F. H. Butt.
The Origin of the Peritrophic Membrane in Seiara and the Honey Bee.
Psyche 41(2):51-56, 1934.

This article at Hindawi Publishing: https://doi.org/10.1155/1934/91817
CEC's scan of this article: http://psyche.entclub.org/pdf/41/41-051.pdf, 820K
This landing page: http://psyche.entclub.org/41/41-051.html

The following unprocessed text is extracted automatically from the PDF file, and is likely to be both incomplete and full of errors. Please consult the PDF file for the complete article.

PSYCHE
VOL. XLI JUNE 1934 No. 2
THE ORIGIN OF THE PERITROPHIC MEMBRANE
IN SCIARA AND THE HONEY BEE
BY F. H. BUTT
Cornell University.
Many explanations have been given for the origin of the peritrophic membrane.
Some authors maintain that it is
formed from secretions of the epithelial cells of the mid-in- testine and is non-chitinous in structure. Others think it is a continuation of the chitinous intima lining the oesopha- gus and is secreted by cells lying at the junction of the fore and mid-intestine. No investigation has been made of its origin in the embryo.*
Recently while making an embryological study of Sciara I was interested in the extreme length attained by the sto- modaeal membrane in the later stages. It so resembled the peritrophic membrane of the larva both in its position and in its point of attachment that a relationship between the two was immediately evident. Therefore a number of newly emerged larvse were killed and sections were made to see if a, peritrophic membrane were present in the very first stage, and if so, whether it had any resemblance to the stomodseal membrane in the embryo. The larvae were fixed in Carnoy-LeBrun fluid for thirty seconds and were em- bedded in rubber-paraffin. The sections were cut at four microns, were stained in magenta and counter-stained in picro-acid-carmine.
*Since this paper was submitted for publication, a paper by Gam- brell has appeared (Ann. Ent. Soc. Am. Vol. XXVI:641) mentioning the origin of the peritrophic membrane in Simuliium. Pu&e 415 1-56 (1934). hup ttpsychu einclub orgHit41-05i.html



================================================================================

52 Psyche [June
In the embryo, the stomodaeum begins as a shallow de- pression in the ectoderm at the anterior end shortly after the thirtieth hour, coincident with the beginning of seg- mentation. As it deepens, it forms a tube closed at its inner end by ectodermal cells (fig. 1). These cells become thin- ner as the end of the tube widens until at the sixty-fifth hour the tube is closed at its inner end by a thin membrane in which no nuclei are present. Between the sixty-fifth and the seventieth hours the end of the stomodseum flattens and spreads out.
At the same time the stomodseal mem-
brane increases in size and hangs loosely in the yolk. The stomodaeum now resembles an, inverted hollow mushroom, the membrane forming the outline of the cap (fig. 2). As the stomodseum continues to grow, the flattened end folds back on itself so that the mesodermal layer (m) surround- ing the stomodseum lies between two layers of ectoderm (fig. 3).
The stomodasal membrane hangs loosely in the yolk and steadily increases in size, not as the result of cell prolifer- ation but apparently by secretions from differentiated cells located on the end of the recurved stomodseum where it joins the mid-intestine (fig. 2, stom m c). These cells are elongated, with their extremities drawn out very thin where the substance of the stomodseal membrane is given off. At the eightieth hour only a few secretory cells are to be seen. They increase in size and in number between the eightieth and ninetieth hours until they form a very conspicuous mass around the stomodaeum (fig. 3). In the meantime the mem- brane (stom m) has lengthened. The muscular wall of the fore-intestine, lying between the two layers of ectoderm of the stomodasum, is still thin. Figure three represents the stomodasum at ninety hours, shortly before the larva emerges from the egg. The walls' of the mid-intestine at this time are complete.
Between the ninetieth hour in the egg, and the time the hatched larva is ready to feed, the appearance of the stomo- dseum changes considerably (fig. 4). The sack-like stomo- dseal membrane becomes the tube-shaped peritrophic mem-



================================================================================

19341 Peritro phic Membrane in Sciara 53 Psyche, 1934
VOL. 41, PLATE 4
Butt-Peritrophic Membrane in Sciara
Ì




================================================================================

54 Psyche [June
brane probably when the first food breaks through the sack on its passage down the intestine. The muscular wall (m) of the oesophagus (oes) that was a simple layer of cells at the ninetieth hour (fig. 3), expands into a bulb-like ring at the end of the oesophageal valve. Inside this ring is an open space which Wigglesworth (30) calls a blood sinus (bl s). This muscle with its blood sinus is a sphincter which, when expanded, closes off the mid-intestine to the entrance of food. When contracted, the passageway through the oeso- phageal valve is open. The ectodermal cells, lining the sto- rnodasum, that were so large in the embryo, have thinned out and disappeared over the end of the bulbous ring, their place being taken by a thin membrane, the chitinous intima (c in). The cells secreting the peritrophic membrane (p c) which have now assumed a very regular appearance with smooth inner and outer walls, are very large and vacuolated. At the sides of the mid-intestine lie the two gastric ceca (coec) which discharge their contents into the intestine near the oesophageal valve. Their contents are prevented from bathing the oesophageal valve by the peritrophic mem- brane (m) which is forced together by the fluid and ex- tends down into the mid-gut.
Nelson ('15) states that the stomoda~um in the honey-bee is closed at its inner end by cells of the anterior mesenteron rudiment. He does not mention any embryonic origin for the peritrophic membrane. Snodgrass ('25) refers to Nel- son in regard to the stomodseal membrane and says, "the old idea that the peritrophic membrane of insects is a back- ward prolongation of the chitinous intima of the proventri- culus has been discredited in all recent investigations on its origin." He finds that it is formed in the adult bee from protoplasmic bodies given off from the epithelial cells of the mid-intestine. These fill' in the granular layer. Wig- glesworth ('30) is of the opinion that the peritrophic mem- brane is of two-fold origin: a chitinous basis, secreted at the anterior end of the mid-gut and a series of indefinite membranes which condense on the outside of this as it pro- ceeds down the gut. Having access to some slides of the fr




================================================================================

19341 Peritrophic Membrane in Sciara 55
honey-bee embryo, I was interested to see if there were any possible embryonic fore-runners of the peritrophic membrane.
An examination of the slides indicated that the stomo- dseal invagination forms in the same manner as in Sciara. The cells in the floor of the invagination are a continuation of the ectoderm which forms the walls of the tube. The tube lengthens and widens at the end, thle floor being re- duced to a thin membrane similar to that described above for Sciara. Late in the embryonic stage the inner walls of the stomodseum protrude into the mid-intestine rupturing the membrane. Around this invaginating tube lies a thick- ened ring of cells that resembles the ring of cells secreting the stomodseal membrane in Sciara. It also corresponds to the basal folds of the mid-gut as figured by Wigglesworth ('30) from which, he says, originates part of thle peri- trophic membrane. Campbell ('29) has demonstrated the presence of chitin in the peritrophic membrane which is further proof that it arises from the ectoderm. A study of
the first stage larva would undoubtedly yileld more evidence but no larvae were available at the time this study was being made.
Summary
An examination of the cesophageal valve in both the em- bryological and the early larval stages of Sciara indicates that the peritrophic membrane is a continuation of the stomodssal membrane and is iectodermal in origin. It arises from a group of large secretory cells lying around the ceso- phageal valve and attached to the upper edge of the mid- '
intestine. These cells which are also ectodermal in origin, begin their development from the end of the stomodseum as it widens out and revlerses its direction of growth. The large bulbous muscular layer of the oesophagus which en- closes the blood sinus, develops from the single layer of mesoderm which surrounds the stomodseum. In the honey-bee the formation of the stomodseum re- sembles the development in Sciara except that the stomo- dseal membrane does not attain such a great length but is



================================================================================

56 Psyche [June
broken when the innler end of the stomodseum pushes through. The peritrophic membrane, as described by Wig- glesworth, is chitinous and arises from a mass of cells cor- responding in position to the base of the stomodseum in the embryo.
This indicates that the peritrophic membrane is ectodermal in origin.
Campbell, I?. L. 1929. The detection and estimation of in- sect chitin; and the irrelation of chitinization to hard- ness and pigmentation of the cuticula of the American cockroach, Periplaneta americana L., Ann. Ent. Soc. Am., Vol. 22, pp. 401-426.
Nelson, J. A. 1915. The embryology of the honey-bee, Princeton University Press, pp. 1-282.
Snodgrass, R. E. 1925. Anatomy and physiology of the honey-bee. McGraw Hill Book Co., New York, pp. 1-327.
Wigglesworth, V. B. 1930. The information of the peritro- phic membrane in insects with special reference to the larvae of mosquitoes. Quart. Jour. Mirc. Sc., Vol. 73, Part IV, pp. 593-616.




================================================================================