M. C. Parsons.
The Esophageal Valve of Some Aquatic Hemiptera.
Psyche 64(4):135-148, 1957.

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THE ESOPHAGEAL VALVE OF SOME
AQUATIC HEMIPTERA
BY MARGARET C. PARSONS
Harvard Biological Laboratories, Cambridge, Mass. Only two previous comparative studies have been made on the esophageal valves of the aquatic Hemiptera. Sutton (1951) described this region in Sigara fallen! Fieb. and Corixa punctata Ullig, and compared it briefly with the valves of naucorids and notonectids. More recently, Marks (1958) compared the esophageal valves of four species of aquatic 'Hemiptera, representing four different families; Notonecta undulata Say (Notonectidae) , Ranatra fusca P.B. (Nepidae), Belostom flumineurn Say (Belostomati- dae) , and Hesperocorixa escheri (Heer) (Gorixidae) . In the present investigation, the valves of the first three species of Marks were studied. The Corixidae used were Sigara ornata (Abbt.) and Hesperocorixa interrupts (Say) ; Pelocoris fernoratus P.B., representing the family Naucoridae, was also examined. Both transverse and longi- tudinal serial sections through the valve were employed, the digestive tracts being fixed in aqueous Bouin's, alcoholic Bouin's, Held's, and Zenker's fluids and sectioned by the paraffin method. The stains most commonly used were Mallory's triple connective tissue stain, Mallory's phospho- tungstic acid hematoxylin, and Delafield's hematoxylin and eosin.
The purposes of the present paper are (1) to compare the esophageal valve of Pelocoris with that of the other aquatic Cryptocerata, and (2) to offer a few comments on the works of Sutton (1951) and Marks (1958). I wish to thank Mr. Edwin P. Marks and my husband, Dr. Thomas S. Parsons, for their valuable suggestions in connection with this problem. The research was carried out partly during the tenure of a National Science Foundation Predoctoral Fellowship and partly under the Ellen C. Sabin Fellowship, awarded by the American Association of Uni- versity Women.




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136 Psyche [December
THE ESOPHAGEAL VALVE OF
PELOCORIS FEMATORUS P.B.
Figure A and Text-figure 2 show the general structure of the Pelocoris esophageal valve. The invagination consists of two layers of foregut epithelium, an inner and an outer one, which are continous with each other. The cells of the outer layer are somewhat taller than those of the inner one. In most of the specimens e~a~ined, the two layers are contiguous, but a few individuals show a small intra- valvular space between them. Such intravalvular spaces contain fine connective tissue fibrils, but never muscle. The cells of the outer cell layer become taller at the an- terior limit of the invagination, where they gradually merge with the annular cells, a ring of tall cells encircling the foregut-mlidgut junction. This corresponds to the "terminal pad" of cells described by Marks in other water bugs, and will be discussed later. The annular cells, like those of the invagination, have basally located nuclei, and are covered by a cuticular intima which is continuous with that of the esophagus. The intima adheres closely to the annular cells, but is pulled away from the epithelium of the invagination to form a definite "entonnoir" (Aubertot, 1934), similar to, although not as pronounced as, that of the Corixidae. The entonnoir and the cells of the invagination are usually connected by fine strands of cuticula which run from the entonnoir to the spaces between the cells. The cells at the posterior tip of the invagination usually contain, at their apical ends, large vacuoles. Such vacuoles occur less frequently in the more anteriorly located cells of the inner and outer cell layers or in the annular cells. Their presence appears to be connected with the secretion of the intima, since in many cases they seem to be passing from the cells into the space between the epithelium and the entonnoir .
EXPLANATION OF PLATE 12
Figure A. Photomicrograph of the esophageal invagination of Pelocoi- is jemoratus. See Text - figure 2 for explantion. Held's, Delafield's hema- toxylin and Eosin Y. 225 X. Figure B. Photomicrograph of the annular cell region of Sigara ornata. See Text - figure 3 for orientation. Aqueous Bourn's, Delafield's hematoxylin and Eosin Y. 600 X.



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138 Psyche [December
Vacuoles similar to these may be seen in the cells at the tip of the invagination in Hesperocorixa and Sigara, but they are rarely found in Belostoma, Notonecta, or Ranatra. This suggests that they may be associated with the pulling away of the cuticula to form the entonnoir, a phenomenon found in corixids and in FeZocoris but not in the other three bugs. Vacuolated cells have been described in the esophageal valves of Ptychoptera contaminata (van Gehuchten, 1890), and in two species of aphids (Weber, 1928, and Miller, 1932), all of these having a cuticula which is somewhat separated from the cells of the invagination. Sutton, after examining Naucoris cimicoides, concluded that there are two "varieties" of that species. The first of these, she stated, has a "long o'esophageal valve" (Sutton, 1951, p. 489; she did not say how long), with a shorter entonnoir than that found in corixids, and possesses a de- finite corixid-like "proventriculus". The latter term is mis- leading, since it has been used by some authors to designate the "gizzard" of the foregut; in the present study, the "proventriculus" of Sutton, which is part of the midgut, will be called the "perivalvular region". In corixids it sur- rounds the esophageal invagination (Text-fig. 3), and is narrower in diameter than the more posterior part of the midgut, from which it is separated by a constriction. No such perivalvular region was found in any of the naucorids examined in this study.
Sutton found a second "variety" of Naucoris cimicoides in which there is no distinct perivalvular region and the esophageal valve is reduced to a vestige. In Pelocoris, all the esophageal invaginations appeared to be equally prom- inent. Whether Pelocoris is more similar to the first "va- riety" or the second "variety" of N. cimicoides cannot be definitely determined, since Sutton did not include illustra- tions of the valves of both of these; the lack of a differen- tiated perivalvular region in Pelocoris, however, suggests that it more closely resembles the second "variety". This theory is supported by the conclusion of Marks (in press) that the food pump of Pelocoris bears more similarity to the second "variety" of N. cimicoides than to the first.



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l9s7I Parsons - Esophageal Valve in Hemiptera 139 NOTES ON THE ESOPHAGEAL VALVE OF
Since Marks' description of the histology of the crypto- cerate esophagus was brief, a few additional observations may be mentioned here. The epithelium' consists, as that author has stated, of a single layer of cuboidal cells, with an inner cuticular intima. It is surrounded by an inner circular and an outer longitudinal layer of muscle. The present investigation has shown that the histology of the corixid esophagus differs somewhat from that of Belostoma, Ranatra, and Notonecta. The intima in the latter three adheres fairly closely to the esophageal cells; it gen- erally has a scalloped appearance in section, the scallops more or less corresponding to the individual cells which secrete it. In these three bugs, the esophageal epithelium is usually quite folded, the folds projecting into the lumen. In Sigara and Hesperocorixa, on the other hand, the epithe- lium is less folded and the intima is pulled away fr$om the cells, lying free and much folded in the lumen of the eso- phagus. In many preparations, the cells appear to be se- creting additional layers of intima beneath the ones which fill much of the lum'en.
It has been shown by other authors (Hungerford, 1917; Griffith, 1945; Sutton, 1951) that the corixids ingest particulate matter. In this respect they differ from the other Hemiptera, which, as far as has been demonstrated, take in only fluids. It may be that the pulling away of the esophageal cuticula and the secretion of additional layers beneath it is a protective phenomenon, shielding the epithe- ilum fr'om abrasion by particles.
The histology of the esophagus of Pelocoris resembles that of the fluid-feeding water bugs rather than that of the corixids. Although Sutton found that Naucoris cimzcoides was able to ingest solid food, no particulate matter was observed in any of the Pelocoris guts in the present study.



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ÌÔ\Ì JNTIMA OF ESOPHAGI.
CELL LAYER
CELL LAYER
Fig. 1. Diagram of the esophageal invagination of Belostoma fiumih- eum. Heavy stippling indicates annular cell region; light stippling in- dicates rest of foregut epithelium; shading indicates midgut epithelium. Muscle is omitted except for that of the sphincter. 300X. Fig. 2. Diagram of the esophageal invagination of Pelocoris fernoratus. Legend same as for Text - figure 1. 375X.



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l9571 Parsons - Esophageal Valve in Hemiptera 141 1. Location of the Muscle
In their studies of the esophageal valve of corixids, both Sutton and Marks described circular muscle strands within the intravalvular space of the invagination. In the present study, muscle was absent in this area in all 36 corixids exa- mined. The muscle is limited to a strongly dteveloped sphinc- ter at the point where the esophagus enters the midgut (Text-fig. 3) and a l'ess well developed longitudinal layer overlying this sphincter.
It is the author's belief that the "muscle strands" of Sutton and Marks were only fine connective tissue fibers; these are very comlmon in the subepithelial tissue of the gut, and appear to run between the basement membrane of the epithelium and the ~ar~olernma 'of the muscle. Such fibers have been described in the connective tissue sur- rounding the gut of other insects (Rengel, 1896; Nazari, 1899; Leger and Duboscq, 1902). In the corixids, these connective tissue fibers, along with small tracheoles, pen- etrate the intravalvular space of the esophageal invagina- tion, and may quite easily be mistaken for muscle strands (Mr. Marks has examined my material, and agrees with this conclusion).
2. The Annular Cells
In all five bugs, the junction of the foregut and midgut is encircled by a ring of tall foregut cells. These correspond to the "terminal pad" of Marks, who showed them in his figures of Hesperocorixa, Belostoma, Ranatra, and Noton- ecta. Sutton apparently mistook them for midgut cells, as Marks has pointed out.
Text-figure 3 shows the location of the annular cells in Sigara and Hesperocorixa. The annular cell region in cor- ixids is more extensive than Marks' figures (1958, his plate VII, figures 1, 3, and 4) would indicate; the author has examined Marks' slides, and ftound that this region showed some distortion in his material, which probably accounts for this difference.
The most outstanding feature of the annular cells, which was overlooked by both Sutton and Marks, is their high



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142 Psyche
[December
mitotic rate. This is particularly evident in the corixids; one specimen of Sigara ornata showed 181 mitoses in the an- nular cell region. Figure B shows a detail of the annular cells in this specimlen. Mitoses are nlot nearly as frequent in the annular cells of representatives of the other four fami- lies, although Table 1 (below) shows that some amount of cell division is always present.
TABLE 1
A B C
Notonecta undzdata 28 5 3
Ranatra f usca 17 3 8
Pelocoris f emoratus 21 4 6
Belostoma f lumineum 24 11 14
Hesperocorixa int errupta
and Sigara ornata 36 28 181
Frequency of mitotic figures observed in the annular cell region. Column A, number of valves examined; Column B, number of valves showing mitoses in annular cell region; Column C, maximum number of mitoses seen in any one valve.
It is difficult to account for this high mlitotic rate in corixids. Verson (1897) reported that in the silkworm, cell division in this region adds to the cells of the esopha- geal valve. However, degenerating cells are rarely observed within the esophagus or the 'esophageal invagination of cor- ixids, and there appears to be no real need for such frequent cell addition. The location of the annular cells corresponds to that of the imaginal disc which regenerates the f'oregut of nymphs after a moult; it may be that the annular cells are remnants of this highly active nymphal region, which retain their high mitotic rates.
3. Comparative Aspects
In his study of the esophageal valves of four species of water bugs, Marks described a sequence of increasing com- plexity in the following order : Notonecta, Ranatra, Belosto- ma, and Hesperocorixa. In general, the present study sup- ports this conclusion.
The valvular action in Notonecta and Ranatra is derived from the circular muscle sphincter which, when it contracts, draws together the tall annular cells. There is no real



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19571 Parsons - Esophageal Valve in Hemiptera 143 invagination in either of these bugs. The valves of Noton- ecta and Ranatra appear, to the author, to be equally simple, although Marks considered the latter to be symewhat more developed than the former.
The form of the valve in Belostoma is more complex (see Text-fig. 1). Here a shallow invagination is present, which may offer resistance to the passage of material from the midgut into the foregut. Although an inner cell layer is present, there is nothing corresponding to the outer cell layer of Hesperocorixa or Pelocoris; instead, the annular cells occupy the posterior and outer surfaces of the invag- ination.
The Pelocoris valve is more complicated than that of Belostoma, but less so than that of Hesperocorixa and Sigara. In its degree of complexity, therefore, it appears to be an intermediate between these two groups. The invagination is deeper than that of Belostoma but shallower than the invagination of corixids. The presence of an enton- noir indicates another advancement in complexity. In Pel- ocoris an outer cell layer is present, but the annular cell region appears to extend part way into the invaginated area, gradually merging with the tall cells of the outer cell layer (Text-fig. 2) .
The increased length of the invagination, the prominence of the entonnoir, and the placement of the annular cells in the corixid valve make it the most complex of the five. Sutton's assertion that the entonnoir may extend as much as two-thirds of the length of the midgut was not borne out in the present study. The cuticula does extend farther into the midgut than in the other four bugs, but it was never observed to penetrate more than one-tenth the length of the mesenteron in thte material used in the present study. In corixids, the annular cell region never extends into the invagination, as it does in Belostoma and Pelocoris. It is, instead, sharply set off from the outer cell layer, form'ing a distinct region which encircles the area between the ter- mination of the invagination and the beginning of the rnidgut (see Text-fig. 3).
The conclusion of Sutton that the corixid esophageal invagination is long when the midgut contains small



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144 Psyche [December
amounts of food, and either extended or retracted with large quantities, was not supported in the present study. In the four corixids with the shfortest invaginations, the midgut was empty. Sutton's claim that the intravalv~la~ space contains a blood sinus mlay be true, but there is no evidence from the present study to support her theory that the valve takes an active part in moving the food posterior- into the midgnt.
\\
CELL LAYER
INTRAVALVULAR
Fig. 3. Diagram of the esophageal invagination of Sigara ornata or Hesperocorixa interrupts. Legend same as for Text - figure 1. Dotted lines indicate region from which Figure B (Plate 12) was taken. 330X.



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19571 Parsons - Esophageal Valve in Hemiptera 145 Although the increasing complexity of the valve, from Notonecta and Ranatra to the corixids, represents a mor- phological sequence, I, like Marks, will not here attempt to draw any phylogenetic conclusions. In terrestrial Heterop- tera, both simple and complex esophageal valves are rep- resented ; in Oncopeltus fasciatus, the valve resembles that of Notonecta (Hood, 1937), while the esophageal invagin- ation of the cacao capsid bug (Goodchild, 1952) is similar to that of corixids.
4. Sutton's Interpretation of the Significance of the Cor- ixid Esophageal Valve
Suttlon proposed that the complex valve 'of corixids is a primitive feature. This theory was based primarily on her belief that the primitive corixids secreted two kinds of peritrophic membranes, one from the cells of the posterior midgut (the Type I of Wigglesworth, 1950) and a second from the anteriormost midgut cells of the perivalvular re- gion (Wigglesworth's Type 11). Sutton's hypothesis was that modern corixids have lost the second type of mem- brane, but have retained the first type. The latter theory is to be the subject of another paper (Parsons, in press) ; the proposal that corixids once secreted a Type I1 mem- brane will be discussed here, however, since part of Sutton's evidence for this hypothesis is based upon an apparently incorrect interpretation of the nature of the annular cells. When the ancestral corixid secreted a Type I1 peritrophic membrane, according tho Sutton, a long eslophageal invagin- ation was present; this helped to mould the membrane and to move it posterirorly by alternate extension and retraction. The membrane was secreted by the anterior cells of the perivalvular region. In the course of evolution, the latter region has lost its ability to secrete chitin, but it has not yet acquired a digestive function. If any food were to get into this non-functional region, it would only decompose; to prevent this, Sutton claimed, the long esophageal invag- ination has been retained in mocdern corixids. Sutton cited the work of Aubertot
(1934), who, in his
study of the peritrophic membrane in many orders of insects, distinguished a groove or "sillon" which marks the



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146 [Decembsr Psijche
boundary between foregut and midgut. It is from the midgut cells directly posterior to this groove that the Type I1 peritrophic membrane is secreted, and the sillon marks its anteriormost point of insertion. This secretory group of midgut cells, the "massif des cellules-meres de la pkri- trophique" of Aubertot, is histologically distinct from the rest 'of the midgut in somk insects.
ANNULAR CELLS
Fig.
4. Detail of the annular cell region in Sigma ornata. Heavy line indicates the
cuticular intima of the foregut, with which the entonnoh is continuous. Orientation same as that of Figure B (Plate 12) ; the eso- phagus and inner cell layer are not shown. The midgut epithelium is stippled. 850 X.
It appears, however, that Sutton has mistaken the an- nular cells, which are definitely of foregut origin, for mid- gut epithelium, perhaps believing them to represent a "massif". In so doing, she has taken the groove between the annular cells and the esophageal invagination to be the sillon; this appears to be the case in her figure 10. In the present study, however, the intima was seen to cover the annular cells and to end at a point more posteriorly located than the sillon of Sutton's diagram. This area is quite com- plicated in corixids, since the annular cells which are closest to the migut bend inwards, towards the lumen, fborming a whorl. The true sillon lies at the apices of these curved annular cells, and the terminal part of the intima therefore extends up into the whorl (see Text-fig. 4). There is rarely



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19571 Parsons - Esophageal Valve in Hemiptera 147 a distinct groove here, and the sillon is obscured by the
close approximation of the whorl of annular cells with the anteriormost midgut cells.
The evidence cited by Sutton to support her theory of a Type I1 peritrophic membrane in the corixid ancestor appears to be two-fold: the presence of a distinct sillon in about half of her specimens, and the existence of a non- secretory perivalvular region in all of them. The present study casts considerable doubt upon h'er first piece of evi- dence, since the true sillon of corixids is not a distinct groove. Her observation of a non-secretory perivalvular re- gion in corixids was correct, however, and will be discussed in a later paper. Whether or not this is sufficient evidence to support the idea that the corixids once secreted a Type I1 peritr'ophic membrane is difficult to say ; it may be that the lack of a secretory function in this area is due to other causes. Certainly her thelory that the long esophageal in- vaginati,on is a device for keeping food out of this region is open to question; long valves are present in Anasa tristis (Breakey, 1936) and the cacao capsid bug (Goodchild, 1952), neither of which has a non-secretory perivalvular region.
LITERATURE CITED
AVBERTOT, M.
1934. Re,-herc,hcs sur ies p6ritrophiques des insectes et en particulior des Diptcres. Theses: Fac. Sci. Vniv. Strasbourg. BREAKEY, E.P.
1936. Histo!ogica! studies of the digestive system of the squash bug (Anasa tristis DeG. Hcmiptera. Coreidae). Ann. Ent. Soc. Amer.. 29 :561-577.
VAX GEHUCHTEX, A.
1890. Recherches histologiques sur l'appareil digestif de la Ptychop- tera contaminata. 1. Part. Etude du rev6tement bpithbliale et re- cherche~ sur la secretion. La Cellule, 6 : 185-289. GOODCHILD, A.J.P.
1952.
A study of the digestive system of the West African cacao cap- sid bugs. Proc. Zool. Soc. Loud., 122:543-572. GRIFFITH, M.E.
1945.
The environment, life history, and structure of the water boat- man Rhamphocorixa acuminata (Uhler) (Hemiptera. Corixidae) Tniv. Kans. Sci. Bull., 30 :241-365.




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148 Psyche [December
HOOD, C.W.
1937. The anatomy of the digestive system of Oncopeltus fasciatus Dall. (Hemiptera, Lygaeidae). Ohio J. Sci., 37 : 151-160. HUNGERFORD, H.B.
1917. Food habits of corixids. J. New York Ent. Soc., 25 :1-5. LEGER, L. AND 0. DUBOSCQ.
1902.
Les gregannes et 1'6pith6lium intestinal chez leg tracheates. Arch Parasit., 6 : 377-473.
MARKS, E.P.
1958.
A comparative study of the foregut of several aquatic Hemiptera, J. Kans. Ent. Soc., 31 :138-153.
In press. The food pump of Pelocoris, and comparative studies on othei aquatic Hemiptcra. Psyche, 64 (4).
MILLER, F.W.
1932. The digestive epithelium of the aphid, Macrosiphum sanbornii. Proc. Penn. Acad. Sci., 6 : 148-151.
NAZARI, A.
1899. Richerche sulla struttura del tubo digerente e sul process0 di- gestivo del Bombgx mori a110 stato larvale. Rip. Laboi. Anat Roma, 7 :75-84.
PARSONS, M.C.
In press.
The presence of peritrophic membrane in some iiquatic Hcmip- tera. Psyche, 64 (4).
RENGEL, C.
1896.
Uber die Veriindorungen des Darmepithels bei Tenebrio dtor. wahrend der Metamorphose. Zeitschr. Wiss. Zool., 62 : 1-60. SUTTON, M.F.
1951. On the food, feeding mechanism and alimentary canal of Corixi- dae (Hemiptera, Heteroptera). Proc. Zool. Soc. Lond., 121 :465-499. VERSON, E.
1897. La evoluzione del tubo intestinale del filugello. Atti R. 1st. Ven- eto Sci. Lett. Arti.. (7) 8:917-956.
WEBER, H.
1928. Skelett, Muskalatur und Darm der schwarzen Blattlaus Aphis fabae Scop. mit besonderer Beriicksichtigung der Funktion der Mundwerkzeuge und des Darms. Zoologica (Stuttgart) , 28 : (76) : 1-120. WIGGLESWORTH, V.B.
1950. The Principles of Insect Physiology. 4th ed. ev. Methuen, London.




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