Ultrastructure of the excretory tubes of the miteMacrocheles muscaedomesticae (Mesostigmata, Macrochelidae) with notes on altered mitochondria

Reprinted from THE JOURNAL OF MORPHOLOGYVol. 133, No.3, March 1971 @ The Wistar Institute Press 1971

37

Ultrastructure of the Excretory Tubes of the MiteM aClocheles m uscaedomesticae ( Mesostigmata,Macrochelidae) with Notes onAltered Mitochondria

JLEWIS B. COONS AND RICHARDC. AXTELLDepartment of Entomology, North Carolina State University,Raleigh, North Carolina 27607

ABSTRACT The fine structure of the excretory tubes of the mesostigmatidmite Macrocheles muscaedomesticae were investigated. These paired tubes arepartially ensheathed by fat body and invested throughout by a branching systemof visceral muscles. The fine structure of the cells of the excretory tube is ingeneral similar with only minor differences found throughout its length. Thebasal region of each epithelial cell of the excretory tube borders the hemocoeland is divided into many compartments by the extensive infolding of the plasmamembrane. Mitochondria and vacuolar inclusions are often closely associatedwith these compartments. More than one morphological type of mitochondriawas found distributed throughout the cells of the excretory tubes. The most com-monly encountered type had well developed cristae and an electron dense matrix.Less commonly, mitochondria with somewhat poorly developed cristae and atranslucent matrix often containing myelin-like figures of varying complexitywere observed. It is suggested that they represent part of a normal process ofmitochondrial degeneration. The apical region of the cell has a border composedof plate-like folds of the plasma membrane termed microlamellae. The lumencontains abundant granules of the excretory product.

.

Aside from the insects, the mites are themost widely diversified group of arthropodswith respect to habitat. They have adaptedto a wide variety of environmentalcondi-tions. This has resulted in several differentapproaches to the problem of nitrogenouswaste removal. Three types of excretory or-gans are found within the Acarina: coxalglands, excretory tubes, and, in the Trom-bidiformes, a modified hindgut (Baker andWharton, '52). Excretory tubes that openinto the hindgut, such as found in theMacrochelidae, are the most common typeof excretory organ.

This paper presents the results of an ul-trastructural study on the excretory tubesof Macrocheles muscaedomesticae (Sco-poli), a free living terrestrial mite thatfeeds on the eggs of the housefly, Muscadomestica L. This mite has a number offeatures advantageous to this type of study.It is a relatively large mite (about 1.1 mmin length), is easily reared in large num-

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J. MORPH., 133: 319-338.

bers in the laboratory, and is a representa-tive of free living mesotigmatid mites andis less specialized than many of the para-sitic forms.

MATERIALS AND METHODS

Mites used in this study were obtainedfrom laboratory cultures mass reared inplastic dishes in a substrate of fresh cowmanure mixed equally with CSMA mediumwhich had been used to raise housefly lar-vae. Colonies were fed a mixture of house-fly eggs, previously frozen to prevent hatch-ing, and the nematode, Rhabditella leptura.This procedure has been adapted fromRodriguez, Wade and Wells ('62).

The small size and hard exoskeleton ofthis mite, which prevents penetration offixatives, necessitated the development ofa microdissection technique that would in-sure proper fixation of the excretory tubesand yet allow them to be removed intact.This enabled all areas of the tubes tobe

319

320 LEWIS B. COONS AND RICHARD C. AXTELL

studied in a more precise manner. For thistechnique mites were immobilized in sten-dor dishes by carefully melting, with a hotneedle, a small amount of paraffin aroundeach leg. Mites appearing moribund wererejected. The remaining mites were thenprechilled for about 30 minutes (Pease,'64) and flooded with fixative consisting of2.5% glutaraldehyde in a 0.05 M sodiumcacodylate buffer (pH 7.2) containing0.15 M sucrose. Using microscalpels madefrom razor blades and electrolyticallysharpened tungsten wire probes (Brady,'65), the dorsal shield of each mite wasremoved and the internal organs exposed.After an initial half hour period of fixa-tion, the excretory tubes were dissectedout. They were immediately cut into sev.eral smaller pieces, and placed in freshglutaraldehyde fixative for one to twohours. The tissue was then washed in thesodium cacodylate buffer containing 0.30 Msucrose for four to eight hours and post-fixed in 1% osmium tetroxide in veronalacetate buffer (pH 7.2) containing 0.30 Msucrose. Following postfixation, the tissuewas dehydrated in a graded series of ethylalcohols. After three changes of propyleneoxide, the tissue was infiltrated and em-bedded in Epon 812 according to the meth-od of Luft ('61). All steps in this procedureprior to dehydration in absolute ethyl alco-hol were carried out at a temperature offrom 2° to 6°C.

Histochemical localization of acid phos-phatase at the fine structural level was ac-complished using a Gomori medium. Theprocedure of Miller and Palade ('64) wasfollowed except that whole excretory tubesand not frozen tissue sections were used,and the incubation time in the Gomori me-dium was extended to 25 minutes. Controlswere obtained by omitting the incubationmedium.

Tissue blocks were sectioned using eithera Reichert OmU2 or a MT-l Sorvall"Porter-Blum" ultramicrotome. Both wereequipped with diamond knives. Tissue sec-tions mounted on 200 mesh copper gridswere double stained in saturated uranylacetate in 50% ethyl alcohol (10 minutes),and lead citrate (8 minutes) formulatedaccording to Venable and Coggeshall ('65).Sections were examined with either a Sie-

mens Elmiskop II at 50 kV, or a SiemensElmiskop I-A at 80 kV.

RESULTS

The paired excretory tubes of this miteare about 1.5 mm in length, and vary inwidth from 30 to 270 p..These tubes extendfrom their junction with the rectal bulb toblind endings in the anterior of the bodycavity (fig. 1). Here, they are attached tothe body wall by a small filament of con-nective tissue. The epithelial cells of theexcretory tubes protrude into the lumen.The excretory product, which is present inthe lumen, is visible through the integu-ment of the mite as a white granular sub-stance. This is well illustrated by the photo-micrographs of Rodriguez and Wade ('61)in which the e:;:cretory tubes, appearing asopaque structures, are incorrectly referredto as the gut.

A three dimensional reconstruction of awedge-shaped section of an excretory tubecell is shown in figure 2. A branching mus-cle system surrounds the cell. Each cellmay be divided into three distinct morpho-logical regions: a basal region borderingthe hemocoel and possessing a highly in-folded plasma membrane; next an inter-mediate region; and, bordering the lumenof the excretory tube, an apical region char-acterized by plate-like folds of the plasmamembrane which we term microlamellae.

Fat body sheath and muscle system. Theepithelial cells of the excretory tubes aresurrounded by a muscle system and en-sheathed by fat body. The fat body has astructure similar to that of the fat body ofinsects (Smith, '68). The ensheathment ofthe excretory tubes is only partial, leavinglarge areas of the tubes open to be bathedby the fluid in the body cavity (fig. 3). Incross sections of muscle fibers the sarco-plasmic reticulum and T-tube system aremuch reduced and often absent (figs. 4, 5).The ultrastructure of these muscle fibersresembles the insect visceral muscle fibersdescribed by Smith, Gupta and Smith ('66).Separate circular or longitudinal fiberswere not observed in the muscle systemaround the excretory tubes. Occasionally,both longitudinal and cross sectional pro-files of fibrils within the same muscle fiberwere found. This is suggestive of a branch-ing type of visceral muscle system as in

ULTRASTRUCTURE OF MITE EXCRETORY TUBES 321

the Malpighian tubules of the honeybee(Morison, '27). The visceral muscle systemof the excretory tubes is reconstructed ina diagrammatic fashion in figure 2.

Excretory tube cells. The basal area ofeach epithelial cell rests on a basementmembrane that is about 0.13 fL thick (fig.3). No connective tissue fibers could bedemonstrated and it appears to be com-posed of an amorphous extracellular sub-stance. This area of the cell is dividedinto many compartments by the infoldingsof the plasma membrane (fig. 3). Theseoccur at right angles to the basement mem-brane and extend about one third of thedistance between the outer cell surface andthe lumen of the excretory tube. Often,islets of cytoplasm are created by this com-partmentalization (figs. 4, 5). The infoldedplasma membranes are separated by a dis-tance of about 0.016 fL,except at the cellsurface where the openings have a widerand more variable space. The basementmembrane follows the contour of the cellsurface but does not infold with the plasmamembrane.

The most abundant organelles found inthe cytoplasm are the mitochondria. Theyrange over a wide variety of sizes andshapes. Often, mitochondria are closely as-sociated with the compartments formed bythe infolded plasma membrane (fig. 3). Twodistinct morphological types of mitochon-dria were observed. The type most com-monly encountered were normal in appear-ance, having a uniformly electron densematrix and well developed cristae. Lesscommonly, mitochondria with an alteredstructure were observed. These were dis-tributed throughout the length of the tubes.Within individual cells the altered mito-condria were found in the basal area (fig.4), the intermediate area (fig. 5), and theapical area (figs. 6, 7). They were foundin all areas of the cell where normal-ap-pearing mitochondria are present. Myelin-like figures appear within the matrix ofmany of the altered mitochondria (figs. 4,5, 6, 7). In the immediate vicinity of thesefigures, the matrix is electron lucent. Inmany of these altered mitochondria thecristae are poorly developed and oftenfound only near the periphery of thematrix. Rarely mitochondria with a trans-lucent matrix and somewhat poorly devel-

oped cristae but without the myelin-likeformations were encountered (fig. 5).

Because of the poor sampling powers ofthe techniques associated with electron mi-croscopy, it was not possible to follow anindividual mitochondrion throughout itsstructure. It is possible, therefore, that themitochondria showing only an electron lu-cent matrix actually possess myelin-likefigures. The altered mitochondria are some-what larger than the surrounding mito-chondria.

In the region of the cell between thebasal area and the apical region whichborders the lumen of the excretory tube, alarge oval or spheroid nucleus is found(fig. 5). Other constituents of the cyto-plasm commonly found in this region ofthe cell are vacuolar inclusions, lysosomesand Golgi bodies. The vacuolar inclusionsare bounded by a single membrane (fig. 3).Although they are distributed throughoutthe cell, they are most commonly foundin close association with the compartmentsof the basal area. The contents "of thevacuolar inclusions appear to have beenlost during preparation of the tissue. Thelysosomes are also bounded by a singlemembrane (fig. 9). They most often ap-pear in groups, commonly near the apicalarea of the cell. In tissue assayed foracid phosphatase, the reaction product ap-peared in the lysosomes as a dense pre-cipitate which was most common alongthe limiting membrane (fig. 10). Controlsfailed to show the' reaction product. Be-cause of the difficulty of identifying lyso-somes on the basis of their morphologyalone, this enzyme is used as a marker.Electron dense bodies of varying sizes arefound within the lysosomes. The Golgibodies are not associated with the basal orapical region of the cell, but are foundscattered throughout the area between thetwo regions (figs. 4, 5). Free ribosomesappear throughout the cytoplasm of thecell, and granular endoplasmic reticulum(fig. 5) which is often associated withmi tochondria.

The apical region of the cell, next to thelumen of the excretory tube, has a borderthat consists of flat plate-like folds of theplasma membrane termed microlamellae(figs. 6, 7, 8, 9). Although transverse,longitudinal, and oblique sections through


this area of the epithelial cells werestudied, these folds never showed circularor elliptical profiles characteristic of thefinger-like microvilli. The microlamellaevary in length from about 0.75 0 to 1.50 0'They have a width of about 0.056 0' Somemicrolamellae appear to branch, but prob-ably have a common origin on a raisedarea of tissue that is out of the plane ofsection. Curves are often found along thelength of the longer microlamellae. Thecytoplasm of the microlamellae does notcontain any of the organelles that weredescribed as being present in the rest ofthe cytoplasm. Between many of the mi-crolamellae, small pits are present whichappear to lead back some distance intothe cytoplasm (figs. 6, 7). Rarely, micro-lamellae appear to loop back and join thecell proper (fig. 6).

Cell to cell junctional specialization be-tween the epithelial cells of the excretorytube consist of a tight junction or zonaoccludens (fig. 4). These have a typicalstructure, with an obliterated intercellularspace and a thickened inner leaflet of theplasma membrane. No other type of spe-cialization at the site of cellular junctionwas observed.

Throughout the length of the excretorytubes, no major ultrastructural differenceswere observed. Minor differences do occur,especially where a local accumulation ofthe excretory product results in a disten-sion of the adjacent cells. In these areas,the infoldings of the plasma membranesin the basal region of the cell and the de-velopment of the lamellar border of theapical region of the cell is not as extensive.Although these distended areas are foundall along the excretory tubes, they are mostcommon in the region just prior to thejunction of the tube with the rectal bulb.

Lumen of the excretory tubes. Thelumen of the excretory tubes containsabundant bodies of round, spherical, orrectangular shapes (figs. 11, 12). Fila-mentous strands were sometimes observedin the lumen, and these were associatedwith both the microlamellae and the bodiesfound in the lumen (fig. 11). Often thesebodies failed to infiltrate properly with theplastic embedding media (fig. 12). In thelight microscope, they appear as highlyrefractive particles. They make up the

white granular excretory product the lu-men of the excretory tubes.

DISCUSSION

The ultrastructure of the Malpighiantubules of insects have been the subject ofa number of investigations (refs. in Smith,'68). The excretory organs of differentcrustaceans have also received attentionfrom electron microscopists (Beams, Tah-misian and Devine, '55; Anderson andBeams, '56; Schmidt-Nielsen, Gertz andDavis, '68). Other arthropod groups havenot been as extensively investigated, andto our knowledge, no ultrastructural studyof the excretory organs of mites has beenreported.

Studies to date have shown that arthro-pod excretory organs have in common cellspossessing a basal region with an infoldedplasma membrane, a cytoplasm containinglarge numbers of well developed mitochon-dria, and an apical region having a seriesof complex folds. This general descriptionalso applies to the cells of the excretorytubes of M. muscaedomesticae.

More specifically, the epithelium of theMalpighian tubules of insects have beenfound to be of two types. It may be similar,with only minor differences throughout itslength, as in this mite, or it may be differ-entiated into morphological regions. Thesimple type of epithelium is best seen inthe grasshoppers Melanoplus differentialisdifferentialis (Beams, Tahmisan and De-vine, '55), and Dissoteira carolina (Tsuboand Brandt, '62). The more complex typehaving distinct regions is found in the leaf-hopper Macrosteles fascifrons (Smith andLittau, '60), the immatures of the olivefruit fly Dacus oleae (Mazzi and Baccetti,'63), and the reduviid bug Rhodnius pro-lixus (Wigglesworth and Salpeter, '62). InMacrosteles, three types of cells were foundin four regions of the tubules, while inDacus, four distinct regions were found inthe anterior pair of tubules, but only twodistinct regions in the posterior pair of tu-bules. In Rhodnius, the upper segment ofthe Malpighian tubules has a striated bor-der with closely packed elements, and anapical region in which mitochondria aremuch more abundant than in the rest ofthe cell. The lower segment of the tubuleshas a brush border composed of elements


"

that are more variable in structure andmore widely spaced. Mitochondria in thisarea are more commonly associated withthe basal area of the cell. It is suggested bythese authors that the distribution of mito-chondria reflects the difference in the di-rection of active transport between cells inthe two regions.

In the Malpighian tubules of several in-sects, mitochondria with altered structureshave been reported. Dense homogenousbodies were observed in Macrosteles fasci-frons (Smith and Littau, '60). It was sug-gested that they represent degeneratingmitochondria. Wessing ('62) has describedthe process of mitochondrial degenerationin the cells of Malpighian tubules of larval,pupal and adult Drosophila melanogaster.This process was divided into a number ofstages, one of which was marked by theappearance of lamellar whorls within, themitochondria. These lamellae ultimatelybecome dissolved, and often a mitochon-drion with a nearly homogenous contentresulted. This complex process was mostcommon in the developing stages of thevinegar gnat. Wessing states that thesestages have an increased metabolism.Other investigations on insects that havealtered mitochondria in their Malpighiantubules are discussed below in connectionwith the formation of the excretorygranules.

lntramitochondrial bodies of several dif-ferent types have been reported in a num-ber of kinds of cells from a variety of ani-mals other than insects. Wessing ('62 )gives a number of references and morerecently Suzuki and Mostofi ('67) haveclassified these inclusions with respect totheir structure and localization within themitochondria.

Myelin-like figures within mitochondriahave been reported by a number of workers.The results of their studies have been dis-cussed by Beux, Hetenyi and Phillips ('69),who also studied intramitochondrial mye-lin-like formations in the liver cells ofrats under a variety of experimental con-ditions. While noting that these formationshave been produced under a variety of ex-perimental conditions and are consideredby some workers to indicate mitochondrialregeneration or biogenesis (Beck andGrennawalt, '68; Pannese, '66), Beux et al.

r

believe that myelin-like figures occur nor-mally but are enhanced by such differentstimuli as fasting, glucose infusion andinsulin administration.

It is believed that the altered mitochon-dria found in the excretory tubes of M.muscaedomesticae represent part of a nor-mal process of mitochondrial degeneration.That this process was observed at all isprobably due to the large number of mito-chondria present. It is possible that thesealtered mitochondria are merely artifactsintroduced by the techniques necessary toprepare the tissue for study in the electronmicroscope. Because of the normal appear-ance of the cytoplasm surrounding the al-tered mitochondria, it is difficult to accountfor them as such. In addition, altered mito-chondria were nGt observed in the cells ofother organ systems of this mite. The staticnature of electron microscopy makes analy-sis of dynamic processes difficult. However,in this study, micrographs show thataltered mitochondria exhibit varyingamounts of myelin-like figures. This sug-gests that there are intermediate forms ofthe altered mitochondria and that thechange is a progressive one.

One of the most unusual morphologicalfeatures of the excretory tubes of this miteis the lamellar border of the apical areaof the cell which is made up of flat plate-like microlamellae. A lamellar border, asopposed to a striated or brush border, hasbeen described in the apical area of cellsfrom several organ systems of insects.Smith and Littau ('60) found this type ofborder in two of the four regions of theMalpighian tubules and throughout thehindgut of Macrosteles fascifrons. In theMalpighian tubules, this type of border wasfound in flask-like depressions of the api-cal surface of the cells. In the hindgut,the lamellar border was arranged almostat a right angle to the long axis of thelumen. Mitochondria are found within theindividuallea£lets of the border in the hind-gut but are absent from those of the Mal-pighian tubules.

A lamellar border is also found in theapical area of lipophilic cells in the midgutof Australian sheep blowfly larvae, Luciliacuprina (Waterhouse and Wright, '60). Thisborder most closely resembles that of theexcretory tubes of this mite. The cyto-


plasm of both borders does not containany cellular organelles. Most conspicuousis the absence of mitochondria, a commoncomponent of the cytoplasm of the micro-villae of the Malpighian tubules of insectsand, as noted above, the lamellar borderof the hindgut of Macrosteles fascifrons.Curves are present along the length ofthe microlamellae in the blowfly larvae,and are found in the longer microlamellaein M. muscaedomesticae. The curves aremuch more common and more pronouncedin the blowfly larvae. Neither border hasany pinocytotic vesicles as are found inthe microvillae of the grasshopper Disso-steira carolina (Tsubo and Brandt, '62). Itis believed that these vesicles are involvedin the movement of large molecules acrossthe cell.

The intracellular formation of the ex-cretory granules that are ultimately de-posited in the lumen has been describedin at least two insects. Berkaloff ('58;'59a,b; '60) found that the intracellularformation of globule pigments in thetubules of Gryllus domesticus results fromchanges in the mitochondria. In the lumen,these pigments appear as concentric lami-nated structures. Wigglesworth and Sal-peter ('62) suggest that the mineralizedgranules found in the lumen of the tubulesof Rhodnius prolixus are the results of thebreakdown of mitochondria.

It was not possible to correlate any struc-ture or process of the cells of the excretorytubes of this mite with the formation ofthe granules observed in the lumen. It ismost likely that in this mite the nitrogenous

ET

Fig. 1 Diagramatic representation of the ex-cretory tubes (ET). Numbered circles indicate theposition of the four pairs of legs. Only the rectaltube (RT) and rectal bulb (RB) of the digestivesystem are shown.

wastes pass through the cytoplasm of thecells of the excretory tubes in a solubleform which is changed into the insolublegranules in the lumen.

ACKNOWLEDGMENTS

This research was supported in part byU. S. Public Health Service Researchgrant EC-246 from The EnvironmentalControl Administration, training grant ES-00069 from the National Institute of En-vironmental Health Sciences and by theOffice of Naval Research Department ofthe Navy. This is paper 3278 of the JournalSeries of the North Carolina State Univer-sity Agricultural Experiment Station.

LITERATURE CITED

Anderson, E., and H. W. Beams 1956 Lightand electron microscope studies on the cells ofthe labyrinth in the "green gland" of Cambarussp. Proc. Iowa Acad. ScL, 63: 681-685.

Baker, E. W., and G. W. Wharton 1952 AnIntroduction to Acarology. The Macmillian Co.,New York.

Beams, H. W., T. N. Tahmisian and R. L. Devine1955 Electron microscope studies on the cellsof the Malpighian tubules of the grasshopper(Orthoptera, Acrididae). J. Biophys. Biochem.Cytol., 1: 197-202.

Beck, D. P., and J. W. Greenawalt 1968 Fac-tors affecting the formation of membranousstructures in the cytop-lasm -and mitochondriaof Neurospora crassa. J. Cell BioI., 39: ll-a.

Berkaloff, A. 1958 Les grains de secretion destubes de Gryllus domesticus (Orthopere, Gryl-lidae). C. R. Acad. ScL, Paris, 246: 2.807-2809.

- 1959a Transformations mitochondrialeset formation de pigment dans les tubes de Mal-pighi de Gryllus domesticus (Orthoptere, Gryl-lidae). C. R. Acad. Sci., Paris, 249: 1934-1936.

- 1959b Repartition de la phosphatasealcaline et des grains de secretion dans lestubes de Malpighi de Gryllus domesticus(Orthoptere, Gryllidae). C. R. Acad. ScL, Paris,249: 2120-2121.

- 1960 Contribution a l'excretion ohezles insects. Annis. ScL Nat., 12: 869-942.

Beux, Yvi Le, G. Hetenyi, Jr. and M. J. Phillips1969 Mitochondrial myelin-like figures: a non-specific reactive process of mitochondrial phos-pholipid membranes to several stimuli. Z. Zell-forsch., 99: 491-506.

Brady, J. 1965 A simple technique for makingvery fine durable dissecting needles by sharpen-ing tungsten wire electrolytically. Bull. WId.Health Or., 32: 143-144.

Luft, J. H. 1961 Improvements in epoxy resinembedding methods. J. Biophys. Biochem.,Crytol., 9: 409-414.

Mazzi, V., and B. Baccetti 1963 Ricerche isto-chimiche e -al microscopio elettronico sui tubiMalpighiani di Dacus oleae Gmel. I. La larva. Z.Zellforsch., 59: 47-70.


Miller, F., and G. E. Palade 1964 Lytic ac-tivities in renal protein adsorption droplets. Anelectron microscopical cytochemical study. J.Cell BioI., 23: 519-552.

Morison, G. C. 1927 The muscles of the adulthoney-bee. Part II. The healthy muscles of theadult honey-bee. Muscles of the alimentarycanal, heart, diaphragms, and the reproductiveorgans, and the indirect muscles of the wings.Q. J. Microsc. Sci., 71: 563-651.

Pannese, E. 1966 Structures possibly related tothe formation of new mitochondria in spinalganglion neuroblasts. J. Ultrastr. Res., 15: 57-65.

Pease, D. C. 1964 Histological Techniques forElectron Microscopy. Academic Press, New York.

Rodriguez, J. G., and C. F. Wade 1961 Thenutrition of Macrocheles muscaedomesticae(Acarina: Macrochelidae) in relation to its pred-atory action on the house fly egg. Ann. Entomoi.Soc. Am., 54: 782-788.

Rodriguez, J. G., C. F. Wade and C. N. Wells1962 Nematodes as a natural food for Macro-cheles muscaedomesticae (Acarina: Macro-chelidae), a predator of the house fly egg. Ann.Entomol. Soc. Amer., 55: 507-511.

Schmidt-Nielsen, B., K. H. Gertz and L. E. Davis1968 Excretion and ultrastructure of the an-tennal gland of the fiddler crab Uca mordax.J. Morph., 125: 473-495.

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Smith, D. S. 1968 Insect Cells, Their Structureand Function. Oliver and Boyd, London.

Smith, D. S., B. L. Gupta and U. Smith 1966The organization and myofilament array of in-sect visceral muscles. J. Cell Sci., 1: 49-57.

Smith, D. S., and V. C. Littau 1960 Cellularspecialization in the excretory epithelia of aninsect, Macrosteles fascifrons Stal (Homoptera).J. Biophys. Biochem. CYIol., 8: 103-133.

Susuki, T., and F. K. Mostofi 1967 Intramito-chondrial filamentous bodies in the thick limbof Henle of the rat kidney. J. Cell BioI., 33:605-623.

Tsubo, I., and P. W. Brandt 1962 An electronmicroscopic study of the Malpighian tubules ofthe grasshopper Dissosteira carolina. J. Ultrastr.Res., 6: 28-35.

Venable, J. H., ,and R. Coggeshall 1965 A sim-plified lead citrate stain for use in electronmicroscopy. J. Cell BioI., 25: 407-408.

Waterhouse, D. F., and M. Wright 1960 Thefine structure of the mosaic midgut epitheliumof blowfly larvae. J. Insect PhysioI., 5: 230-239.

Wessing, A. 1962 Die Transformation der Mito-chondrien in den Malpighischen GefaBen vonDrosophila melanogaster. Protoplasma, 55: 294-304.

Wigglesworth, V. B., and M. M. Salpeter 1962Histology of the Malpighian tubules in Rhod-nius prolixus Stal (Hemiptera). J. Insect.Physiol., 8: 299-307.

,

PLATE 1

ULTRASTRUCTURE OF :MITE EXCRETORY TUBESLewis B. Coons and Richard C. Axtell

\.U

328

PLATE 2

EXPLANATION OF FIGURE

3 The basal area of an excretory tube cell which is partially ensheathedwith fat body (FB). The cell rests on an amorphous basement mem.brane (BM). The plasma membrane (PM) of the excretory cell infoldsat right angles to the basement membrane dividing this area of thecell into many compartments. Mitochondria (M) with well developedcristae, and vacuolar inclusions (VI), are closely associated with theinfolded plasma membrane. X 24,000.

326

Abbreviations

BM, basement membraneEP, excretory productER, rough endoplasmic

reticulumET, excretory tubesFB, fat bodyG, Golgi bodiesLu, lumenM, mitochondria

MF, visceral muscle fibersML, microlamellaeN, nucleusPM, plasma membraneRB, rectal bulbRT, rectal tubeTJ, tight junctionVI, vacuolar inclusions

PLATE 1


2 Diagramatic three dimensional representation of a wedge-shaped sec-tion from an excretory tube cell. Visceral muscle fibers (MF), in theform of a branching synctium, invest the cell. A basement membrane(BM) surrounds the muscle system and the basal region of the cell.The plasma membrane (PM) in this region infolds and often thiscreates islets of cytoplasm. Mitochondria (M) are common throughoutthe cell. The apical area of the cell is thrown into a series of plate-like folds or microlamellae (ML) that project into the lumen (Lu)of the tube.

ULTRASTRUCTURE OF MITE EXCRETORY TUBESLewis B. Coons and Richard C. Axtell

PLATE 2

329

330

PLATE 3

EXPLANATION OF FIGURES

4-5 A region showing the basal and intermediate areas of two differentcells of the excretory tube. Large mitochondria (M') are shown whichhave electron lucent matrices and few cristae that are generally re-stricted to the periphery. Myelin-like inclusions are found in two ofthe large mitochondria. Other structures identified in the micrographsare infolding of the plasma membrane (PM), Golgi bodies (G), andmuscle fibers (MF). In figure 4, a tight junction (TJ), and in fig-ure 5, rough endoplasmic reticulum (ER), and part of a nucleus (N)are shown. X 16,000.


PLATE 3

332

PLATE 4

EXPLANATIO'N O'F FIGURES

6-7 A regian shawing the apical area af twO' different cells af the excre-tary tube. Large mitachO'ndria (M') with electran lucent matricesand myelin inclusians are present. A mitachandrian (M) with a typ-ical structure is shawn in figure 6. The mitochO'ndrian in figure 7with the large myelin-like inclusiO'n has few cristae that are generallyrestricted to' the periphery. Micralamellae (ML) are shawn praject-ing intO' the lumen (Lu) af the excretary tube. Small pits (arraws)are present between the microlamellae and appear to' lead same dis-tance back intO' the cytaplasm. In figure 6, ane micralamella (daublearraw) appears to' laap back and jain the cell praper. X 20,000.


PLATE 4

334

PLATE 5


8 High magnification electron micrograph of a gro'-1p of microlamellae(ML) which project into the l'-1men (L'-1). This micrograph illmtratesthe '-1niformity of the cytoplasm and the pa'-1city of cell'-1lar organelleswithin the microlamellae. A mitochondrion (M) is also identified.X 150,000.


PLATE 5

~.

335

11-12

336

PLATE 6

EXPLANATION OF FIGURES

9 Cross-section of an excretory tube cell showing a group of lyso-somes (arrows). Each is bounded by a single membrane and con-tains many round bodies of varying degrees of size and electrondensity. Microlamellae (ML) which make up the border of theapical region of the cell and project into the lumen of the excre-tory tube are also identified. X 20,000.

Electron micrograph showing lysosomes that have a dense precipi-tate of acid phosphatase reaction product. This deposit is mostcommon along the limiting membrane. X 30,000.

10

Electron micrographs of the lumen of the excretory tube showingthe excretory product (EP). In figure 11, filamentous strands (ar-rows) are associated with both the microlamellae (ML) and theexcretory products. Often, as shown in figure 12 (asterisk), theexcretory product fails to infiltrate properly. Figure 11 X 40,000;figure 12 X 20,000.


PLATE 6

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Documents

Ultrastructure of the excretory tubes of the miteMacrocheles muscaedomesticae (Mesostigmata, Macrochelidae) with notes on altered mitochondria