What Are Brochosomes For? an Enigma of Leafhoppers (Hemiptera, Cicadellidae) 411-432 © Biologiezentrum Linz/Austria; Download Unter
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ZOBODAT - www.zobodat.at Zoologisch-Botanische Datenbank/Zoological-Botanical Database Digitale Literatur/Digital Literature Zeitschrift/Journal: Denisia Jahr/Year: 2002 Band/Volume: 0004 Autor(en)/Author(s): Rakitov Roman Artikel/Article: What are brochosomes for? An enigma of leafhoppers (Hemiptera, 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 honeydew. Another pos- of early Membracoidea 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, evolution. Neue Folge Nr. 176 (2002), 411-432 411 © Biologiezentrum Linz/Austria; download unter www.biologiezentrum.at 1. Introduction immatures and adults of the same species (STOREY & NICHOLS 1937; NAVONE 1987; Leafhoppers (Cicadellidae) can he charac- RAKITOV 1996, 2000b). An adult leafhopper 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 subfamilies, that do not produce bro- over the ventral body surface and appendages; chosomes until the last instar, 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- Auchenorrhyncha and insects 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 family 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 years 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 Draeculacephala 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 leaf- hoppers they are hollow spheres, 0.2-0.6 urn in Fig. 2. A brochosome of Paraphlepsius 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 Oncopsis 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. Exitianus 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 Typhlocybinae. 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). 413 © Biologiezentrum Linz/Austria; download unter www.biologiezentrum.at 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, Ulopinae, 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.