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Anatomy, Ultrastructure, and Functional Morphology of the Metathoracic Tracheal Defensive Glands of the Grasshopper Romalea Guttata

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Anatomy, Ultrastructure, and Functional Morphology of the Metathoracic Tracheal Defensive Glands of the Grasshopper Romalea Guttata Anatomy, ultrastructure, and functional morphology of the metathoracic tracheal defensive glands of the grasshopper Romalea guttata DOUGLASW. WHITMAN Department of Biological Sciences, Illinois State University, Normal, IL 61 761, U. S.A. JOHANP. J. BILLEN Zoological Institute, University of Leuven, B-3000 Leuven, Belgium DAVIDALSOP Department of Biology, Queens College, Flushing, NY 11367, U.S.A. AND MURRAYS. BLUM Department of Entomology, University of Georgia, Athens, GA 30602, U. S. A. Received January 4, 1991 WHITMAN,D. W., BILLEN,J. P. J., ALSOP,D., and BLUM,M. S. 1991. Anatomy, ultrastructure, and functional morphology of the metathoracic tracheal defensive glands of the grasshopper Romalea guttata. Can. J. Zool. 69: 2100-2108. In the lubber grasshopper Romalea guttata, the respiratory system produces, stores, and delivers a phenolic defensive secretion. The exudate is secreted by a glandular epithelium surrounding the metathoracic spiracular tracheal trunks. Embedded in the glandular tissue are multiple secretory units, each comprised of a basal secretory cell and an apical duct cell. Secretory cells have numerous mitochondria, a tubular, smooth endoplasmic reticulum, well-developed Golgi bodies, and a microvilli- lined vesicle thought to transfer secretion to the intracellular cuticular duct of a duct cell. Ducts empty into the metathoracic tracheal lumina where the exudate is stored behind the closed metathoracic spiracle. Tactile stimulation elicits secretion discharge, which,begins when all spiracles except the metathoracic pair are closed and the abdomen is compressed. Increased hemostatic and pneumatic pressures drive air and secretion out of the spiracle with an audible hiss. Both metathoracic spiracles discharge simultaneously. The secretion erupts first as a dispersant spray, then as an adherent froth, and finally assumes the form of a slowly evaporating repellent droplet. Discharge force and number vary with eliciting stimuli, volume of stored secretion, and age, disturbance state, and temperature of the insect. Molting grasshoppers are unable to discharge because the stored exudate is lost with the shed cuticle. The advantages and limitations of a tracheal defensive system are discussed. WHITMAN,D. W., BILLEN,J. P. J., ALSOP,D., et BLUM,M. S. 1991. Anatomy, ultrastructure, and functional morphology of the metathoracic tracheal defensive glands of the grasshopper Romalea guttata. Can. J. Zool. 69 : 2100-2108. Chez le criquet Romalea guttata, le systkme respiratoire produit, emmagasine et tmet une stcrttion phtnolique de dtfense. Cette exsudation est stcrttte par l'tpithtlium glandulaire qui entoure les trachtes des stigmates mttathoraciques. De nombreuses unitts stcrttrices sont enfouies dans le tissu glandulaire et chacune est constitute d'une cellule basale stcrttrice et d'une cellule apicale canaliculaire. Les cellules stcrttrices comportent de nombreuses mitochondries, un rtticulum endoplasmique agranulaire tubulaire, des appareils de Golgi kndtveloppts et une vtsicule tapisste de microvillositts que l'on croit servir au transfert des stcrttions au canal cuticulaire intracellulaire d'une cellule canaliculaire. Les canaux se vident dans la lumikre de la trachte mttathoracique et la stcrttion s'accumule denikre le stigmate mttathoracique fermt. La stimulation tactile dtclenche le rejet de la stcrttion; au moment du rejet, tous les stigmates sont fermts, l'exception de la paire mttathoracique, et l'abdomen est comprimk. L'augmentation des pressions htmostatique et pneumatique poussent l'air et la stcrttion au-dehors par le stigmate avec un sifflement perceptible. Les deux stigmates mttathoraciques se vident simultantment. La stcrttion sort d'abord cornrne un jet de vapeur, puis sous forme de mousse collante, et finalement sous forme d'une gouttelette rtpulsive qui s'tvapore lentement. La force des Cmissions et leur nombre varient en fonction des stimulus dtclencheurs, du volume de stcrttion emmagasinte, de l'ige, du degrt d'agitation et de la temptrature de l'insecte. Les criquets en ptriode de mue sont incapables d'tmettre des stcrttions parce que les stcrttions accumultes sont rejettes avec la cuticule. Les avantages et les dtsavantages d'un systkme de dtfense trachten font l'objet d'une discussion. [Traduit par la rtdaction] Introduction through the metathoracic spiracles (Fig. 1) with an audible hiss Only two groups of animals possess a respiratory-derived (Morse 1907; Duncan 1924; Roth and Eisner 1962). chemical defensive system. Certain blaberid cockroaches eject The products of these tracheal glands have been studied only a defensive secretion from the second pair of abdominal in R. guttata. In this species, the water-based secretion is spiracles (Roth and Stay 1958), and two closely related spe- exceedingly complex, containing over 50 compounds. Major cies of New World romaleid grasshoppers, Romalea guttata constituents are synthesized de novo and include phenolics, ( = microptera) and Taeniopoda eques (Rhen and Grant 1959, quinones, and an allenic sesquiterpenoid, romallenone (Mein- 1961), possess a thoracic defensive mechanism. In both wald et al. 1968; Eisner et al. 1971; Jones et al. 1986). Other grasshopper species, the tracheal trunks leading to the meta- constituents are obtained from the diet (alkyl sulfides from thoracic spiracles are specialized for the storage and discharge wild onion and nepetalactone metabolites from catnip) (Jones of secretion produced in an overlying glandular epithelium. et al. 1989; Blum et al. 1990). Man-made compounds may be During predator encounters, the secretion is forcibly ejected sequestered as well; the herbicide breakdown product, 2,5 - Printed in Canada 1 ImprimC au Canada WHITMAN ET AL. 2101 postero-directed nerves exiting the metathoracic ganglion were severed. Two days later, six operated and six sham-operated individ- uals were each squeezed at the head and the degree of abdominal contraction and secretory discharge was noted. For anatomical studies grasshoppers were killed or immobilized by refrigeration and dissected under Ringer's solution. For light micros- copy studies, grasshopper tracheae were fixed in alcoholic Bouin's (Brasil's) fluid and stained with haematoxylin and eosin. For trans- mission electron microscopy studies, the tracheal glands of cold- anesthetized grasshoppers were dissected and immediately fixed in cold 2% glutaraldehyde, buffered with 0.05 M sodium cacodylate (pH = 7.3) in 0.15 M sucrose. After postfixation in 2% osmium tetroxide in the same buffer, tissues were dehydrated in a graded acetone series and embedded in AralditeB. Thin sections from both sexes were stained with uranyl acetate followed by lead citrate, then examined with a Philips EM 400 electron microscope. Semithin sections stained with thionin and methylene blue were also examined by light microscopy. To investigate stimuli influencing secretion release, we performed the following routine on 40 adult ground-foraging grasshoppers encountered in the field between 13:00 and 15:OO (T,,, -30°C): the experimenter (i) advanced to within 30 cm of grasshopper; (ii) rapidly moved an open hand toward grasshopper (five times in 10 s); (iii) lightly touched grasshopper (five times in 10 s); (iv) roughly poked insect, knocking it off balance (five times); (v) held insect and squeezed one antenna; (vi) held insect and squeezed one front leg; (vii) squeezed head; and (viii) squeezed insect's anterior abdomen. All grasshoppers received all eight stimuli, and approximately 5 s separated different stimuli. Any secretion discharge was recorded. Molting, mating, and ovipositing adults were also disturbed by squeezing their thoraces or heads. For volumetric studies, discharge was collected into capillary tubes and measured. Results The respiratory system of Romalea guttata, as in other grasshoppers (Uvarov 1966), consists of 10 pairs of spiracles and various interconnecting tracheae, air sacs, and tracheoles. FIG. 1. Foamy defensive secretion emerging from Romalea guttata Each spiracle possesses a sclerotized or membranous valve metathoracic spiracles. serving to regulate air flow into and out of the body. The spiracles differ in size, gegree of sclerotization, and develop- dichlorophenol was reported to occur in the secretion of ment of a surrounding cuticular plate (peritreme) (Fig. 2). The Romalea (Eisner et al. 1971). anterior mesothoracic spiracles (Ms) are the largest and are The phenolic products of Romalea tracheal glands are well- hidden from view beneath the posteroventral flanges of the known defensive agents in both plants and arthropods (Blum prothorax. They are located in a membranous field immediately 198 1; Rodriquez et al. 1984). The secretion from,Romalea anterior to the sclerotized anterior border of the mesopleuron, repels ants (Eisner et al. 1971; Jones et al. 1987), and the have well-sclerotized spiracular valves, and a large, posteriorly secretion of the related T. eques is repellent to grasshopper directed protuberance (P) that presumably prevents occlusion mice (Whitman et al. 1985). The metathoracic secretions of of the spiracular opening by the overlying pronotum (Fig. 3). both Taeniopoda and Romalea females also function as con- The metathoracic spiracles (Mt) are slightly smaller than the tact sexual pheromones, eliciting mating behavior in males mesothoracic spiracles and are located directly above the (Whitman 1982; D. W. Whitman, unpublished data). mesocoxal cavities. They lack a protuberance and are situated Although the composition and function
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