. 2001). However, the life-history traits of treehoppers that may cor- subfamilies that contain species not producing relate with the absence of a brochosome coat brochosomes at the nymphal stage (Macrop- are the sedentary life style, gregariousness, and sinae, Idiocerinae, Ulopinae, and Typhlocy- . binae) appear to be advanced lineages, sug- gesting that production of brochosomes during both the nymphal and adult stages is a plesio- 6. Conclusion and morphic trait. Perspectives

The variation of brochosome structure Available evidence suggests that the most among leafhoppers gives little indication of likely role of brochosomes in Cicadellidae is evolutionary trends. One type of brochoso- that of a protective coating that (1) repels mes, 0.3-0.6 jjm spherical honeycombs found water and sticky honeydew and/or (2) pre- in the majority of studied species from a vents fungal infection. These hypothetical variety of subfamilies (Fig. 2) (RAKITOV 1995, functions are generally consistent with the 1999a), may represent a plesiomorphic type. biology of leafhoppers and at least partly rela- "Brochosomes-for-eggs", produced by females ted to the peculiar structure of brochosomes. of certain Proconiini genera, are usually elon- Similar functions are performed in other ins- gate and significantly larger than "brochoso- ects by the epidermis and its derivatives, in mes-for-integument" (Fig. 18) (RAKITOV particular, waxes. The apparent functional 1999b and unpublished; Hix 2001). These substitution of epidermal waxes with the Mal- properties may facilitate storing the particles pighian tubule secreta may have been associa- on the forewings and transferring them onto ted with the cryptic life mode of the immatu- the egg nests. Masses of larger particles may res in early Cicadomorpha and related physio- also ensure better access of air to the eggs. At logical and behavioral constraints. Inadequate the earlier stages, the same females produce knowledge of the properties of brochosomes and apply onto the body typical "brochoso- makes these functional interpretations highly mes-for-integument" (RAKITOV 2000a; HlX speculative.

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A variety of approaches may contribute to chosome coat (e.g., in Nionta, Figs 19, 20). defining the function of brochosomes. First, Other insights may be gained by study of the biochemical studies of brochosomes are nee- brochosome coats of the leafhopper species ded to clarify the relation between this secre- inhabiting contrasting environments. Such tion and the metabolism of leafhoppers. They studies should take phylogeny into account to would also provide additional hints regarding correct for its effects on the distribution of the the function of brochosomes. Brochosomes observed characters (e.g., WARD & SEELY need to be isolated, purified, and studied by 1996). Phylogenetic methods will also be modern analytical methods, and their compo- instrumental in elucidating the causes of sition should be compared between species as secondary losses of the brochosome produc- well as between "brochosomes-for-integu- tion, that apparently occurred independently ment" and "brochosomes-for-eggs". Of special multiple times. Development of techniques interest is the inner contents of the particles for quantification of brochosomes on the body because, as was pointed out by DAY (1993), of individual leafhoppers will be important for the secret of brochosomes may be in their fil- all kinds of functional studies. Comparative ling. In addition, the nature of the alternative ultrastructural studies are needed to find out Malpighian tubule products, found in certain whether the presence of brochosome coats in leafhopper nymphs and in Membracidae, leafhoppers correlates with some modificati- should be studied to clarify the relationship ons of their epicuticle. Finally, studies of bro- between such products and brochosomes, and chosomes and related aspects of the leafhop- to elucidate the function of the brochosome- per biology should be extended to additional free anointing behaviors. Anti-microbial pro- taxa, including little-known groups, particu- perties of brochosomes also need to be tested. larly , thought to be the most Such tests should employ a representative plesiomorphic family of the extant Membra- sample of known fungal pathogens of Hemip- coidea (HAMILTON 1999). tera, including species with different modes of distribution and attachment of propagules Future studies may uncover functions of (SOPER 1985; BOUCIAS &. PENDLAND 1991). In brochosomes different from any of the hypo- the design of these experiments, special care thetical roles discussed above. One of the should be taken to separate potential direct challenges for such studies is the apparent and indirect effects of brochosomes. Wettabi- multifunctionality of the brochosome coats, lity, contaminability, and other surface pro- characteristic of all structures that form an perties of brochosome layers also await experi- interface between an organism and the envi- mental study. In particular, it would be inte- ronment. Testing and confirming any of the resting to know which physical properties cor- functions discussed above may not be suffi- relate with the variation in size, shape, and cient to conclude that it is the primary and sculpture of brochosomes observed among original function of brochosomes. Therefore, leafhopper species. As with the microbiologi- functional interpretation of brochosomes will cal assays, such studies may be conducted on only be possible within a broader context of intact leafhoppers, denuded "brochosome- comparative and experimental studies. free" leafhoppers (obtained by impeding anointing behavior, RAKITOV unpublished), and substrates artificially coated with brocho- 7. Acknowledgments somes. Valuable insights into the function of brochosomes can also be derived from behavi- I am grateful to Dr. C.H. Dietrich and oral observations. Of particular interest are D.M. Takiya (Illinois Survey) the frequency and duration of anointing and for their valuable discussion and comments on grooming in relation to certain environmental the manuscript, and Dr. D.E. Shcherbakov parameters, e.g., humidity. Laboratory studies (Paleontological Institute, Russian Academy of these behaviors may help explain individu- of Sciences) for his earlier discussion of the al variation in the development of the bro- subject.

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7. Zusammenfassung References Cited

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Address of the author:

Dr. Roman RAKITOV Illinois Natural History Survey 607 E. Peabody Dr. Champaign, IL 61820 U.S.A. E-mail: [email protected]

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